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Chen Y, Tong E, Rao Y, Yu EYW, Zeegers M, Wesselius A. The association between insomnia (related symptoms) and glycaemic control: a systematic review and meta-analysis. J Glob Health 2025; 15:04016. [PMID: 39916567 PMCID: PMC11803432 DOI: 10.7189/jogh.15.04016] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 02/11/2025] Open
Abstract
Background Insomnia characterised by difficulties in falling asleep and maintaining sleep, and early awaking, is a prevalent worldwide sleep disorder. While previous studies have suggested an association between insomnia and adverse glycaemic control, the evidence remains inconclusive. Therefore, this meta-analysis aims to explore this association. Methods Insomnia was assessed based on defined criteria, including related symptoms such as poor sleep quality and low sleep efficiency. Glycaemic control was evaluated using indicators such as fasting plasma glucose, haemoglobin A1c, and the presence of diabetes. A literature search was performed in PubMed, Web of Science, and Scopus. The quality of the included studied was assessed using The Newcastle-Ottawa Scale. Effect sizes, including odds ratio, relative risk, mean difference, and standard mean difference, were chosen based on data type. Forest plots visually displayed pooled effect sizes and corresponding 95% confidence intervals, while the I2 test calculated heterogeneity. Meta-regression and subgroup analysis explored potential sources of heterogeneity. Leave-one-out sensitivity analysis assessed result robustness, and Begg's and Egger's tests evaluated publication bias. Results Ninety-one articles, comprising 84 are cross-sectional studies, (five are case-control studies, and two are cohort studies) with 2 217 521 participants, were included. Ten separate meta-analyses were conducted based on variable type (binary/continuous), study design (cross-sectional, case-control, or cohort), and measurement of exposures/outcomes. All meta-analyses indicated a positive association between insomnia (related symptoms) and adverse glycaemic control. However, three meta-analyses showed significant heterogeneity, and three lacked robustness. No publication bias was detected across any of the analyses. Conclusions Insomnia is likely associated with adverse glycaemic control. As the included studies are observational, future research should prioritise diverse methodologies and robust study designs to further explore this complex relationship. Keywords insomnia, insomnia related symptoms, glycaemic control, systematic review, meta-analysis. Registration PROSPERO CRD42024491688.
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Affiliation(s)
- Yiming Chen
- School of Nutrition and Translational Research in Metabolism, Maastricht University, Maastricht, Limburg, the Netherlands
- Department of Epidemiology, Maastricht University, Maastricht, Limburg, the Netherlands
| | - Enyu Tong
- Department of Health, Ethics and Society, Maastricht University, Maastricht, Limburg, the Netherlands
| | - Yufeng Rao
- School of Nutrition and Translational Research in Metabolism, Maastricht University, Maastricht, Limburg, the Netherlands
- Department of Epidemiology, Maastricht University, Maastricht, Limburg, the Netherlands
| | - Evan YW Yu
- Key Laboratory of Environmental Medicine and Engineering of Ministry of Education, and Department of Epidemiology & Biostatistics, School of Public Health, Southeast University, Nanjing, Jiangsu, China
| | - Maurice Zeegers
- Department of Epidemiology, Maastricht University, Maastricht, Limburg, the Netherlands
| | - Anke Wesselius
- School of Nutrition and Translational Research in Metabolism, Maastricht University, Maastricht, Limburg, the Netherlands
- Department of Epidemiology, Maastricht University, Maastricht, Limburg, the Netherlands
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Agnoletto L, Vandeleur M, White M, Adams A, Halligan R, Peters H. Sleep quality in children with hepatic glycogen storage diseases, a prospective observational pilot study. JIMD Rep 2025; 66:e12462. [PMID: 39723121 PMCID: PMC11667772 DOI: 10.1002/jmd2.12462] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Figures] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 07/24/2024] [Revised: 10/16/2024] [Accepted: 11/20/2024] [Indexed: 12/28/2024] Open
Abstract
Background Hepatic glycogen storage diseases (GSDs) are characterised by enzyme defects affecting liver glycogen metabolism, where carbohydrate supplementation to prevent overnight hypoglycaemia is common. Concerns around sleep quality in hepatic GSDs relate to emerging evidence that overnight dysglycaemia impacts sleep quality. Methods This prospective observational study reported sleep quality and duration in children with hepatic GSDs over 7 days utilising: actigraphy (Actiwatch 2 by Phillips Respironics), sleep diaries, proxy reported age-appropriate sleep and quality-of-life (QoL) questionnaires, in the context of nocturnal glycaemic profiles continuous glucose monitor (CGM, Dexcom G6) and nocturnal dietary management strategies. Significant hypo- and hyperglycaemia were defined as ≥1% of sleep diary documented nocturnal period, recording <3.5 and >10.0 mmol/L, respectively. Results Seven children with hepatic GSD (aged 1-17 years) participated. Objective sleep quality was poor, with actigraphy demonstrating that no child achieved the minimum sleep duration recommended for age. Subjective sleep quality was also poor, with 4/5 documenting significant daytime sleepiness and 6/6 reporting poor sleep hygiene. Children prescribed overnight bolus feeds (OBF) (n = 2) recorded shorter sleep duration compared to other nocturnal management strategies. Parent-reported QoL suggested poor disease-related QoL outcomes for this cohort. Conclusion Objective and subjective sleep disturbances and reduced QoL are common within our sample of children with hepatic GSD. From our observations these outcomes may be linked to nutritional overnight interventions, especially OBFs, rather than overnight glucose levels. Consideration of the impacts of overnight feeding strategies on sleep quality and QoL in children with hepatic GSD should inform future management strategies.
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Affiliation(s)
- Lucas Agnoletto
- Murdoch Children's Research InstituteMelbourneVictoriaAustralia
- Department of PaediatricsUniversity of MelbourneMelbourneVictoriaAustralia
| | - Moya Vandeleur
- Murdoch Children's Research InstituteMelbourneVictoriaAustralia
- Department of Respiratory and Sleep MedicineRoyal Children's HospitalMelbourneVictoriaAustralia
| | - Mary White
- Murdoch Children's Research InstituteMelbourneVictoriaAustralia
- Department of Endocrinology and DiabetesRoyal Children's HospitalMelbourneVictoriaAustralia
- Melbourne School of Global and Population Health, University of MelbourneMelbourneVictoriaAustralia
| | - Anne‐Marie Adams
- Murdoch Children's Research InstituteMelbourneVictoriaAustralia
- Department of PaediatricsUniversity of MelbourneMelbourneVictoriaAustralia
- Department of Respiratory and Sleep MedicineRoyal Children's HospitalMelbourneVictoriaAustralia
| | - Rebecca Halligan
- Department of Metabolic MedicineRoyal Children's HospitalMelbourneVictoriaAustralia
- Department of Inherited Metabolic DiseasesEvelina London Children's HospitalLondonUK
| | - Heidi Peters
- Murdoch Children's Research InstituteMelbourneVictoriaAustralia
- Department of PaediatricsUniversity of MelbourneMelbourneVictoriaAustralia
- Department of Metabolic MedicineRoyal Children's HospitalMelbourneVictoriaAustralia
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İpar N, Boran P, Barış HE, Us MC, Aygün B, Haliloğlu B, Gökçe T, Can E, Eviz E, İnan NG, Mutlu GY, Bereket A, Hatun Ş. Associations between sleep characteristics and glycemic variability in youth with type 1 diabetes. Sleep Med 2023; 109:132-142. [PMID: 37437493 DOI: 10.1016/j.sleep.2023.06.018] [Citation(s) in RCA: 3] [Impact Index Per Article: 1.5] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 04/19/2023] [Revised: 06/15/2023] [Accepted: 06/18/2023] [Indexed: 07/14/2023]
Abstract
OBJECTIVE This study aimed to determine sleep characteristics and their associations with glycemic variability in youth with type 1 diabetes (T1D). MATERIAL AND METHODS This cross-sectional study conducted at two pediatric diabetes centers in Istanbul, Turkey, included 84 children with T1D (mean age 10.5 years). Sleep characteristics and glycemic variability were determined by actigraphy, DSM-5 Level 2-Sleep Disturbance Scale Short Form and continuous glucose monitoring. Circadian preference was evaluated by the Children's Chronotype Questionnaire. Sleep disturbances were assessed by the. The sleep quality was determined by actigraphy-derived sleep measures. RESULTS Eighty-eight percent of participants had insufficient age-appropriate total sleep time (TST) (<9 h for 6-13-year-olds and <8 h for 14-17-year-olds). Chronotype was classified as intermediate in 50%, evening in 45.2%, and morning in 4.8%. A higher chronotype score indicating a stronger eveningness preference was associated with more time spent in hypoglycemia (β = 0.433, p = 0.002). On nights when participants had lower sleep efficiency and longer sleep onset latency, they had significantly higher overnight glycemic variability (β = -0.343, p = 0.016, β = 0.129, p = 0.017, respectively). Prolonged nocturnal wake duration was significantly associated with more time spent in daytime hypoglycemia (β = 0.037, p = 0.046) and higher overnight glycemic variability (J index, β = 0.300, p = 0.015). The associations between TST and glycemic variability indices were not significant. CONCLUSIONS Sleep quality rather than TST was significantly associated with glycemic variability in children with T1D. Eveningness preference might contribute to an increased risk of hypoglycemia. Addressing sleep patterns and chronotypes can be crucial in management plans for youth with T1D.
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Affiliation(s)
- Necla İpar
- Institute of Health Sciences, Social Pediatrics PhD Program, Marmara University, Istanbul, Turkey; Department of Pediatrics, Koc University School of Medicine, Istanbul, Turkey.
| | - Perran Boran
- Institute of Health Sciences, Social Pediatrics PhD Program, Marmara University, Istanbul, Turkey; Department of Pediatrics, Division of Social Pediatrics, Marmara University School of Medicine, Istanbul, Turkey.
| | - Hatice Ezgi Barış
- Institute of Health Sciences, Social Pediatrics PhD Program, Marmara University, Istanbul, Turkey; Department of Pediatrics, Division of Social Pediatrics, Marmara University School of Medicine, Istanbul, Turkey.
| | - Mahmut Caner Us
- Institute of Health Sciences, Social Pediatrics PhD Program, Marmara University, Istanbul, Turkey.
| | - Burcu Aygün
- Institute of Health Sciences, Social Pediatrics PhD Program, Marmara University, Istanbul, Turkey.
| | - Belma Haliloğlu
- Department of Pediatrics, Division of Pediatric Endocrinology, Marmara University School of Medicine, Istanbul, Turkey.
| | - Tuğba Gökçe
- Department of Pediatrics, Division of Pediatric Endocrinology, Koç University School of Medicine, Istanbul, Turkey.
| | - Ecem Can
- Department of Pediatrics, Division of Pediatric Endocrinology, Koç University School of Medicine, Istanbul, Turkey.
| | - Elif Eviz
- Department of Pediatrics, Division of Pediatric Endocrinology, Koç University School of Medicine, Istanbul, Turkey.
| | - Neslihan Gökmen İnan
- College of Engineering, Department of Computer Engineering, Koc University, Istanbul, Turkey.
| | - Gül Yeşiltepe Mutlu
- Department of Pediatrics, Division of Pediatric Endocrinology, Koç University School of Medicine, Istanbul, Turkey.
| | - Abdullah Bereket
- Department of Pediatrics, Division of Pediatric Endocrinology, Marmara University School of Medicine, Istanbul, Turkey.
| | - Şükrü Hatun
- Department of Pediatrics, Division of Pediatric Endocrinology, Koç University School of Medicine, Istanbul, Turkey.
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Cho MK, Kim MY. Associated factors with depression and sleep quality in T1DM patients: a cross-sectional descriptive study. BMC Psychiatry 2023; 23:18. [PMID: 36624402 PMCID: PMC9830728 DOI: 10.1186/s12888-023-04516-2] [Citation(s) in RCA: 5] [Impact Index Per Article: 2.5] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 08/09/2022] [Accepted: 01/02/2023] [Indexed: 01/11/2023] Open
Abstract
BACKGROUND Individuals with type 1 diabetes (T1DM) may experience sleep problems, usually due to low blood sugar levels during sleep or performance of blood sugar management (e.g., blood sugar monitoring). This study aimed to identify the disease-related characteristics, psychosocial aspects, and related factors underlying sleep quality in patients with T1DM. METHODS This study employed a descriptive research design. The participants were 159 individuals with T1DM who completed online questionnaires. The data were analyzed using descriptive statistics, correlations, and multiple regression analyses. RESULTS The average score for depression in T1DM patients was 23.77 (SD 5.31), and sleep quality received a score of 4.58 (SD 3.22). Depression was positively correlated with sleep quality and negatively correlated with the total resilience score. The factors linked to depression in T1DM patients were duration of disease, sleep latency, sleep duration, sleep disturbance, and resilience-acceptance of self and life sub-factors, with an explanatory power of 44.4% for the depression variance. The associated factors with sleep quality in T1DM patients were complications, resilience-personal competence sub-factors, and depression, with an explanatory power of 37.4% for sleep quality variance. CONCLUSIONS The results of this study suggest that to improve sleep quality in patients with T1DM, it is necessary to develop and support disease management to prevent complications and implement interventions for improving resilience and reducing negative emotions such as depression.
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Affiliation(s)
- Mi-Kyoung Cho
- grid.254229.a0000 0000 9611 0917Department of Nursing Science, Chungbuk National University, Chungdae-Ro, Seowon-Gu, Cheongju, Korea
| | - Mi Young Kim
- College of Nursing, Hanyang University, 222 Wangsimni-Ro, Seongdong-Gu, Seoul, Korea.
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Botella-Serrano M, Velasco JM, Sánchez-Sánchez A, Garnica O, Hidalgo JI. Evaluating the influence of sleep quality and quantity on glycemic control in adults with type 1 diabetes. Front Endocrinol (Lausanne) 2023; 14:998881. [PMID: 36896174 PMCID: PMC9989462 DOI: 10.3389/fendo.2023.998881] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 07/20/2022] [Accepted: 01/19/2023] [Indexed: 02/25/2023] Open
Abstract
BACKGROUND Sleep quality disturbances are frequent in adults with type 1 diabetes. However, the possible influence of sleep problems on glycemic variability has yet to be studied in depth. This study aims to assess the influence of sleep quality on glycemic control. MATERIALS AND METHODS An observational study of 25 adults with type 1 diabetes, with simultaneous recording, for 14 days, of continuous glucose monitoring (Abbott FreeStyle Libre system) and a sleep study by wrist actigraphy (Fitbit Ionic device). The study analyzes, using artificial intelligence techniques, the relationship between the quality and structure of sleep with time in normo-, hypo-, and hyperglycemia ranges and with glycemic variability. The patients were also studied as a group, comparing patients with good and poor sleep quality. RESULTS A total of 243 days/nights were analyzed, of which 77% (n = 189) were categorized as poor quality and 33% (n = 54) as good quality. Linear regression methods were used to find a correlation (r =0.8) between the variability of sleep efficiency and the variability of mean blood glucose. With clustering techniques, patients were grouped according to their sleep structure (characterizing this structure by the number of transitions between the different sleep phases). These clusters showed a relationship between time in range and sleep structure. CONCLUSIONS This study suggests that poor sleep quality is associated with lower time in range and greater glycemic variability, so improving sleep quality in patients with type 1 diabetes could improve their glycemic control.
