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Moon AM, Lupu GV, Green EW, Deutsch-Link S, Henderson LM, Sanoff HK, Yanagihara TK, Kokabi N, Mauro DM, Barritt AS. Rural-Urban Disparities in Hepatocellular Carcinoma Deaths Are Driven by Hepatitis C-Related Hepatocellular Carcinoma. Am J Gastroenterol 2025:00000434-990000000-01703. [PMID: 40214295 DOI: 10.14309/ajg.0000000000003487] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Grants] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 12/09/2024] [Accepted: 03/28/2025] [Indexed: 05/11/2025]
Abstract
INTRODUCTION Recent data suggest emerging rural-urban disparities in hepatocellular carcinoma (HCC) burden in the United States. We aimed to assess (i) trends in rural vs urban HCC-related mortality and (ii) differences in underlying chronic liver disease etiologies contributing to HCC-related deaths. METHODS We used the National Vital Statistics System to examine crude and age-adjusted HCC death rates overall and by etiology for rural and urban residents from 2005 to 2023. Using the National Cancer Institute Joinpoint Trend Analysis Software, we identified statistically significant changes in annual percentage change (APC) in HCC mortality rates. RESULTS Examining mortality rates over time, average APC in HCC deaths was significantly higher in rural residents (crude average annual percentage change [AAPC] 4.64, 95% confidence interval [CI] 4.10, 5.34; age-adjusted AAPC 3.53, 95% CI 3.09, 4.07) compared with urban residents (crude AAPC 2.72, 95% CI 2.43, 3.01; age-adjusted AAPC 1.68, 95% CI 1.28, 2.13). Differences in HCC death rate changes were driven by a significantly greater recent decline in HCC cases from hepatitis C virus (HCV) in urban residents (crude APC -6.69, 95% CI -8.85, -5.30 from 2017 to 2023) compared with rural residents (crude APC -3.31, 95% CI -8.05, 0.73 from 2016 to 2023). DISCUSSION Annual increases in HCC deaths have been more pronounced in rural compared with urban populations. Deaths from HCV-related HCC have declined with a geographical disparity that favors urban populations, possibly driven by decreased access to HCV screening or availability of highly effective direct-acting antiviral therapies for rural residents. These findings underscore the need for targeted HCV screening and treatment strategies in rural populations in addition to ongoing strategies to combat alcohol use and metabolic diseases.
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Affiliation(s)
- Andrew M Moon
- Division of Gastroenterology and Hepatology, University of North Carolina at Chapel Hill School of Medicine, Chapel Hill, North Carolina, USA
- Lineberger Comprehensive Cancer Center, University of North Carolina, Chapel Hill, North Carolina, USA
| | - Gabriel V Lupu
- Division of Gastroenterology and Hepatology, University of North Carolina at Chapel Hill School of Medicine, Chapel Hill, North Carolina, USA
| | - Ellen W Green
- Division of Gastroenterology and Hepatology, University of North Carolina at Chapel Hill School of Medicine, Chapel Hill, North