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Affiliation(s)
- Marta Botella-Serrano
- Endocrinology and Nutrition Service, Hospital Universitario Príncipe de Asturias, Madrid, Spain
- *Correspondence: Marta Botella-Serrano, ; Jose Manuel Velasco, ; J. Ignacio Hidalgo,
| | - Jose Manuel Velasco
- Computer Architecture and Automation Department, Universidad Complutense de Madrid, Madrid, Spain
- *Correspondence: Marta Botella-Serrano, ; Jose Manuel Velasco, ; J. Ignacio Hidalgo,
| | | | - Oscar Garnica
- Computer Architecture and Automation Department, Universidad Complutense de Madrid, Madrid, Spain
| | - J. Ignacio Hidalgo
- Computer Architecture and Automation Department, Universidad Complutense de Madrid, Madrid, Spain
- *Correspondence: Marta Botella-Serrano, ; Jose Manuel Velasco, ; J. Ignacio Hidalgo,
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Wu N, Jamnik VK, Koehle MS, Guan Y, Li Y, Kaufman K, Warburton DER. Associations between Sleep Characteristics and Cardiovascular Risk Factors in Adolescents Living with Type 1 Diabetes. J Clin Med 2022; 11:5295. [PMID: 36142941 PMCID: PMC9503476 DOI: 10.3390/jcm11185295] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 08/14/2022] [Revised: 09/06/2022] [Accepted: 09/07/2022] [Indexed: 11/16/2022] Open
Abstract
Adolescents living with type 1 diabetes (T1D) have an increased risk of developing cardiovascular disease. Sleep patterns have physiological and behavioral impacts on diabetes outcomes. This study aimed to investigate the associations between sleep patterns and CVD risk factors in adolescents living with T1D and their peers living without T1D. This cross-sectional study assessed CVD risk factors and sleep characteristics (and their associations) in adolescents, aged 12-18 years, living with T1D (n = 48) and their peers (n = 19) without T1D. Outcomes included blood pressure, lipid profiles, and sleep characteristics (accelerometry). Statistical differences between groups were determined with chi-square or independent samples t-tests. The associations between sleep characteristics and CVD risk factors were assessed with multivariate linear regression analyses. We found no significant differences between the two groups in terms of sleep duration, efficiency, sleep onset and offset, and frequency of awakenings, and there were associations between sleep efficiency and LDL-C (β = -0.045, p = 0.018, model R2 = 0.230) and triglycerides (β = -0.027, p = 0.012, model R2 = 0.222) after adjusting confounders (diabetes status, sex, age, pubertal stage) in all participants. In conclusion, adolescents with T1D and without T1D sleep less than the recommended eight hours per night. The associations between sleep efficiency and LDL-C and triglycerides are independent of sleep duration, regardless of sex, age, and pubertal stage.
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Affiliation(s)
- Nana Wu
- Physical Activity Promotion and Chronic Disease Prevention Unit, The University of British Columbia, Vancouver, BC V6T 1Z4, Canada
| | - Veronica K. Jamnik
- School of Kinesiology and Health Science, York University, Toronto, ON M3J 1P3, Canada
| | - Michael S. Koehle
- Division of Sports Medicine, Faculty of Medicine, The University of British Columbia, Vancouver, BC V6T 1Z4, Canada
- School of Kinesiology, Faculty of Education, The University of British Columbia, Vancouver, BC V6T 1Z4, Canada
| | - Yanfei Guan
- Physical Activity Promotion and Chronic Disease Prevention Unit, The University of British Columbia, Vancouver, BC V6T 1Z4, Canada
| | - Yongfeng Li
- College of Sports and Health, Shandong Sport University, Jinan 250102, China
| | - Kai Kaufman
- Physical Activity Promotion and Chronic Disease Prevention Unit, The University of British Columbia, Vancouver, BC V6T 1Z4, Canada
| | - Darren E. R. Warburton
- Physical Activity Promotion and Chronic Disease Prevention Unit, The University of British Columbia, Vancouver, BC V6T 1Z4, Canada
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Monzon AD, Patton SR, Koren D. Childhood diabetes and sleep. Pediatr Pulmonol 2022; 57:1835-1850. [PMID: 34506691 DOI: 10.1002/ppul.25651] [Citation(s) in RCA: 4] [Impact Index Per Article: 1.3] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 03/02/2021] [Revised: 07/18/2021] [Accepted: 08/26/2021] [Indexed: 12/18/2022]
Abstract
Sleep modulates glucose metabolism, both in healthy states and in disease. Alterations in sleep duration (insufficient and excessive) and obstructive sleep apnea may have reciprocal ties with obesity, insulin resistance and Type 2 diabetes, as demonstrated by emerging evidence in children and adolescents. Type 1 diabetes is also associated with sleep disturbances due to the influence of wide glycemic fluctuations upon sleep architecture, the need to treat nocturnal hypoglycemia, and the need for glucose monitoring and insulin delivery technologies. In this article, we provide an extensive and critical review on published pediatric literature regarding these topics, reviewing both epidemiologic and qualitative data, and provide an overview of the pathophysiology linking sleep with disorders of glucose homeostasis.
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Affiliation(s)
- Alexandra D Monzon
- Department of Psychology and Applied Behavioral Science, Clinical Child Psychology Program, University of Kansas, Lawrence, Kansas, USA
| | - Susana R Patton
- Department of Biomedical Research, Center for Healthcare Delivery Science, Nemours Children's Health System, Jacksonville, Florida, USA
| | - Dorit Koren
- Department of Pediatrics, Pediatric Endocrinology Unit, Massachusetts General Hospital, Boston, Massachusetts, USA
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Franceschi R, Scotton C, Leonardi L, Cauvin V, Maines E, Angriman M, Pertile R, Valent F, Soffiati M, Faraguna U. Impact of intermittently scanned continuous glucose monitoring with alarms on sleep and metabolic outcomes in children and adolescents with type 1 diabetes. Acta Diabetol 2022; 59:911-919. [PMID: 35397650 DOI: 10.1007/s00592-022-01882-3] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.3] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 12/29/2021] [Accepted: 03/13/2022] [Indexed: 11/01/2022]
Abstract
AIMS Data about sleep quality and quantity are not available in patients with type 1 diabetes (T1D) using intermittently scanned continuous glucose monitoring (isCGM). We questioned whether the isCGM with alarms could fragment sleep in patients and parents, compared to isCGM without alarms. METHODS A prospective, observational study including 47 child-adolescents with T1D who had experience with isCGM without alarms (Freestyle Libre 1-FSL1). They were asked to wear the isCGM with alarms (Freestyle Libre 2-FSL2) for 14 days. Patients enrolled and their caregiver (s), during a 14 day period with FSL1 and the following 14 days with FSL2, completed psychosocial and sleep-related questionnaires. Furthermore they wore an actigraph that was downloaded to a web platform and processed by the validated and certified algorithm "Dormi®." RESULTS By the switch to the alarmed FSL2 we found about a 5% increase in Time In Range (from 62.5 to 67.8%), a reduction in time spent in hypoglycemia, number of weekly hypoglycemic events, and coefficient of variation. We did not find significant differences in sleep parameters in patients and their parents; therefore, alarms did not worsen the duration and quality of sleep. A significant improvement in the Quality of Life was perceived by parents using FSL2. CONCLUSIONS Introduction of alarms in isCGM systems gives, in the short term, an improvement in metabolic control in terms of time in range and reduction in hypoglycemia, without worsening duration and quality of sleep, measured by actigraphy, in children-adolescent and their parents.
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Affiliation(s)
- Roberto Franceschi
- Pediatric Diabetology Unit, Pediatric Department, S. Chiara General Hospital, Largo Medaglie d'Oro, 9, 38122, Trento, Italy.
| | - Chiara Scotton
- Pediatric Diabetology Unit, Pediatric Department, S. Chiara General Hospital, Largo Medaglie d'Oro, 9, 38122, Trento, Italy
| | - Letizia Leonardi
- Pediatric Diabetology Unit, Pediatric Department, S. Chiara General Hospital, Largo Medaglie d'Oro, 9, 38122, Trento, Italy
| | - Vittoria Cauvin
- Pediatric Diabetology Unit, Pediatric Department, S. Chiara General Hospital, Largo Medaglie d'Oro, 9, 38122, Trento, Italy
| | - Evelina Maines
- Pediatric Diabetology Unit, Pediatric Department, S. Chiara General Hospital, Largo Medaglie d'Oro, 9, 38122, Trento, Italy
| | - Marco Angriman
- Health Management, General Hospital of Bolzano, Bolzano, Italy
| | - Riccardo Pertile
- Clinical and Evaluative Epidemiology Unit, Department of Governance, APSS, Trento, Italy
| | - Francesca Valent
- Clinical and Evaluative Epidemiology Unit, Department of Governance, APSS, Trento, Italy
| | - Massimo Soffiati
- Pediatric Diabetology Unit, Pediatric Department, S. Chiara General Hospital, Largo Medaglie d'Oro, 9, 38122, Trento, Italy
| | - Ugo Faraguna
- Department of Translational Research and New Technologies in Medicine and Surgery, University of Pisa, Pisa, Italy
- Department of Developmental Neuroscience, IRCSS Stella Maris Foundation, Pisa, Italy
- SleepActa Srl, A spinoff company of the University of Pisa, Pisa, Italy
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Cobry EC, Karami AJ, Meltzer LJ. Friend or Foe: a Narrative Review of the Impact of Diabetes Technology on Sleep. Curr Diab Rep 2022; 22:283-290. [PMID: 35522354 DOI: 10.1007/s11892-022-01468-x] [Citation(s) in RCA: 10] [Impact Index Per Article: 3.3] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Accepted: 03/21/2022] [Indexed: 12/23/2022]
Abstract
PURPOSE OF REVIEW The purpose of this review is to present a review of sleep science, the relationship between sleep and type 1 diabetes, and highlight the current literature on sleep outcomes in adult and pediatric diabetes technology research. RECENT FINDINGS Sleep quality is associated with glycemic outcomes, diabetes self-management, and mental health in people with type 1 diabetes. Diabetes technologies, including insulin pumps, continuous glucose monitors, and hybrid closed-loop systems improve glycemic outcomes. However, many people find this technology challenging for a variety of reasons, including increased burden and frequent alarms, especially during the night. The impact of different devices on sleep quality and quantity has been mixed. The newest technology, the hybrid closed-loop systems, offers the best opportunity for nocturnal glycemic regulation and has improved patient and family perspectives on sleep quality. However, objective sleep assessment has not shown significant improvement on sleep duration. Sleep quality and quantity in people with type 1 diabetes are widely recognized as an important component of health care, and the literature regarding the impact of diabetes devices on sleep is increasing. However, sleep disruptions are common and a barrier to device use. Despite finding minimal changes to sleep duration with device use, subjective accounts of sleep quality are overall positive, especially in those using hybrid closed-loop systems. Sleep quantity and quality are important outcomes to consider as diabetes technology continues to evolve.
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Affiliation(s)
- Erin C Cobry
- Barbara Davis Center, Pediatric Endocrinology and Diabetes, University of Colorado Anschutz Medical Campus, 1775 Aurora Ct, MSA140, Aurora, CO, 80045, USA.
| | - Angela J Karami
- Barbara Davis Center, Pediatric Endocrinology and Diabetes, University of Colorado Anschutz Medical Campus, 1775 Aurora Ct, MSA140, Aurora, CO, 80045, USA
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Cobry EC, Bisio A, Wadwa RP, Breton MD. Improvements in Parental Sleep, Fear of Hypoglycemia, and Diabetes Distress With Use of an Advanced Hybrid Closed-Loop System. Diabetes Care 2022; 45:1292-1295. [PMID: 35202468 PMCID: PMC9174965 DOI: 10.2337/dc21-1778] [Citation(s) in RCA: 33] [Impact Index Per Article: 11.0] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 08/23/2021] [Accepted: 01/30/2022] [Indexed: 02/03/2023]
Abstract
OBJECTIVE Parental sleep quality may contribute to glycemic control in youth with type 1 diabetes. In this article we present sleep analysis from a multicenter, randomized trial of children ages 6-13 years with type 1 diabetes evaluating the Tandem Control-IQ (CIQ) hybrid closed-loop (HCL) system. RESEARCH DESIGN AND METHODS Pittsburgh Sleep Quality Index (PSQI) scores were assessed at baseline to identify parents as "poor" sleepers (PSQI >5). Glycemic and psycho-behavioral outcomes before and after CIQ use were analyzed in poor sleepers (n = 49) and their children. RESULTS Nocturnal time in range (P < 0.001) and time hyperglycemic (P < 0.001), Hypoglycemia Fear Survey for Parents score (P < 0.001), Problem Areas in Diabetes scale score (P < 0.001), PSQI score (P < 0.001), and Hypoglycemia Fear Survey for Children score (P = 0.025) significantly improved. Of poor sleepers, 27 became good sleepers (PSQI score <5). CONCLUSIONS Use of CIQ in youth with type 1 diabetes ages 6-13 years significantly improved sleep and psychosocial measures in parent poor sleepers, coinciding with improvements in child nocturnal glycemia, highlighting the relationship between HCL systems and parent sleep quality.
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Affiliation(s)
- Erin C Cobry
- Barbara Davis Center for Diabetes, University of Colorado Anschutz Medical Campus, Aurora, CO
| | - Alessandro Bisio
- Center for Diabetes Technology, University of Virginia, Charlottesville, VA
| | - R Paul Wadwa
- Barbara Davis Center for Diabetes, University of Colorado Anschutz Medical Campus, Aurora, CO
| | - Marc D Breton
- Center for Diabetes Technology, University of Virginia, Charlottesville, VA
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Abstract
PURPOSE OF REVIEW To review the relationship between sleep and hypoglycemia, sleep characteristics, and their associations with glycemic control in persons with type 1 diabetes (T1D). The effects of sleep interventions and diabetes technology on sleep are summarized. RECENT FINDINGS Nocturnal hypoglycemia affects objective and subjective sleep quality and is related to behavioral, psychological, and physiological factors. Sleep disturbances are common, including inadequate sleep, impaired sleep efficiency, poor subjective satisfaction, irregular timing, increased daytime sleepiness, and sleep apnea. Some have a bidirectional relationship with glycemic control. Preliminary evidence supports sleep interventions (e.g., sleep extension and sleep coach) in improving sleep and glycemic control, while diabetes technology use could potentially improve sleep. Hypoglycemia and sleep disturbances are common among persons with T1D. There is a need to develop sleep promotion programs and test their effects on sleep, glucose, and related outcomes (e.g., self-care, psychological health).
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Affiliation(s)
- Bingqian Zhu
- School of Nursing, Shanghai Jiao Tong University, Shanghai, China
| | - Ghada Mohammed Abu Irsheed
- College of Nursing, Department of Biobehavioral Nursing Science, University of Illinois at Chicago, Chicago, IL, USA
| | - Pamela Martyn-Nemeth
- College of Nursing, Department of Biobehavioral Nursing Science, University of Illinois at Chicago, Chicago, IL, USA
| | - Sirimon Reutrakul
- Division of Endocrinology, Diabetes, and Metabolism, Department of Medicine, University of Illinois at Chicago, 835 S. Wolcott Ave, Suite 625E, M/C 640, IL, 60612, Chicago, USA.
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12
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Ji X, Wang Y, Saylor J. Sleep and Type 1 Diabetes Mellitus Management Among Children, Adolescents, and Emerging Young Adults: A Systematic Review. J Pediatr Nurs 2021; 61:245-253. [PMID: 34182231 DOI: 10.1016/j.pedn.2021.06.010] [Citation(s) in RCA: 12] [Impact Index Per Article: 3.0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 09/23/2020] [Revised: 06/14/2021] [Accepted: 06/14/2021] [Indexed: 11/19/2022]
Abstract
BACKGROUND Type 1 diabetes mellitus (T1DM) is one of the most common chronic illnesses among the youth. Emerging evidence has suggested poor sleep as a risk factor for glycemic control. This review aimed to examine the associations between sleep characteristics and diabetes management in children, adolescents, and emerging young adults with T1DM. METHODS Following PRISMA guidelines, the authors searched articles in PubMed, Web of Science, and Scopus from 2000 through August 2020. Using inclusion and exclusion criteria, observational studies and clinical trials that examined sleep and diabetes management among individuals with T1DM (up to 25 years old) were selected for review. RESULTS Twenty-four articles met the review criteria. Most studies did not report differences in self-report sleep between individuals with and without T1DM. However, several studies using objective sleep measures (actigraph and PSG) suggested shorter sleep duration and worse sleep quality in individuals with T1DM. Higher A1C levels and undesirable T1DM self-care behaviors were associated with short and long sleep duration, poor sleep quality, sleep disturbances, and irregular sleep, particularly among adolescent boys, young men and those from immigrant families. Self-care behaviors mediated the associations between sleep and subsequent A1C levels. CONCLUSIONS Too much or too little sleep, poor sleep quality, sleep disturbances and sleep variability are associated with undesirable T1DM management. Although more research is needed, our findings indicate the importance of including sleep education in the plan of care for children, adolescents and emerging young adults with T1DM.
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Affiliation(s)
- Xiaopeng Ji
- College of Health Sciences, School of Nursing, University of Delaware, DE, USA.
| | - Yiqi Wang
- College of Health Sciences, School of Nursing, University of Delaware, DE, USA; University of Pennsylvania School of Nursing, PA, USA.
| | - Jennifer Saylor
- College of Health Sciences, School of Nursing, University of Delaware, DE, USA.
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13
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Salah NY, Abido AY, Rashed HR. Relationship of glycaemic derangement using continuous glucose monitoring system with sleep pattern among children with type 1 diabetes. Diabetes Metab Res Rev 2021; 37:e3407. [PMID: 32935448 DOI: 10.1002/dmrr.3407] [Citation(s) in RCA: 3] [Impact Index Per Article: 0.8] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 06/01/2020] [Revised: 07/25/2020] [Accepted: 08/24/2020] [Indexed: 12/23/2022]
Abstract
BACKGROUND Glycaemic derangement has been linked to sleep disruption. However, the impact of glycaemic derangement on sleep pattern among children with type 1 diabetes (C-T1D) remains unraveled. AIM To assess the effect of nocturnal hyperglycaemia and clinically significant (CS) hypoglycaemia on sleep pattern among C-T1D. METHODOLOGY Thirty C-T1D were compared to 30 age and sex matched healthy siblings. Patients having other organ disease that might cause sleep disorders or on medications causing sleep disturbance were excluded. History included diabetes-duration, type and dose of insulin therapy, chronic diabetic-complications, and manifestations of sleep disorders. Epworth Sleepiness Scale-Child Adolescent was used. Continuous glucose monitoring system (CGMS) and overnight polysomnography were done and analysed. RESULTS C-T1D had significantly lower sleep efficiency and significantly higher arousal index (AI), periodic limb movement index and apnoea-hypopnoea index compared to controls. Moreover, they had significantly longer sleep-onset latency, light sleep percentage, and shorter rapid eye movement percentage than controls. According to nocturnal CGMS readings, 15 C-T1D had nocturnal hyperglycaemia (50%), six experienced CS hypoglycaemia (20%), two had level-1 hypoglycaemia (6.7%), and seven were within the normoglycaemic range (23.3%). C-T1D experiencing nocturnal CS hypoglycaemia had significantly higher stage 3 sleep (P = 0.004) than controls. On the other hand, C- T1D experiencing nocturnal hyperglycaemia had significantly higher sleep onset latency (P = 0.013), light sleep percentage (P < 0.001), and AI (P < 0.001) than controls. Nocturnal CS hypoglycaemia was positively correlated to deep sleep duration, while hyperglycaemia was correlated to number of awakenings, sleep-onset latency, and light sleep duration. CONCLUSION In children with T1D CS hypoglycaemia is associated with sleep deepening, while hyperglycaemia is associated with increased light sleep, sleep onset latency.
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Affiliation(s)
- Nouran Y Salah
- Department of Pediatrics, Faculty of Medicine, Ain Shams University, Cairo, Egypt
| | - Amal Y Abido
- General Practitioner, Health Insurance Hospital, Giza, Egypt
| | - Hebatallah R Rashed
- Department of Neurology, Faculty of Medicine, Ain Shams University, Cairo, Egypt
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14
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Eriksen TLM, Gaulke A, Skipper N, Svensson J. The impact of childhood health shocks on parental labor supply. JOURNAL OF HEALTH ECONOMICS 2021; 78:102486. [PMID: 34192649 DOI: 10.1016/j.jhealeco.2021.102486] [Citation(s) in RCA: 5] [Impact Index Per Article: 1.3] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Subscribe] [Scholar Register] [Received: 09/03/2020] [Revised: 04/15/2021] [Accepted: 06/03/2021] [Indexed: 06/13/2023]
Abstract
We leverage the onset of type 1 diabetes (T1D) in childhood to estimate the impact of a childhood health shock on parental labor supply. T1D is the second most common childhood chronic physical health condition, inheritability is low, the exact cause is unknown, the onset is unpredictable, and receiving treatment is crucial to survival. Using Danish administrative registry data with both an event study and difference-in-differences analysis shows that mothers shift to part-time work, marginally shift from the private to public sector, and experience a long-term 4-5% decrease in wage income. The dynamic effects reveal large initial impacts, but the magnitudes decrease (although are not eliminated) over time. Fathers do not experience any long-term reduction in wage income. This suggests part of the motherhood penalty is likely due to mothers bearing the economic burden when their child is diagnosed with a chronic health condition.
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Affiliation(s)
| | - Amanda Gaulke
- Department of Economics, Kansas State University, 327 Waters Hall, 1603 Old Claflin Place, Manhattan, KS 66506, United States.
| | - Niels Skipper
- Department of Economics and Business Economics, Aarhus University, Aarhus, Denmark
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15
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Macaulay GC, Galland BC, Boucher SE, Wiltshire EJ, Haszard JJ, Campbell AJ, Black SM, Smith C, Elder D, Wheeler BJ. Impact of type 1 diabetes mellitus, glucose levels, and glycemic control on sleep in children and adolescents: a case-control study. Sleep 2021; 43:5580781. [PMID: 31583407 DOI: 10.1093/sleep/zsz226] [Citation(s) in RCA: 9] [Impact Index Per Article: 2.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 12/04/2018] [Revised: 07/03/2019] [Indexed: 12/13/2022] Open
Abstract
STUDY OBJECTIVES To assess differences in habitual sleep patterns and sleep states between children and adolescents with type 1 diabetes mellitus (T1DM) and control subjects, and to explore the relationships between sleep, glucose levels, and glycemic control. METHODS Participants included 82 children (5-18 years); 41 with T1DM (cases), and 41 healthy control subjects group matched for age and sex. Sleep was measured by 7-day actigraphy and single-night home-based polysomnography (PSG) recordings. Hemoglobin A1c (HbA1c) and 7 days of continuous glucose monitoring (CGM) data were collected in cases. Regression analyses were used to model all within- and between-group comparisons adjusted for age, sex, and BMI z-scores. RESULTS There were no significant differences in sleep duration, efficiency, or awakenings as measured by actigraphy and PSG between cases and controls, nor sleep states measured by PSG. However, cases had significantly later sleep onset and offset than controls (both p < 0.05), partially moderated by age. Cases with suboptimal glycemic control (HbA1c ≥ 58 mmol/mol [≥7.5%]) had significantly shorter actigraphy-derived total sleep time (TST) (mean difference = -40 minutes; 95% confidence interval = -77, -3), with similar differences in TST measured by PSG. Cases with mean CGM glucose levels ≥10 mmol/L (≥180 mg/dL) on PSG night had significantly more stage N3 (%) sleep and less stage REM (%) sleep (both p < 0.05). CONCLUSIONS Short- and long-term suboptimal glycemic control in T1DM children appears to be associated with sleep alterations. Pediatric diabetes care teams should be aware of potential interrelationships between sleep and T1DM, including management and glycemic control.
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Affiliation(s)
- Grace C Macaulay
- Department of Women's and Children's Health, University of Otago, Dunedin, New Zealand
| | - Barbara C Galland
- Department of Women's and Children's Health, University of Otago, Dunedin, New Zealand
| | - Sara E Boucher
- Department of Women's and Children's Health, University of Otago, Dunedin, New Zealand
| | - Esko J Wiltshire
- Department of Paediatrics and Child Health, University of Otago, Wellington, New Zealand
| | - Jillian J Haszard
- Department of Human Nutrition, University of Otago, Dunedin, New Zealand
| | - Angela J Campbell
- WellSleep Investigation Centre, Department of Medicine, University of Otago, Wellington, New Zealand and
| | - Stephanie M Black
- WellSleep Investigation Centre, Department of Medicine, University of Otago, Wellington, New Zealand and
| | - Claire Smith
- Department of Women's and Children's Health, University of Otago, Dunedin, New Zealand
| | - Dawn Elder
- Department of Paediatrics and Child Health, University of Otago, Wellington, New Zealand
| | - Benjamin J Wheeler
- Department of Women's and Children's Health, University of Otago, Dunedin, New Zealand.,Paediatric Endocrinology, Southern District Health Board, Dunedin, New Zealand
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16
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Abdelmaksoud AA, Salah NY, Ali ZM, Rashed HR, Abido AY. Disturbed sleep quality and architecture in adolescents with type 1 diabetes mellitus: Relation to glycemic control, vascular complications and insulin sensitivity. Diabetes Res Clin Pract 2021; 174:108774. [PMID: 33745994 DOI: 10.1016/j.diabres.2021.108774] [Citation(s) in RCA: 13] [Impact Index Per Article: 3.3] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 02/15/2021] [Revised: 03/15/2021] [Accepted: 03/15/2021] [Indexed: 12/16/2022]
Abstract
BACKGROUND Insufficient sleep duration and poor sleep quality have been linked to insulin resistance and impaired glucose metabolism. However, the relation between sleep disruption and type1 diabetes (T1D) hasn't been thoroughly explored. AIM To study the association between sleep parameters and glycemic control, insulin resistance and micro-vascular complications among adolescent with T1D. METHODOLOGY Sixty adolescents with T1D were compared to 60 matched controls. Diabetes-duration, insulin-therapy, fundus, Epworth Sleepiness Scale-Child Adolescent and the neuropathy disability score were assessed. Fasting lipids, fraction-C of glycosylated hemoglobin(HbA1c) and urinary albumin-excretion were measured with calculation of the insulin sensitivity score(ISS). Overnight polysomnography(PSG) was done. RESULTS Adolescents with T1D had significantly lower sleep efficiency and rapid eye movement(REM) sleep than controls with significantly higher sleep onset latency, non-REM sleep and arousal index(P < 0.001). Although ISS was negatively correlated to total sleep time(P = 0.002); it was positively correlated to sleep efficiency(P < 0.001). HbA1C was negatively correlated to sleep efficiency(<0.001) and REM sleep(P = 0.003) and positively correlated to sleep onset latency(P = 0.005). T1D adolescents with micro-vascular complications had significantly lower sleep efficiency and REM sleep than those without micro-vascular complications. CONCLUSION Poor sleep quality and architecture among adolescents with T1D are associated with impaired glycemic control, insulin resistance and micro-vascular complications.
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Affiliation(s)
- Abeer A Abdelmaksoud
- Department of Pediatrics, Faculty of Medicine, Ain Shams University, Cairo, Egypt
| | - Nouran Y Salah
- Department of Pediatrics, Faculty of Medicine, Ain Shams University, Cairo, Egypt.
| | - Zeinab M Ali
- Department of Psychiatry, Faculty of Medicine, Ain Shams University, Cairo, Egypt
| | - Hebatallah R Rashed
- Department of Neurology, Faculty of Medicine, Ain Shams University, Cairo, Egypt
| | - Amal Y Abido
- Department of Pediatrics, Health Insurance Hospital, 6(th) of October, Giza, Egypt
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ALTIN Z, BAYRAK B. The relationship between sleep and metabolic factors in diabetes mellitus. FAMILY PRACTICE AND PALLIATIVE CARE 2020. [DOI: 10.22391/fppc.747615] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/23/2022] Open
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Griggs S, Redeker NS, Jeon S, Grey M. Daily variations in sleep and glucose in adolescents with type 1 diabetes. Pediatr Diabetes 2020; 21:1493-1501. [PMID: 32902901 PMCID: PMC7642150 DOI: 10.1111/pedi.13117] [Citation(s) in RCA: 18] [Impact Index Per Article: 3.6] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 03/27/2020] [Revised: 07/21/2020] [Accepted: 09/02/2020] [Indexed: 01/03/2023] Open
Abstract
OBJECTIVE We used multilevel models (MLMs) to determine person (between-persons) and day level (within-person) associations between glucose variability indices and sleep characteristics in adolescents with type 1 diabetes (T1D). METHODS Adolescents with T1D (Mean age 13.4 ± 1.8 years; 37.8% male; mean HbA1c 8.2 ± 1.2%, 66 mmol/mol) monitored their sleep and glucose patterns concurrently for 3-7 days with a wrist actigraph on their non-dominant wrist and a continuous glucose monitor (CGM) (their own or a provided, blinded CGM). Glucose variability indices included J index, coefficient of variation, low and high blood glucose risk indices (LBGI and HBGI), time in range, and sleep characteristics, including bedtime, wake time, total sleep time, sleep efficiency, wake after sleep onset, awakenings, and sleep fragmentation index. RESULTS More overall glucose variability was associated within person, more sleep disruptions (more awakenings and more fragmentation) or poorer sleep in our study (earlier wake time or longer wake after sleep onset). Also, more time spent in hypoglycemia <70 mg/dL and a higher LBGI was associated within person with earlier wake time indicating poorer sleep. However, a lower LBGI was associated with a later between-persons wake time. CONCLUSIONS Monitoring over a longer period of time in subsequent studies would allow researchers to determine the within person association between habitual short sleep duration and glucose variability. Providers should regularly assess sleep habits in adolescents as a way to improve glycemic control. Targeting a euglycemic range overnight is also important to promote better sleep and to decrease sleep disruptions.
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Affiliation(s)
- Stephanie Griggs
- Instructor of Nursing, Frances Payne Bolton School of Nursing, Case Western Reserve University, 10900 Euclid Avenue, Cleveland, Ohio 44106
| | - Nancy S. Redeker
- Beatrice Renfield Term Professor of Nursing & Professor of Medicine, Yale University, School of Nursing and School of Medicine, West Haven, Connecticut, USA 06477
| | - Sangchoon Jeon
- Research Scientist, Yale University, School of Nursing, West Haven, Connecticut, USA 06477
| | - Margaret Grey
- Annie Goodrich Professor of Nursing and Professor of Pediatrics, Yale University, School of Nursing and School of Medicine, West Haven, Connecticut, USA 06477
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Cobry EC, Hamburger E, Jaser SS. Impact of the Hybrid Closed-Loop System on Sleep and Quality of Life in Youth with Type 1 Diabetes and Their Parents. Diabetes Technol Ther 2020; 22:794-800. [PMID: 32212971 PMCID: PMC7698988 DOI: 10.1089/dia.2020.0057] [Citation(s) in RCA: 35] [Impact Index Per Article: 7.0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Indexed: 12/13/2022]
Abstract
Background: Insufficient sleep is common in youth with type 1 diabetes (T1D) and parents, likely secondary to diabetes-related disturbances, including fear of hypoglycemia, nocturnal glucose monitoring, hypoglycemia, and device alarms. Hybrid closed-loop (HCL) systems improve glycemic variability and potentially reduce nocturnal awakenings. Methods: Adolescents with T1D (N = 37, mean age 13.9 years, 62% female, mean HbA1c 8.3%) and their parents were enrolled in this observational study when starting the Medtronic 670G HCL system. Participants completed study measures (sleep and psychosocial surveys and actigraphy with sleep diaries) before starting auto mode and ∼3 months later. Results: Based on actigraphy data, neither adolescents' nor parents' sleep characteristics changed significantly pre-post device initiation. Adolescents' mean total sleep time decreased from 7 h 16 min (IQR: [6:43-7:47]) to 7 h 9 min (IQR: [6:44-7:52]), while parents' total sleep time decreased from 6 h 47 min (IQR: [6:16-7:10]) to 6 h 38 min (IQR: [5:57-6:57]). Although there were no significant differences in most of the survey measures, there was a moderate effect for improved sleep quality in parents and fear of hypoglycemia in adolescents. In addition, adolescents reported a significant increase in self-reported glucose monitoring satisfaction. Adolescents averaged 44.7% use of auto mode at 3 months. Conclusions: Our data support previous research showing youth with T1D and their parents are not achieving the recommended duration of sleep. Lack of improvement in sleep may be due to steep learning curves involved with new technology. We observed moderate improvements in parental subjective report of sleep quality despite no change in objective measures of sleep duration. Further evaluation of sleep with long-term HCL use and larger sample size is needed.
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Affiliation(s)
- Erin C. Cobry
- Barbara Davis Center for Diabetes, University of Colorado School of Medicine, Aurora, Colorado, USA
- Address correspondence to: Erin C. Cobry, MD, Barbara Davis Center, University of Colorado School of Medicine, 1775 Aurora Court, MSA140, Aurora, CO 80045
| | - Emily Hamburger
- Department of Psychology Univeristy of Nebraska-Lincoln, Lincoln, Nebraska, USA
| | - Sarah S. Jaser
- Department of Pediatrics, Vanderbilt University Medical Center, Nashville, Tennessee, USA
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Byun JI, Cha KS, Jun JE, Kim TJ, Jung KY, Jeong IK, Shin WC. Dynamic changes in nocturnal blood glucose levels are associated with sleep-related features in patients with obstructive sleep apnea. Sci Rep 2020; 10:17877. [PMID: 33087786 PMCID: PMC7578637 DOI: 10.1038/s41598-020-74908-x] [Citation(s) in RCA: 4] [Impact Index Per Article: 0.8] [Reference Citation Analysis] [Abstract] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 04/01/2020] [Accepted: 10/06/2020] [Indexed: 12/12/2022] Open
Abstract
Obstructive sleep apnea (OSA) has a bidirectional relationship with insulin resistance conditions; however, the mechanism remains unclear. This study aimed to compare dynamic nocturnal glucose changes among patients with OSA of varying levels of severity and evaluate temporal changes associated with the cardinal features of OSA (sympathetic hyperactivation, intermittent hypoxemia, and sleep fragmentation) in nondiabetic subjects. Nocturnal glucose was measured with a continuous glucose monitoring device every 5 min during polysomnography (PSG). The OSA features were evaluated using heart rate variability (HRV), minimum saturation, and electroencephalography. Eleven subjects with moderate to severe OSA and 12 subjects with no or mild OSA were evaluated. Those with moderate to severe OSA showed an increasing trend in blood glucose levels after sleep onset, whereas those without or with mild OSA showed a decreasing trend (F = 8.933, p < 0.001). Delta band power also showed different trends during sleep between the two groups (F = 2.991, p = 0.009), and minimum saturation remained lower in the moderate to severe OSA group than in the no or mild OSA group. High degrees of coupling between nocturnal glucose levels and each OSA feature were observed. Altered trends in nocturnal glucose in moderate to severe OSA may reflect glucose intolerance and result in metabolic consequences. Managing the features of sleep-related OSA may have implications for metabolic management in the future.
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Affiliation(s)
- Jung-Ick Byun
- Department of Neurology, Kyung Hee University School of Medicine, Kyung Hee University Hospital At Gangdong, 892 Dongnam-ro, Gangdong-gu, Seoul, 134-727, Republic of South Korea
| | - Kwang Su Cha
- Department of Neurology, Seoul National University Hospital, Seoul National University College of Medicine, Seoul, Republic of South Korea
| | - Ji Eun Jun
- Department of Endocrinology and Metabolism, Kyung Hee University School of Medicine, Kyung Hee University Hospital At Gangdong, 892 Dongnam-ro, Gangdong-gu, Seoul, 134-727, Republic of South Korea
| | - Tae-Joon Kim
- Department of Neurology, Ajou University School of Medicine, Suwon, Republic of South Korea
| | - Ki-Young Jung
- Department of Neurology, Seoul National University Hospital, Seoul National University College of Medicine, Seoul, Republic of South Korea
| | - In-Kyung Jeong
- Department of Endocrinology and Metabolism, Kyung Hee University School of Medicine, Kyung Hee University Hospital At Gangdong, 892 Dongnam-ro, Gangdong-gu, Seoul, 134-727, Republic of South Korea.
| | - Won Chul Shin
- Department of Neurology, Kyung Hee University School of Medicine, Kyung Hee University Hospital At Gangdong, 892 Dongnam-ro, Gangdong-gu, Seoul, 134-727, Republic of South Korea.
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Hur MH, Lee MK, Seong K, Hong JH. Deterioration of Sleep Quality According to Glycemic Status. Diabetes Metab J 2020; 44:679-686. [PMID: 32431108 PMCID: PMC7643591 DOI: 10.4093/dmj.2019.0125] [Citation(s) in RCA: 9] [Impact Index Per Article: 1.8] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 06/25/2019] [Accepted: 08/20/2019] [Indexed: 12/17/2022] Open
Abstract
BACKGROUND Type 2 diabetes mellitus (T2DM) is a progressive disease with multiple complications. The present study aimed to determine the effects of glycemic status on sleep quality in individuals with T2DM, prediabetes, and normal glucose tolerance (NGT). METHODS A total of 90 participants were categorized into three groups, T2DM (n=30), prediabetes (n=30), and NGT (n=30). Objective sleep quality was measured with the actigraph wrist-worn device over 3 nights and subjective sleep quality was evaluated with a questionnaire. RESULTS The duration of diabetes in the T2DM group was 2.23 years and the glycosylated hemoglobin (HbA1c) levels in the T2DM, prediabetes, and NGT groups were 7.83%, 5.80%, and 5.31%, respectively. Sleep efficiency decreased across the T2DM, prediabetes, and NGT groups (86.25%, 87.99%, and 90.22%, respectively; P=0.047). Additionally, HbA1c levels revealed a significant negative correlation with sleep efficiency (r=-0.348, P=0.001). The sleep quality questionnaire results were similar among the three groups. CONCLUSION Although the participants in the present study were not necessarily conscious of their sleep disturbances, deterioration in sleep quality progressed according to glycemic status.
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Affiliation(s)
| | | | - Kayeon Seong
- Eulji University College of Nursing, Daejeon, Korea
| | - Jun Hwa Hong
- Division of Endocrinology, Department of Internal Medicine, Daejeon Eulji Medical Center, Eulji University School of Medicine, Daejeon, Korea
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Al Hayek AA, Al Dawish MA. Assessing Diabetes Distress and Sleep Quality in Young Adults with Type 1 Diabetes Using FreeStyle Libre: A Prospective Cohort Study. Diabetes Ther 2020; 11:1551-1562. [PMID: 32495021 PMCID: PMC7324459 DOI: 10.1007/s13300-020-00849-3] [Citation(s) in RCA: 21] [Impact Index Per Article: 4.2] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 04/22/2020] [Indexed: 12/19/2022] Open
Abstract
INTRODUCTION The burden of diabetes, its potential complications, and related self-care activities can induce negative psychosocial effects in patients with type 1 diabetes mellitus (T1DM). This prospective cohort study investigated the psychosocial benefits associated with 3 months of FreeStyle Libre (FSL) flash glucose monitoring use in young adults with T1DM in Saudi Arabia. METHODS Patients completed the Diabetes Distress Scale (DDS) and the Pittsburgh Sleep Quality Index (PSQI) questionnaires at baseline and 3 months. HbA1c, number of confirmed hypoglycemia episodes per month, and frequency of blood glucose testing were also collected at baseline and 3 months. RESULTS Of 95 patients analyzed, significant reductions were observed in mean DDS (3.8 vs. 2.5; p < 0.001) and PSQI (8.7 vs. 3.9; p < 0.001) scores from baseline to 3 months. Furthermore, HbA1c and confirmed hypoglycemia episodes per month also decreased from baseline to 3 months (HbA1c 8.3 vs. 7.7% [67 vs. 61 mmol/mol], p < 0.001; hypoglycemia episodes 3.0 vs. 2.3, p < 0.001). In contrast, mean frequency of blood glucose testing per day increased from baseline to 3 months (2.5 vs. 5.2; p < 0.001). CONCLUSION These data demonstrate improvements in diabetes distress and sleep quality as well as glycemic outcomes following 3 months' FSL use in young adults with T1DM.
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Affiliation(s)
- Ayman A Al Hayek
- Department of Endocrinology and Diabetes, Diabetes Treatment Center, Prince Sultan Military Medical City, Riyadh, Saudi Arabia.
| | - Mohamed A Al Dawish
- Department of Endocrinology and Diabetes, Diabetes Treatment Center, Prince Sultan Military Medical City, Riyadh, Saudi Arabia
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Monzon AD, Marker AM, Noser AE, Clements MA, Patton SR. Associations Between Objective Sleep Behaviors and Blood Glucose Variability in Young Children With Type 1 Diabetes. Ann Behav Med 2020; 55:144-154. [PMID: 32542309 DOI: 10.1093/abm/kaaa040] [Citation(s) in RCA: 10] [Impact Index Per Article: 2.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 01/17/2023] Open
Abstract
BACKGROUND Young children with Type 1 diabetes (T1D) are at risk for extreme blood glucose variability, a risk factor for suboptimal glycated hemoglobin A1c (HbA1c) and long-term health complications. We know that a reciprocal relationship exists between sleep and glycemic outcomes in older youth with T1D; however, little research has examined objective sleep in young children (<7 years) with T1D. PURPOSE This study examines bidirectional associations between sleep behaviors and glycemic variability in young children with T1D. METHODS Thirty-nine young children with T1D (Mage 4.33 ± 1.46 years; MHbA1c 8.10 ± 1.06%) provided accelerometry data to objectively measure sleep onset latency, number of nighttime awakenings, and total sleep time. We also assessed HbA1c, average blood glucose, and glycemic variability (i.e., standard deviation of blood glucose from device downloads). We evaluated bidirectional relationships using multilevel modeling in SAS, with weekday/weekend as a Level 2 moderator. RESULTS Children averaged 8.5 ± 1.44 hr of sleep per night, but only 12.8% met current sleep recommendations. Children experienced more nighttime awakenings, higher blood glucose, and more glycemic variability on weekends. Sleep onset latency and nighttime awakenings predicted greater glycemic variability on weekends, and weekend glycemic variability predicted increased nighttime awakenings. CONCLUSIONS Most young children with T1D did not meet sleep recommendations. Young children experienced more nighttime awakenings, higher blood glucose, and increased glycemic variability on weekends only, when routines may be less predictable. Findings suggest that one way families of young children with T1D may be able to decrease glycemic variability is to keep consistent routines on weekdays and weekends.
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Affiliation(s)
- Alexandra D Monzon
- Clinical Child Psychology Program, University of Kansas, Lawrence, KS, USA
| | - Arwen M Marker
- Clinical Child Psychology Program, University of Kansas, Lawrence, KS, USA
| | - Amy E Noser
- Clinical Child Psychology Program, University of Kansas, Lawrence, KS, USA
| | - Mark A Clements
- Children's Mercy Hospital, Endocrine/Diabetes Clinical Research, Kansas City, MO, USA
| | - Susana R Patton
- Center for Healthcare Delivery Science, Nemours Children's Health System, Jacksonville, FL, USA
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Nefs GM, Bazelmans E, Donga E, Tack CJ, de Galan BE. Sweet dreams or bitter nightmare: a narrative review of 25 years of research on the role of sleep in diabetes and the contributions of behavioural science. Diabet Med 2020; 37:418-426. [PMID: 31833083 DOI: 10.1111/dme.14211] [Citation(s) in RCA: 13] [Impact Index Per Article: 2.6] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Accepted: 12/10/2019] [Indexed: 12/12/2022]
Abstract
The aim of this review was to provide an overview of developments, clinical implications and gaps in knowledge regarding the relationship between diabetes and sleep over the past 25 years, with special focus on contributions from the behavioural sciences. Multiple prospective observational and experimental studies have shown a link between suboptimal sleep and impaired glucose tolerance, decreased insulin sensitivity and the development of type 2 diabetes. While prevalence rates of suboptimal sleep vary widely according to definition, assessment and sample, suboptimal subjective sleep quality appears to be a common reality for one-third of people with type 1 diabetes and over half of people with type 2 diabetes. Both physiological and psychosocial factors may impair sleep in these groups. In turn, suboptimal sleep can negatively affect glycaemic outcomes directly or indirectly via suboptimal daytime functioning (energy, mood, cognition) and self-care behaviours. Technological devices supporting diabetes self-care may have both negative and positive effects. Diabetes and its treatment also affect the sleep of significant others. Research on the merits of interventions aimed at improving sleep for people with diabetes is in its infancy. Diabetes and sleep appear to be reciprocally related. Discussion of sleep deserves a central place in regular diabetes care. Multi-day, multi-method studies may shed more light on the complex relationship between sleep and diabetes at an individual level. Intervention studies are warranted to examine the potential of sleep interventions in improving outcomes for people with diabetes.
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MESH Headings
- Behavioral Sciences/history
- Behavioral Sciences/methods
- Behavioral Sciences/trends
- Blood Glucose/physiology
- Diabetes Mellitus/blood
- Diabetes Mellitus/etiology
- Diabetes Mellitus/physiopathology
- Diabetes Mellitus/psychology
- Diabetes Mellitus, Type 1/blood
- Diabetes Mellitus, Type 1/complications
- Diabetes Mellitus, Type 1/epidemiology
- Diabetes Mellitus, Type 1/physiopathology
- Diabetes Mellitus, Type 2/blood
- Diabetes Mellitus, Type 2/complications
- Diabetes Mellitus, Type 2/epidemiology
- Diabetes Mellitus, Type 2/physiopathology
- History, 20th Century
- History, 21st Century
- Humans
- Prevalence
- Sleep/physiology
- Sleep Wake Disorders/complications
- Sleep Wake Disorders/epidemiology
- Time Factors
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Affiliation(s)
- G M Nefs
- Department of Medical Psychology, Radboud Institute for Health Sciences, Radboud University Medical Centre, Nijmegen, The Netherlands
- Department of Medical and Clinical Psychology, Tilburg University, Centre of Research on Psychological and Somatic Disorders (CoRPS), Tilburg, The Netherlands
- Diabeter, National Treatment and Research Centre for Children, Adolescents and Young Adults with Type 1 Diabetes, Rotterdam, The Netherlands
| | - E Bazelmans
- Department of Medical Psychology, Radboud Institute for Health Sciences, Radboud University Medical Centre, Nijmegen, The Netherlands
| | - E Donga
- Elisabeth-TweeSteden Hospital, Tilburg, The Netherlands
| | - C J Tack
- Department of Internal Medicine, Radboud University Medical Centre, Nijmegen, The Netherlands
| | - B E de Galan
- Department of Internal Medicine, Radboud University Medical Centre, Nijmegen, The Netherlands
- Department of Internal Medicine, Maastricht UMC+, Maastricht, The Netherlands
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25
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Perfect MM. Sleep-related disorders in patients with type 1 diabetes mellitus: current insights. Nat Sci Sleep 2020; 12:101-123. [PMID: 32104119 PMCID: PMC7023878 DOI: 10.2147/nss.s152555] [Citation(s) in RCA: 26] [Impact Index Per Article: 5.2] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 06/12/2018] [Accepted: 01/21/2019] [Indexed: 12/11/2022] Open
Abstract
Type 1 diabetes mellitus (T1DM) is an autoimmune condition that results from destruction of beta cells in the pancreas. Several reviews have concluded that sleep contributes to poor glycemic control, diabetes management, and diabetes-related complications in individuals with T1DM and represents an untapped opportunity for intervention. However, at the current juncture, the American Diabetes Association's Standards of Medical Care are devoid of recommendations about how to address sleep in the management of T1DM. This article summarizes reviews of sleep in youth and adults with T1DM and empirical studies that have examined various sleep parameters ranging from sleep disturbances (general, perceived sleep quality, sleepiness, awakenings, and sleep efficiency), sleep duration, sleep consistency, sleep-disordered breathing (SDB), and sleep architecture. The data show that many individuals with T1DM sleep less than recommendations; individuals with the poorest sleep have difficulties with diabetes management; and sleep deficiency including SDB often corresponds to several disease morbidities (neuropathy, nephropathy, etc). Mixed findings exist regarding direct associations of various sleep parameters and glycemic control. SDB appears to be just as prevalent, if not more, than other conditions that have been recommended for universal screening in individuals with T1DM. The article concludes with recommendations for collaborative research efforts to further elucidate the role of sleep in diabetes-related outcomes; investigations to test behavioral strategies to increase sleep quantity and consistency; and considerations for clinical care to address sleep.
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Affiliation(s)
- Michelle M Perfect
- Department of Disability and Psychoeducational Studies, University of Arizona, Tucson, AZ, USA
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26
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Endothelial Dysfunction is Related to Glycemic Variability and Quality and Duration of Sleep in Adults With Type 1 Diabetes. J Cardiovasc Nurs 2019; 33:E21-E25. [PMID: 29629915 DOI: 10.1097/jcn.0000000000000485] [Citation(s) in RCA: 16] [Impact Index Per Article: 2.7] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Indexed: 11/26/2022]
Abstract
BACKGROUND Elevated cardiovascular disease risk in people with type 1 diabetes (T1DM) is incompletely understood. Glycemic control, glycemic variability, and sleep quality and duration may relate to cardiovascular disease risk in this population via endothelial dysfunction. OBJECTIVE The aim of this study was to examine relationships among glycemic control, glycemic variability, sleep quality and duration, and endothelial function in adults with T1DM. METHODS Endothelial function was measured using flow-mediated dilation. Glycemic control and glycemic variability were measured using A1C and a continuous glucose monitor, respectively; sleep quality and duration were measured with the Pittsburgh Sleep Quality Index. RESULTS Twenty subjects were recruited. Reduced flow-mediated dilation and higher glucose levels were associated with poorer sleep quality (r = -0.51, P = .01; r = 0.52, P = .03). Subjects with shorter sleep duration had greater glycemic variability. CONCLUSIONS Endothelial dysfunction (a precursor to cardiovascular disease) relates to glycemic control, glycemic variability, and sleep quality in T1DM.
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27
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Diabetes management mediates the association between sleep duration and glycemic control in youth with type 1 diabetes mellitus. Sleep Med 2019; 60:132-138. [DOI: 10.1016/j.sleep.2019.01.043] [Citation(s) in RCA: 20] [Impact Index Per Article: 3.3] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 07/16/2018] [Revised: 10/28/2018] [Accepted: 01/31/2019] [Indexed: 01/28/2023]
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28
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Cobry EC, Jaser SS. Brief Literature Review: The Potential of Diabetes Technology to Improve Sleep in Youth With Type 1 Diabetes and Their Parents: An Unanticipated Benefit of Hybrid Closed-Loop Insulin Delivery Systems. Diabetes Spectr 2019; 32:284-287. [PMID: 31462886 PMCID: PMC6695262 DOI: 10.2337/ds18-0098] [Citation(s) in RCA: 3] [Impact Index Per Article: 0.5] [Reference Citation Analysis] [Grants] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Indexed: 11/25/2022]
Affiliation(s)
- Erin C Cobry
- Department of Pediatrics, Vanderbilt University Medical Center, Nashville, TN
| | - Sarah S Jaser
- Department of Pediatrics, Vanderbilt University Medical Center, Nashville, TN
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29
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The Relationship Between Sleep Disturbance and Disease Activity in Pediatric Patients With Inflammatory Bowel Disease. J Pediatr Gastroenterol Nutr 2019; 68:237-243. [PMID: 30256267 PMCID: PMC6344283 DOI: 10.1097/mpg.0000000000002156] [Citation(s) in RCA: 10] [Impact Index Per Article: 1.7] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Indexed: 12/10/2022]
Abstract
OBJECTIVE The aim of this prospective cross sectional study was to assess the prevalence of sleep disturbance in children with inflammatory bowel disease (IBD), including the relationships between sleep, inflammatory markers, and disease activity of pediatric patients with IBD. METHODS Pediatric patients with IBD and parents were enrolled in the study. Patients completed the Pittsburgh Sleep Quality Index (PSQI), the Pediatric Daytime Sleepiness Scale, and the Adolescent Sleep Wake Scale (ASWS) surveys. Parents completed the Child Sleep Habits Questionnaire (CSHQ). Disease activity for Crohn disease (CD) was determined by the Pediatric Crohn Disease Activity Index and the Pediatric Ulcerative Colitis Activity Index was used to define disease activity in ulcerative colitis (UC)/indeterminate colitis patients. RESULTS Fifty-three pediatric patients with IBD (38 CD, 12 UC, and 3 indeterminate colitis) participated in the study. The significant correlations between the CSHQ and Pediatric Crohn Disease Activity Index (P = 0.002) and the PSQI and Pediatric Ulcerative Colitis Activity Index (P = 0.04) were found. Youth with UC and indeterminate colitis significantly reported more sleep disturbance than patients with CD, (P = 0.03, 0.05, and 0.04; PSQI, Pediatric Daytime Sleepiness Scale, ASWS, respectively). Patients self-reported significantly more sleep disturbance than was observed by parents (P < 0.0001). This study showed the significant correlations between CSHQ score compared to erythrocyte sedimentation rate and albumin (P = 0.001 and 0.03, respectively). CONCLUSIONS Results suggest that increased disease activity is associated with adverse effects on sleep quality. Based on the results of this study, pediatric patients with IBD should be screened for sleep disturbance.
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30
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Monzon A, McDonough R, Meltzer LJ, Patton SR. Sleep and type 1 diabetes in children and adolescents: Proposed theoretical model and clinical implications. Pediatr Diabetes 2019; 20:78-85. [PMID: 30447038 DOI: 10.1111/pedi.12797] [Citation(s) in RCA: 29] [Impact Index Per Article: 4.8] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 05/08/2018] [Revised: 10/17/2018] [Accepted: 10/23/2018] [Indexed: 01/01/2023] Open
Abstract
Youth with type 1 diabetes mellitus (T1D) experience more sleep disturbances and shorter sleep durations compared to their healthy peers. Researchers have now uncovered the negative mental health and physical health outcomes associated with poor sleep in youth with T1D. The field of T1D sleep research currently operates under the broad notion that sleep behaviors impact treatment adherence, which ultimately lead to worse long-term health outcomes. This model however does not explain how behavior influences T1D management and sleep outcomes on a day-to-day basis, leading to difficulties in providing tailored treatment recommendations. In this review, we present a theoretical framework that describes the recursive cycle between sleep behaviors, T1D outcomes, and symptoms of negative affect/stress over a 24-hour period. This model is guided by the sleep literature, showing a clear relationship between poor sleep and negative affect, and the T1D literature demonstrating a link between poor sleep and disease management for youth with T1D. Further, emerging literature indicates a need for additional parent sleep assessment considering that T1D management and fear of hypoglycemia negatively impact parent sleep behaviors. Recommendations are provided to move the field toward effective intervention studies and new areas of research to evaluate and modify the proposed model.
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Affiliation(s)
- Alexandra Monzon
- Clinical Child Psychology Program, University of Kansas, Lawrence, Kansas
| | - Ryan McDonough
- Division of Endocrinology & Diabetes, Department of Pediatrics, Children's Mercy-Kansas City, Kansas City, Missouri
| | - Lisa J Meltzer
- Department of Pediatrics, National Jewish Health, Denver, Colorado
| | - Susana R Patton
- Department of Pediatrics, University of Kansas Medical Center, Kansas City, Kansas
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31
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Characterization of abnormal sleep patterns in patients with obesity, type 2 diabetes, or combined. ALEXANDRIA JOURNAL OF MEDICINE 2018. [DOI: 10.1016/j.ajme.2017.10.004] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.1] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Indexed: 11/20/2022] Open
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32
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Martyn-Nemeth P, Phillips SA, Mihailescu D, Farabi SS, Park C, Lipton R, Idemudia E, Quinn L. Poor sleep quality is associated with nocturnal glycaemic variability and fear of hypoglycaemia in adults with type 1 diabetes. J Adv Nurs 2018; 74:2373-2380. [PMID: 29917259 DOI: 10.1111/jan.13765] [Citation(s) in RCA: 32] [Impact Index Per Article: 4.6] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 12/02/2017] [Revised: 04/05/2018] [Accepted: 06/05/2018] [Indexed: 01/20/2023]
Abstract
AIMS To examine sleep quality and its associations with glycaemic control, glycaemic variability (GV), and fear of hypoglycaemia (FOH) in adults with type 1 diabetes. BACKGROUND Poor sleep quality has negative health consequences and is a frequent complaint among adults with type 1 diabetes. Sleep quality in adults with type 1 diabetes is likely affected by glucose levels as well as stressors associated with managing a chronic condition. DESIGN A retrospective secondary analysis of pooled data from two previous cross-sectional studies was conducted. METHODS We examined subjective sleep quality, FOH; objective measures of glycaemic control (HbA1c); and GV (3-day continuous glucose monitoring) in 48 men and women aged 18-45 years with type 1 diabetes. The data were collected over 3 years in 2013-2016. RESULTS/FINDINGS Poor sleep quality was reported by 46% of patients. Those with poor sleep quality had significantly greater nocturnal GV and FOH. Nocturnal GV and FOH were significantly associated with poor sleep quality. The interaction effect of GV and FOH was significant. CONCLUSION These findings suggest that glycaemic control and FOH are targets for intervention to improve sleep quality in those with type 1 diabetes.
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Affiliation(s)
- Pamela Martyn-Nemeth
- Department of Biobehavioral Health Science, College of Nursing, University of Illinois at Chicago, Chicago, Illinois
| | - Shane A Phillips
- Department of Physical Therapy, College of Applied Health Sciences, University of Illinois at Chicago, Chicago, Illinois.,College of Medicine, Endocrinology, Diabetes & Metabolism, University of Illinois at Chicago, Chicago, Illinois
| | - Dan Mihailescu
- College of Medicine, Endocrinology, Diabetes & Metabolism, University of Illinois at Chicago, Chicago, Illinois
| | - Sarah S Farabi
- Division of Endocrinology, Metabolism & Diabetes, School of Medicine, University of Colorado, Anschutz Medical Campus, Aurora, Colorado
| | - Chang Park
- Department of Biobehavioral Health Science, College of Nursing, University of Illinois at Chicago, Chicago, Illinois
| | - Rebecca Lipton
- Departments of Pediatrics and Public Health Sciences, University of Chicago, Chicago, Illinois
| | - Esema Idemudia
- Department of Biobehavioral Health Science, College of Nursing, University of Illinois at Chicago, Chicago, Illinois
| | - Laurie Quinn
- Department of Biobehavioral Health Science, College of Nursing, University of Illinois at Chicago, Chicago, Illinois
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33
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Kostkova M, Durdik P, Ciljakova M, Vojtkova J, Sujanska A, Pozorciakova K, Snahnicanova Z, Jancinova M, Banovcin P. Short-term metabolic control and sleep in children and adolescents with type 1 diabetes mellitus. J Diabetes Complications 2018; 32:580-585. [PMID: 29709336 DOI: 10.1016/j.jdiacomp.2018.03.010] [Citation(s) in RCA: 11] [Impact Index Per Article: 1.6] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 06/29/2017] [Revised: 12/14/2017] [Accepted: 03/17/2018] [Indexed: 12/15/2022]
Abstract
AIMS The aim of this study was to examine sleep in T1D children and in healthy controls by polysomnographic (PSG) examination and to determine the influence of short-term metabolic compensation on sleep quality and sleep disordered breathing (SDB). METHODS The prospective cross-sectional study included 44 T1D subjects and 60 healthy controls, aged 10-19 years. Subjects underwent anthropometric measurements, laboratory testing and standard overnight in-laboratory video polysomnography with continuous glucose monitoring (CGM). RESULTS No significant differences were found in total sleep time, sleep efficiency, percentage of sleep stages and respiratory parameters between T1D and healthy group. T1D children with more optimal short-term metabolic control (AvgSG < 10 mmol/l, n = 18) had a significantly lower apnea-hypopnea index (AHI) (0.3(0-0.5) vs. 0.6 (0.2-0.9) events/h, p < 0.05)and respiratory arousal index (0(0-0,1) vs. 0.2(0-0.3)), p < 0.01) compared to children with suboptimal short-term control(n = 26), no significant differences were found in parameters of sleep architecture. Obstructive sleep apnea (OSA) was diagnosed in only one T1D patient, nine T1D children had mild central apnea. CONCLUSIONS There may be an association between short-term metabolic compensation and SDB in T1D children without chronic complications, obesity or overweight and hypoglycemia. Further research is needed to confirm this result.
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Affiliation(s)
- Martina Kostkova
- Department of Pediatrics, Comenius University Bratislava, Jessenius Faculty of Medicine and University Hospital, 036 01 Martin, Slovakia
| | - Peter Durdik
- Department of Pediatrics, Comenius University Bratislava, Jessenius Faculty of Medicine and University Hospital, 036 01 Martin, Slovakia.
| | - Miriam Ciljakova
- Department of Pediatrics, Comenius University Bratislava, Jessenius Faculty of Medicine and University Hospital, 036 01 Martin, Slovakia; National Endocrinological and Diabetes Institute in Lubochna, Slovakia
| | - Jarmila Vojtkova
- Department of Pediatrics, Comenius University Bratislava, Jessenius Faculty of Medicine and University Hospital, 036 01 Martin, Slovakia
| | - Anna Sujanska
- Department of Pediatrics, Comenius University Bratislava, Jessenius Faculty of Medicine and University Hospital, 036 01 Martin, Slovakia
| | - Katarina Pozorciakova
- Department of Pediatrics, Comenius University Bratislava, Jessenius Faculty of Medicine and University Hospital, 036 01 Martin, Slovakia
| | - Zuzana Snahnicanova
- Department of Pediatrics, Comenius University Bratislava, Jessenius Faculty of Medicine and University Hospital, 036 01 Martin, Slovakia; Division of Oncology, Biomedical Center Martin JFM CU, Jessenius Faculty of Medicine in Martin, Comenius University in Bratislava, Mala Hora 4C, 036 01 Martin, Slovakia
| | - Maria Jancinova
- Department of Pediatrics, Comenius University Bratislava, Jessenius Faculty of Medicine and University Hospital, 036 01 Martin, Slovakia
| | - Peter Banovcin
- Department of Pediatrics, Comenius University Bratislava, Jessenius Faculty of Medicine and University Hospital, 036 01 Martin, Slovakia.
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34
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Patel NJ, Savin KL, Kahanda SN, Malow BA, Williams LA, Lochbihler G, Jaser SS. Sleep habits in adolescents with type 1 diabetes: Variability in sleep duration linked with glycemic control. Pediatr Diabetes 2018; 19:10.1111/pedi.12689. [PMID: 29708297 PMCID: PMC6207484 DOI: 10.1111/pedi.12689] [Citation(s) in RCA: 49] [Impact Index Per Article: 7.0] [Reference Citation Analysis] [Abstract] [Key Words] [Grants] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 02/08/2018] [Revised: 04/17/2018] [Accepted: 04/24/2018] [Indexed: 11/29/2022] Open
Abstract
OBJECTIVE To describe adolescents' sleep on school and weekend nights using multiple methods and to examine the links between sleep variability, quality, and duration with diabetes indicators. METHODS Adolescents with type 1 diabetes (N = 65, mean age = 15.0, 52.3% female, mean HbA1c = 8.9% or 74 mmol/mol) wore an actigraph and kept daily diaries recording sleep, activities, and blood glucose monitoring (BGM) habits for at least 7 days. Average daily BGM and blood glucose (BG) levels were obtained through glucometer downloads. HbA1c was obtained as part of clinic visits. Adolescents completed a sleep quality questionnaire (Pittsburgh sleep quality index [PSQI]), and adolescents and caregivers reported on adherence to diabetes treatment. RESULTS Adolescents reported a mean PSQI global score of 5.37, which is above the clinical cutoff for poor sleep quality. Actigraphy data revealed that mean adolescent total sleep time was 6:54 (h:min), and participants slept more on weekend nights than on school nights (P < .001). Additionally, variability in sleep duration was significantly related to HbA1c, frequency of BGM, and average BG. Total sleep time and self-reported sleep quality were not significantly associated with adherence or glycemic control. CONCLUSIONS Few adolescents with type 1 diabetes met recommendations for sleep duration, and many reported poor sleep quality. We identified significant associations between variability in sleep duration with poorer glycemic control and less frequent BGM, supporting the need to consider sleep patterns as a modifiable factor that may affect adherence and glycemic control.
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Affiliation(s)
- Niral J Patel
- Pediatric Endocrinology and Diabetes, Vanderbilt University Medical Center, Nashville, Tennessee
| | - Kimberly L Savin
- Pediatric Endocrinology and Diabetes, Vanderbilt University Medical Center, Nashville, Tennessee
| | - Sachini N Kahanda
- Pediatric Endocrinology and Diabetes, Vanderbilt University Medical Center, Nashville, Tennessee
| | - Beth A Malow
- Pediatric Endocrinology and Diabetes, Vanderbilt University Medical Center, Nashville, Tennessee
| | - Lauren A Williams
- Pediatric Endocrinology and Diabetes, Vanderbilt University Medical Center, Nashville, Tennessee
| | - Gray Lochbihler
- Pediatric Endocrinology and Diabetes, Vanderbilt University Medical Center, Nashville, Tennessee
| | - Sarah S Jaser
- Pediatric Endocrinology and Diabetes, Vanderbilt University Medical Center, Nashville, Tennessee
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35
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Perez KM, Hamburger ER, Lyttle M, Williams R, Bergner E, Kahanda S, Cobry E, Jaser SS. Sleep in Type 1 Diabetes: Implications for Glycemic Control and Diabetes Management. Curr Diab Rep 2018; 18:5. [PMID: 29399719 PMCID: PMC5842802 DOI: 10.1007/s11892-018-0974-8] [Citation(s) in RCA: 57] [Impact Index Per Article: 8.1] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Indexed: 12/21/2022]
Abstract
PURPOSE OF REVIEW To highlight recent findings from studies of sleep in type 1 diabetes (T1D), with a focus on the role of sleep in self-management, the cognitive and psychosocial outcomes related to sleep disturbances, and factors associated with sleep disturbances specific to T1D. RECENT FINDINGS People with T1D experience higher rates of sleep disturbances than people without diabetes, and these disturbances have negative implications for glycemic control and diabetes management, as well as psychosocial and cognitive outcomes. Inconsistent sleep timing (bedtime and wake time) has emerged as a potential target for interventions, as variability in sleep timing has been linked with poorer glycemic control and adherence to treatment. Sleep-promoting interventions and new diabetes technology have the potential to improve sleep in people with T1D. Sleep is increasingly considered a critical factor in diabetes management, but more multi-method and longitudinal research is needed. We emphasize the importance of sufficient and consistent sleep for people with T1D, and the need for providers to routinely assess sleep among patients with T1D.
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Affiliation(s)
- Katia M Perez
- Wake Forest School of Medicine, Winston-Salem, NC, USA
| | - Emily R Hamburger
- Vanderbilt University Medical Center, Village at Vanderbilt, 1500 21st Ave. South, Suite 1514, Nashville, TN, 37212, USA
| | - Morgan Lyttle
- Vanderbilt University Medical Center, Village at Vanderbilt, 1500 21st Ave. South, Suite 1514, Nashville, TN, 37212, USA
| | - Rodayne Williams
- Vanderbilt University Medical Center, Village at Vanderbilt, 1500 21st Ave. South, Suite 1514, Nashville, TN, 37212, USA
| | - Erin Bergner
- Vanderbilt University Medical Center, Village at Vanderbilt, 1500 21st Ave. South, Suite 1514, Nashville, TN, 37212, USA
| | - Sachini Kahanda
- Vanderbilt University Medical Center, Village at Vanderbilt, 1500 21st Ave. South, Suite 1514, Nashville, TN, 37212, USA
| | - Erin Cobry
- Vanderbilt University Medical Center, Village at Vanderbilt, 1500 21st Ave. South, Suite 1514, Nashville, TN, 37212, USA
| | - Sarah S Jaser
- Vanderbilt University Medical Center, Village at Vanderbilt, 1500 21st Ave. South, Suite 1514, Nashville, TN, 37212, USA.
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36
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Adler A, Gavan MY, Tauman R, Phillip M, Shalitin S. Do children, adolescents, and young adults with type 1 diabetes have increased prevalence of sleep disorders? Pediatr Diabetes 2017; 18:450-458. [PMID: 27488802 DOI: 10.1111/pedi.12419] [Citation(s) in RCA: 25] [Impact Index Per Article: 3.1] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 04/09/2016] [Revised: 06/25/2016] [Accepted: 06/29/2016] [Indexed: 11/28/2022] Open
Abstract
BACKGROUND Sleep has been shown to impact glucose regulation, and may be altered in persons with type 1 diabetes (T1D). OBJECTIVE To assess sleep characteristics in T1D patients and the possible association between sleep disturbances and diabetes-related variables. SUBJECTS AND METHODS In a cross-sectional study in 154 young patients with T1D and 154 age-range-matched nondiabetic controls subjective sleep characteristics were assessed using validated questionnaires: Sleep Disturbance Scale for Children (SDSC), Adolescent Sleep-Wake Scale (ASWS), Pittsburgh Sleep Quality Index (PSQI), Epworth Sleepiness Scale (ESS). Clinical and disease-related variables were obtained from medical charts. RESULTS Sleep disorders were frequent in all age groups, with no significant difference in prevalence or total scores of the SDSC, ASWS, PSQI, or ESS between the patients and the controls. In T1D children, SDSC score was significantly higher in those using continuous glucose monitoring (CGM) vs glucose meters (P = .042). The score of disorders related to "initiating and maintaining sleep" was significantly higher in those treated with pumps vs patients treated with injections (P = .014), in those using CGM vs glucose meters (P = .02), and in those with nocturnal hypoglycemia vs those without (P = .023). The percentage of children with excessive daytime sleepiness was significantly lower in patients vs controls (P = .035). No significant differences were found in the other two age groups. CONCLUSIONS/INTERPRETATION The prevalence of sleep disorders among most of the young T1D patients was no higher than in the nondiabetic population. Studies using objective sleep measures are warranted to further assess sleep quality in T1D patients.
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Affiliation(s)
- Avital Adler
- Sackler Faculty of Medicine, Tel Aviv University, Tel Aviv, Israel
| | - Michal-Yackobovitz Gavan
- The Jesse Z and Lea Shafer Institute of Endocrinology and Diabetes, National Center for Childhood Diabetes, Schneider Children's Medical Center of Israel, Petach Tikva, Israel
| | - Riva Tauman
- Sackler Faculty of Medicine, Tel Aviv University, Tel Aviv, Israel.,Department of Pediatric Pulmonology, Critical Care and Sleep Medicine, Dana Children's Hospital, Tel Aviv Sourasky Medical Center, Tel Aviv, Israel
| | - Moshe Phillip
- Sackler Faculty of Medicine, Tel Aviv University, Tel Aviv, Israel.,The Jesse Z and Lea Shafer Institute of Endocrinology and Diabetes, National Center for Childhood Diabetes, Schneider Children's Medical Center of Israel, Petach Tikva, Israel
| | - Shlomit Shalitin
- Sackler Faculty of Medicine, Tel Aviv University, Tel Aviv, Israel.,The Jesse Z and Lea Shafer Institute of Endocrinology and Diabetes, National Center for Childhood Diabetes, Schneider Children's Medical Center of Israel, Petach Tikva, Israel
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37
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McDonough RJ, Clements MA, DeLurgio SA, Patton SR. Sleep duration and its impact on adherence in adolescents with type 1 diabetes mellitus. Pediatr Diabetes 2017; 18:262-270. [PMID: 27028035 PMCID: PMC6941140 DOI: 10.1111/pedi.12381] [Citation(s) in RCA: 43] [Impact Index Per Article: 5.4] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 08/19/2015] [Revised: 01/21/2016] [Accepted: 02/24/2016] [Indexed: 02/06/2023] Open
Abstract
BACKGROUND Adherence to the type 1 diabetes (T1D) regimen, while predictive of glycemic control, decreases during adolescence. For adolescents, attaining adequate sleep is an additional challenge. This study evaluates the impact of sleep on adherence in teens with T1D. SUBJECTS Forty-five adolescents aged 12-18 yr, with T1D for at least 6 months while on insulin pump therapy. METHODS Adolescents logged their sleep on a written diary for 2 wk. Corresponding insulin pump/glucometer downloads as well as sleep habit questionnaires were also obtained. RESULTS Data from 20 girls and 25 boys, with a mean age of 15 ± 1.6 yr and mean glycated hemoglobin of 8.7 ± 1.1% (72 mmol/mol), were analyzed. Overall, average sleep was 8.6 ± 0.9 h per night. Sleep durations were compared to the next day's frequency of self-monitored blood glucose (SMBG) and total daily insulin bolus frequency. Associations were found between sleep duration and youths' SMBG and insulin bolus frequencies (p < 0.03 and p < 0.001, respectively). Specifically, a 15- and 20-min increase in sleep was associated with one additional SMBG check and one additional insulin bolus, respectively. CONCLUSION Analyses suggest an associated increase in T1D self-management behaviors in youths with increased sleep duration. These findings highlight the importance of assessing sleep in clinical practice, and encourage further research to examine effective strategies to address sleep hygiene as part of routine diabetes management.
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Affiliation(s)
- Ryan J. McDonough
- Department of Pediatrics, Division of Endocrinology/Diabetes, Children’s Mercy – Kansas City, Kansas City, MO, USA, 64111
| | - Mark A. Clements
- Department of Pediatrics, Division of Endocrinology/Diabetes, Children’s Mercy – Kansas City, Kansas City, MO, USA, 64111;,Department of Pediatrics, University of Kansas Medical Center, Kansas City, KS, USA, 66160;,Department of Pediatrics, University of Missouri Kansas City, Kansas City, MO, USA, 64108
| | - Stephen A. DeLurgio
- Center for Health Outcomes and Health Services Research, Children’s Mercy – Kanasas City, Kansas City, MO, USA, 64108
| | - Susana R. Patton
- Center for Children’s Healthy Lifestyles and Nutrition, Children’s Mercy – Kansas City, Kansas City, MO, USA 64108 & University of Kansas Medical Center, Kansas City, KS, USA, 66160;,Department of Pediatrics, Division of Behavioral Pediatrics, University of Kansas Medical Center, Kansas City, KS, USA, 66160
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38
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Taleb N, Haidar A, Messier V, Gingras V, Legault L, Rabasa-Lhoret R. Glucagon in artificial pancreas systems: Potential benefits and safety profile of future chronic use. Diabetes Obes Metab 2017; 19:13-23. [PMID: 27629286 DOI: 10.1111/dom.12789] [Citation(s) in RCA: 42] [Impact Index Per Article: 5.3] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 06/08/2016] [Revised: 09/09/2016] [Accepted: 09/11/2016] [Indexed: 12/17/2022]
Abstract
The role of glucagon in the pathophysiology of diabetes has long been recognized, although its approved clinical use has so far been limited to the emergency treatment of severe hypoglycaemia. A novel use of glucagon as intermittent mini-boluses is proposed in the dual-hormone version (insulin and glucagon) of the external artificial pancreas. Short-term studies suggest that the incorporation of glucagon into artificial pancreas systems has the potential to further decrease hypoglycaemic risk and improve overall glucose control; however, the potential long-term safety and benefits also need to be investigated given the recognized systemic effects of glucagon. In the present report, we review the available animal and human data on the physiological functions of glucagon, as well as its pharmacological use, according to dosing and duration (acute and chronic). Along with its main role in hepatic glucose metabolism, glucagon affects the cardiovascular, renal, pulmonary and gastrointestinal systems. It has a potential role in weight reduction through its central satiety function and its role in increasing energy expenditure. Most of the pharmacological studies investigating the effects of glucagon have used doses exceeding 1 mg, in contrast to the mini-boluses used in the artificial pancreas. The available data are reassuring but comprehensive human studies using small but chronic glucagon doses that are close to the physiological ranges are lacking. We propose a list of variables that could be monitored during long-term trials of the artificial pancreas. Such trials should address the questions about the risk-benefit ratio of chronic glucagon use.
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Affiliation(s)
- Nadine Taleb
- Metabolic diseases unit, Institut de recherches cliniques de Montréal, Montréal, Québec, Canada
- Department of Biomedical Sciences, Faculty of Medicine, Édouard-Montpetit, Université de Montréal, Montréal, Québec, Canada
| | - Ahmad Haidar
- Department of Biomedical Engineering, Faculty of Medicine, McGill University, Montréal, Québec, Canada
- Division of Endocrinology, Department of Medicine, Faculty of Medicine, McGill University, Montréal, Québec, Canada
| | - Virginie Messier
- Metabolic diseases unit, Institut de recherches cliniques de Montréal, Montréal, Québec, Canada
| | - Véronique Gingras
- Metabolic diseases unit, Institut de recherches cliniques de Montréal, Montréal, Québec, Canada
- Nutrition Department, Faculty of Medicine, Université de Montréal, Montréal, Québec, Canada
| | - Laurent Legault
- Montreal Children's Hospital, Department of Pediatrics, McGill University Health Centre, Montréal, Québec, Canada
| | - Rémi Rabasa-Lhoret
- Metabolic diseases unit, Institut de recherches cliniques de Montréal, Montréal, Québec, Canada
- Montreal Diabetes Research Center, Montréal, Québec, Canada
- Nutrition Department, Faculty of Medicine, Université de Montréal, Montréal, Québec, Canada
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39
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Farabi SS, Carley DW, Quinn L. Glucose Variations and Activity Are Strongly Coupled in Sleep and Wake in Young Adults With Type 1 Diabetes. Biol Res Nurs 2016; 19:249-257. [PMID: 28413931 DOI: 10.1177/1099800416685177] [Citation(s) in RCA: 17] [Impact Index Per Article: 1.9] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/16/2022]
Abstract
BACKGROUND Glucose variations are common throughout sleep and wakefulness in people with type 1 diabetes mellitus (T1DM). The objective of this investigation was to characterize the time-varying coupling between glucose and unstructured physical activity over a 60-hr period in young adults with T1DM. The hypothesis was that coupling would differ during sleep versus wakefulness and would exhibit circadian variations. METHOD Young adults with T1DM treated with an insulin pump participated in the study. Glucose variations were monitored with a continuous glucose monitoring system, and activity was assessed using an activity-monitoring band worn on the nondominant wrist. Simultaneous glucose and physical activity data across a continuous 60-hr period were used for analysis. Wavelet coherence analysis was employed to quantify the coupling between physical activity and glucose. Cosinor analysis was used to assess whether glucose/activity coherence exhibited significant circadian variations. RESULTS Participants comprised 23 adults, aged 18-30 years, with T1DM. Coherence analysis demonstrated substantial coupling between physical activity and glucose variations during both wakefulness and sleep. For rapid (10-30 min) fluctuations, mean coherence was higher during sleep than wakefulness ( F = 10.86, p = .003). Rapid glucose variations consistently led to changes in activity ( p = .001) during sleep but not during wake. Cosinor analysis revealed significant circadian modulation of glucose/activity coupling, especially for fluctuation periods 2-4 hr. CONCLUSIONS Unstructured physical activity and glucose variations demonstrated strong time- and frequency-dependent coupling over a 60-hr period in young adults with T1DM, with sleep/wake differences and circadian modulation evident in this relationship.
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Affiliation(s)
- Sarah S Farabi
- 1 Endocrinology, Metabolism & Diabetes, Division of Medicine, University of Colorado Anschutz Medical Campus, Aurora, CO, USA
| | - David W Carley
- 2 Center for Narcolepsy, Sleep and Health Research, University of Illinois at Chicago, Chicago, IL, USA.,3 Department of Biobehavioral Health Science, University of Illinois at Chicago, Chicago, IL, USA.,4 Department of Medicine, University of Illinois at Chicago, Chicago, IL, USA.,5 Department of Bioengineering, University of Illinois at Chicago, Chicago, IL, USA
| | - Lauretta Quinn
- 3 Department of Biobehavioral Health Science, University of Illinois at Chicago, Chicago, IL, USA
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40
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Reutrakul S, Thakkinstian A, Anothaisintawee T, Chontong S, Borel AL, Perfect MM, Janovsky CCPS, Kessler R, Schultes B, Harsch IA, van Dijk M, Bouhassira D, Matejko B, Lipton RB, Suwannalai P, Chirakalwasan N, Schober AK, Knutson KL. Sleep characteristics in type 1 diabetes and associations with glycemic control: systematic review and meta-analysis. Sleep Med 2016; 23:26-45. [PMID: 27692274 PMCID: PMC9554893 DOI: 10.1016/j.sleep.2016.03.019] [Citation(s) in RCA: 164] [Impact Index Per Article: 18.2] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 10/23/2015] [Revised: 02/29/2016] [Accepted: 03/25/2016] [Indexed: 01/22/2023]
Abstract
OBJECTIVES The association between inadequate sleep and type 2 diabetes has garnered much attention, but little is known about sleep and type 1 diabetes (T1D). Our objectives were to conduct a systematic review and meta-analysis comparing sleep in persons with and without T1D, and to explore relationships between sleep and glycemic control in T1D. METHODS Studies were identified from Medline and Scopus. Studies reporting measures of sleep in T1D patients and controls, and/or associations between sleep and glycemic control, were selected. RESULTS A total of 22 studies were eligible for the meta-analysis. Children with T1D had shorter sleep duration (mean difference [MD] = -26.4 minutes; 95% confidence interval [CI] = -35.4, -17.7) than controls. Adults with T1D reported poorer sleep quality (MD in standardized sleep quality score = 0.51; 95% CI = 0.33, 0.70), with higher scores reflecting worse sleep quality) than controls, but there was no difference in self-reported sleep duration. Adults with TID who reported sleeping >6 hours had lower hemoglobin A1c (HbA1c) levels than those sleeping ≤6 hours (MD = -0.24%; 95% CI = -0.47, -0.02), and participants reporting good sleep quality had lower HbA1c than those with poor sleep quality (MD = -0.19%; 95% CI = -0.30, -0.08). The estimated prevalence of obstructive sleep apnea (OSA) in adults with TID was 51.9% (95% CI = 31.2, 72.6). Patients with moderate-to-severe OSA had a trend toward higher HbA1c (MD = 0.39%, 95% CI = -0.08, 0.87). CONCLUSION T1D was associated with poorer sleep and high prevalence of OSA. Poor sleep quality, shorter sleep duration, and OSA were associated with suboptimal glycemic control in T1D patients.
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Affiliation(s)
- Sirimon Reutrakul
- Division of Endocrinology and Metabolism, Faculty of Medicine Ramathibodi Hospital, Mahidol University, Bangkok, Thailand.
| | - Ammarin Thakkinstian
- Section for Clinical Epidemiology and Biostatistics, Faculty of Ramathibodi Hospital, Mahidol University, Bangkok, Thailand
| | - Thunyarat Anothaisintawee
- Section for Clinical Epidemiology and Biostatistics, Faculty of Ramathibodi Hospital, Mahidol University, Bangkok, Thailand; Department of Family Medicine, Ramathibodi Hospital, Mahidol University, Bangkok, Thailand
| | - Sasipas Chontong
- Division of Endocrinology and Metabolism, Faculty of Medicine Ramathibodi Hospital, Mahidol University, Bangkok, Thailand
| | - Anne-Laure Borel
- Hypoxia Pathophysiology (HP2) Laboratory, INSERM U1042, Grenoble Alpes University, and Endocrinology Department, University Hospital, Grenoble, France
| | - Michelle M Perfect
- Department of Disability and Psychoeducational Studies, University of Arizona, Tucson, AZ, USA
| | | | - Romain Kessler
- Department of Pneumology, Hôpitaux Universitaires de Strasbourg, Strasbourg, France
| | - Bernd Schultes
- eSwiss Medical & Surgical Center, St. Gallen, Switzerland
| | - Igor Alexander Harsch
- Department of Internal Medicine 2, Thuringia Clinic Saalfeld, "Georgius Agricola", Saalfeld/Saale, Germany
| | - Marieke van Dijk
- Department of Endocrinology and Metabolic Diseases, Leiden University Medical Centre, Leiden, The Netherlands
| | - Didier Bouhassira
- INSERM U-987, Centre d'Evaluation et Traitement de la Douleur, CHU Ambroise Pare, APHP, Boulogne-Billancourt, France; Université Versailles-Saint-Quentin, Versailles, France
| | - Bartlomiej Matejko
- Department of Metabolic Diseases, Jagiellonian University Medical College, Krakow, Poland
| | - Rebecca B Lipton
- Institute for Endocrine Discovery and Clinical Care & Department of Health Studies, University of Chicago, Chicago, IL, USA
| | - Parawee Suwannalai
- Division of Allergy Immunology and Rheumatology, Faculty of Medicine Ramathibodi Hospital, Mahidol University, Bangkok, Thailand
| | - Naricha Chirakalwasan
- Division of Pulmonary and Critical Care Medicine, Department of Medicine, Faculty of Medicine, Chulalongkorn University, Bangkok, Thailand; Excellence Center for Sleep Disorders, King Chulalongkorn Memorial Hospital, Thai Red Cross Society, Bangkok, Thailand
| | - Anne-Katrin Schober
- Department of Internal Medicine, Regional Hospital of Feldbach-Fürstenfeld, Fürstenfeld, Austria
| | - Kristen L Knutson
- Section of Pulmonary and Critical Care, Department of Medicine, University of Chicago, Chicago, IL, USA
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Perfect MM, Beebe D, Levine-Donnerstein D, Frye SS, Bluez GP, Quan SF. The Development of a Clinically Relevant Sleep Modification Protocol for Youth with Type 1 Diabetes. CLINICAL PRACTICE IN PEDIATRIC PSYCHOLOGY 2016; 4:227-240. [PMID: 27747146 DOI: 10.1037/cpp0000145] [Citation(s) in RCA: 21] [Impact Index Per Article: 2.3] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 12/11/2022]
Abstract
Findings from type 2 diabetes research indicate that sleep is both a predictor of onset and a correlate of disease progression. However, the role sleep plays in glucose regulation and daytime functioning in youth with type 1 diabetes mellitus (T1DM) has not been systematically investigated. Nonetheless, preliminary findings have supported that various sleep parameters are strongly correlated to health-related and neurobehavioral outcomes in youth with T1DM. This suggests that improving sleep might reduce morbidity. A critical step in developing evidence-based guidelines regarding sleep in diabetes management is to first determine that sleep modification in natural settings is possible (i.e., instructing youth to have a healthy sleep opportunity leads to more total sleep time) and that an increased sleep duration impacts disease and psychosocial outcomes in these youth. This article describes the background, design, and feasibility of an ongoing randomized clinical trial that aims to examine if increasing sleep relative to youth's own sleep routines affects glucose control and daytime functioning.
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Affiliation(s)
- Michelle M Perfect
- Disability and Psychoeducational Studies, University of Arizona, Tucson, AZ
| | - Dean Beebe
- Department of Pediatrics, Cincinnati's Children's Hospital Medical Center, Cincinnati, OH
| | | | - Sara S Frye
- Disability and Psychoeducational Studies, University of Arizona, Tucson, AZ
| | - Grai P Bluez
- Disability and Psychoeducational Studies, University of Arizona, Tucson, AZ
| | - Stuart F Quan
- Arizona Respiratory Center, University of Arizona, Tucson, AZ; Division of Sleep Medicine, Harvard Medical School, Boston, MA
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EEG power and glucose fluctuations are coupled during sleep in young adults with type 1 diabetes. Clin Neurophysiol 2016; 127:2739-2746. [PMID: 27417046 DOI: 10.1016/j.clinph.2016.05.357] [Citation(s) in RCA: 17] [Impact Index Per Article: 1.9] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 03/04/2016] [Revised: 05/25/2016] [Accepted: 05/27/2016] [Indexed: 12/26/2022]
Abstract
OBJECTIVE To determine the coupling between brain activity and glucose variations during sleep in young adults with type 1 diabetes mellitus (T1DM). METHODS 27 participants, age 18-30, wore a continuous glucose monitoring system (CGMS) and underwent in-laboratory overnight polysomnography (PSG). Quantitative electroencephalogram (qEEG) metrics were determined from the PSG and included Delta, Theta, Alpha, Sigma, Beta and Gamma Band power at 5-min intervals. Wavelet Coherence Analysis was employed to determine the time varying and frequency specific coupling between glucose and EEG Band power. ANOVA was used to compare differences across fluctuation speeds and EEG bands. RESULTS There was a high degree of time varying and frequency specific coupling between glucose variations and EEG power in all EEG Bands during sleep. The average number of intervals of statistically significant coherence was highest for fluctuations periods between 10 and 30min in all Bands (p<0.0001 for each). Mean significant coherence was negatively correlated with hemoglobin A1c, a marker of glycemic control. CONCLUSIONS The relationship between glucose and EEG power during sleep is time varying and frequency dependent in young adults with T1DM. SIGNIFICANCE Understanding the time varying mutual relationship between glucose changes and brain activity during sleep may have implications for disease management in T1DM.
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43
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Chontong S, Saetung S, Reutrakul S. Higher sleep variability is associated with poorer glycaemic control in patients with type 1 diabetes. J Sleep Res 2016; 25:438-44. [PMID: 26912272 DOI: 10.1111/jsr.12393] [Citation(s) in RCA: 69] [Impact Index Per Article: 7.7] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 11/05/2015] [Accepted: 01/09/2016] [Indexed: 01/01/2023]
Abstract
Sleep disturbances have been linked to insulin resistance and poor glycaemic control in patients with type 2 diabetes. However, the data are limited in type 1 diabetes. Recently, varying day-to-day sleep schedules, i.e. sleep variability, have been associated with adverse metabolic profile in healthy individuals. This study explored whether sleep variability affects glycaemic control and insulin requirement in type 1 diabetes. Forty-one adult patients with type 1 diabetes wore an actigraphy for 5 nights. Standard deviation of sleep duration, efficiency and mid-sleep time were sleep variability parameters. Sleep apnoea risk and self-reported sleep quality were assessed by the Berlin questionnaire and Pittsburgh Sleep Quality Index. Haemoglobin A1c, diabetes complications and insulin regimen were obtained from medical records. After adjusting for neuropathic symptoms, sleep apnoea risk and poor self-reported sleep quality, higher sleep variability was significantly associated with poorer glycaemic control (standard deviation of sleep duration, B = 0.100, P = 0.004; and standard deviation of mid-sleep time, B = 0.068, P = 0.04). In addition, standard deviations of sleep duration and mid-sleep time were highly correlated, suggesting that participants changed their sleep duration along with sleep timing. After adjusting for covariates, the standard deviation of sleep duration (P = 0.009) and standard deviation of mid-sleep time (P = 0.012) were associated with higher insulin requirement. In summary, higher sleep variability, which likely reflects sleep deprivation alternating with sleep compensation along with shifts in their circadian timing, was associated with poorer glycaemic control and higher insulin requirement in patients with type 1 diabetes. Increased sleep regularity may improve metabolic control in type 1 diabetes.
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Affiliation(s)
- Sasipas Chontong
- Section of Endocrinology, Department of Medicine, Faculty of Medicine Ramathibodi Hospital, Mahidol University, Bangkok, Thailand
| | - Sunee Saetung
- Section of Endocrinology, Department of Medicine, Faculty of Medicine Ramathibodi Hospital, Mahidol University, Bangkok, Thailand
| | - Sirimon Reutrakul
- Section of Endocrinology, Department of Medicine, Faculty of Medicine Ramathibodi Hospital, Mahidol University, Bangkok, Thailand
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Abstract
IN BRIEF In people with type 1 diabetes, sleep may be disrupted as a result of both behavioral and physiological aspects of diabetes and its management. This sleep disruption may negatively affect disease progression and development of complications. This review highlights key research findings regarding sleep in people with type 1 diabetes.
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Affiliation(s)
- Sarah S Farabi
- Center for Narcolepsy, Sleep and Health Research, University of Illinois, Chicago, IL
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Farabi SS, Carley DW, Cinar A, Quinn L. Routine daily physical activity and glucose variations are strongly coupled in adults with T1DM. Physiol Rep 2015; 3:3/12/e12644. [PMID: 26660554 PMCID: PMC4760432 DOI: 10.14814/phy2.12644] [Citation(s) in RCA: 4] [Impact Index Per Article: 0.4] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 12/03/2022] Open
Abstract
Type 1 Diabetes (T1DM) is characterized by altered glucose homeostasis resulting in wide glucose variations throughout a 24‐h period. The relationship between routine daily physical activity and glucose variations has not been systematically investigated in adults with T1DM. The objectives of this study were to characterize and quantify the relationship between routine daily activity and glucose variations in a small group of adults with T1DM. Adults with T1DM treated with an insulin pump were recruited for the study. Over a 3‐day period, glucose variations were monitored with a continuous glucose monitoring system (CGMS) and routine daily physical activity was assessed using an accelerometer‐based physical activity‐monitoring band. Simultaneous glucose and physical activity data for one 24‐h period were used for analysis. Cross‐correlation function and wavelet coherence analyses were employed to quantify the coupling between physical activity and glucose. Twelve subjects were included in the analysis. Cross‐correlation function analysis revealed strong coupling between activity and glucose. Wavelet Coherence demonstrated that slower oscillations (120–340 min) of glucose and physical activity exhibited significantly greater coherence (F = 12.6, P < 0.0001) than faster oscillations (10 and 120 min). Physical activity and glucose demonstrate strong time and frequency‐dependent coupling throughout a 24‐h time period in adults with T1DM.
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Affiliation(s)
- Sarah S Farabi
- Center for Narcolepsy, Sleep and Health Research, University of Illinois at Chicago, Chicago, Illinois Department of Biobehavioral Health Science, University of Illinois at Chicago, Chicago, Illinois
| | - David W Carley
- Center for Narcolepsy, Sleep and Health Research, University of Illinois at Chicago, Chicago, Illinois Department of Biobehavioral Health Science, University of Illinois at Chicago, Chicago, Illinois Department of Medicine, University of Illinois at Chicago, Chicago, Illinois Department of Bioengineering, University of Illinois at Chicago, Chicago, Illinois
| | - Ali Cinar
- Ilinois Institute of Technology, Chicago, Illinois
| | - Lauretta Quinn
- Department of Biobehavioral Health Science, University of Illinois at Chicago, Chicago, Illinois
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Hazen RA, Fehr KK, Ievers-Landis CE, MacLeish SA. Sleep parameters and diabetes-related considerations for children and adolescents with Type 1 diabetes. ACTA ACUST UNITED AC 2015. [DOI: 10.2217/dmt.15.42] [Citation(s) in RCA: 2] [Impact Index Per Article: 0.2] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/21/2022]
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Rachmiel M, Cohen M, Heymen E, Lezinger M, Inbar D, Gilat S, Bistritzer T, Leshem G, Kan-Dror E, Lahat E, Ekstein D. Hyperglycemia is associated with simultaneous alterations in electrical brain activity in youths with type 1 diabetes mellitus. Clin Neurophysiol 2015; 127:1188-1195. [PMID: 26277825 DOI: 10.1016/j.clinph.2015.07.011] [Citation(s) in RCA: 12] [Impact Index Per Article: 1.2] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 11/22/2014] [Revised: 06/27/2015] [Accepted: 07/12/2015] [Indexed: 01/29/2023]
Abstract
OBJECTIVE To assess the association between hyperglycemia and electrical brain activity in type 1 diabetes mellitus (T1DM). METHODS Nine youths with T1DM were monitored simultaneously and continuously by EEG and continuous glucose monitor system, for 40 h. EEG powers of 0.5-80 Hz frequency bands in all the different brain regions were analyzed according to interstitial glucose concentration (IGC) ranges of 4-11 mmol/l, 11-15.5 mmol/l and >15.5 mmol/l. Analysis of variance was used to examine the differences in EEG power of each frequency band between the subgroups of IGC. Analysis was performed separately during wakefulness and sleep, controlling for age, gender and HbA1c. RESULTS Mean IGC was 11.49 ± 5.26 mmol/l in 1253 combined measurements. IGC>15.5 mmol/l compared to 4-11 mmol/l was associated during wakefulness with increased EEG power of low frequencies and with decreased EEG power of high frequencies. During sleep, it was associated with increased EEG power of low frequencies in all brain areas and of high frequencies in frontal and central areas. CONCLUSIONS Asymptomatic transient hyperglycemia in youth with T1DM is associated with simultaneous alterations in electrical brain activity during wakefulness and sleep. SIGNIFICANCE The clinical implications of immediate electrical brain alterations under hyperglycemia need to be studied and may lead to adaptations of management.
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Affiliation(s)
- M Rachmiel
- Pediatric Diabetes Service, Pediatric Division, Assaf Haroffeh Medical Center, Zerifin 70300, Israel; Sackler School of Medicine, Tel Aviv University, Israel
| | - M Cohen
- Pediatric Diabetes Service, Pediatric Division, Assaf Haroffeh Medical Center, Zerifin 70300, Israel; Sackler School of Medicine, Tel Aviv University, Israel
| | - E Heymen
- Sackler School of Medicine, Tel Aviv University, Israel; Pediatric Neurology Department, Assaf Haroffeh Medical Center, Zerifin 70300, Israel
| | - M Lezinger
- Pediatric Neurology Department, Assaf Haroffeh Medical Center, Zerifin 70300, Israel
| | - D Inbar
- Department of Neurology and Agnes Ginges Center of Human Neurogenetics, Hadassah-Hebrew University Medical Center, POB 12000, Jerusalem 91120, Israel
| | | | - T Bistritzer
- Pediatric Diabetes Service, Pediatric Division, Assaf Haroffeh Medical Center, Zerifin 70300, Israel; Sackler School of Medicine, Tel Aviv University, Israel
| | - G Leshem
- Pediatric Neurology Department, Assaf Haroffeh Medical Center, Zerifin 70300, Israel
| | - E Kan-Dror
- Pediatric Neurology Department, Assaf Haroffeh Medical Center, Zerifin 70300, Israel
| | - E Lahat
- Sackler School of Medicine, Tel Aviv University, Israel; Pediatric Neurology Department, Assaf Haroffeh Medical Center, Zerifin 70300, Israel
| | - D Ekstein
- Department of Neurology and Agnes Ginges Center of Human Neurogenetics, Hadassah-Hebrew University Medical Center, POB 12000, Jerusalem 91120, Israel.
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Hazen RA, Fehr KK, Fidler A, Cousino MK, MacLeish SA, Gubitosi-Klug R. Sleep disruption in adolescents with Type 1 diabetes mellitus: relationships with adherence and diabetes control. ACTA ACUST UNITED AC 2015. [DOI: 10.2217/dmt.15.18] [Citation(s) in RCA: 14] [Impact Index Per Article: 1.4] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/21/2022]
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Litmanovitch E, Geva R, Rachmiel M. Short and long term neuro-behavioral alterations in type 1 diabetes mellitus pediatric population. World J Diabetes 2015; 6:259-270. [PMID: 25789107 PMCID: PMC4360419 DOI: 10.4239/wjd.v6.i2.259] [Citation(s) in RCA: 18] [Impact Index Per Article: 1.8] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 08/28/2014] [Revised: 12/03/2014] [Accepted: 12/17/2014] [Indexed: 02/05/2023] Open
Abstract
Type 1 diabetes mellitus (T1DM) is one of the most prevalent chronic conditions affecting individuals under the age of 18 years, with increasing incidence worldwide, especially among very young age groups, younger than 5. There is still no cure for the disease, and therapeutic goals and guidelines are a challenge. Currently, despite T1DM intensive management and technological interventions in therapy, the majority of pediatric patients do not achieve glycemic control goals. This leads to a potential prognosis of long term diabetic complications, nephrological, cardiac, ophthalmological and neurological. Unfortunately, the neurological manifestations, including neurocognitive and behavioral complications, may present soon after disease onset, during childhood and adolescence. These manifestations may be prominent, but at times subtle, thus they are often not reported by patients or physicians as related to the diabetes. Furthermore, the metabolic mechanism for such manifestations has been inconsistent and difficult to interpret in practical clinical care, as reported in several reviews on the topic of brain and T1DM. However, new technological methods for brain assessment, as well as the introduction of continuous glucose monitoring, provide new insights and information regarding brain related manifestations and glycemic variability and control parameters, which may impact the clinical care of children and youth with T1DM. This paper provides a comprehensive review of the most recently reported behavioral, cognitive domains, sleep related, electrophysiological, and structural alterations in children and adolescences from a novel point of view. The review focuses on reported impairments based on duration of T1DM, its timeline, and modifiable disease related risk parameters. These findings are not without controversy, and limitations of data are presented in addition to recommendations for future research direction.
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Barone MTU, Wey D, Schorr F, Franco DR, Carra MK, Lorenzi Filho G, Menna-Barreto L. Sleep and glycemic control in type 1 diabetes. ARCHIVES OF ENDOCRINOLOGY AND METABOLISM 2015; 59:71-8. [DOI: 10.1590/2359-3997000000013] [Citation(s) in RCA: 31] [Impact Index Per Article: 3.1] [Reference Citation Analysis] [Track Full Text] [Subscribe] [Scholar Register] [Received: 06/11/2014] [Accepted: 10/24/2014] [Indexed: 11/22/2022]
Affiliation(s)
| | | | | | - Denise Reis Franco
- Associação de Diabetes Juvenil, Brazil; Centro de Pesquisas Clínicas, Brazil
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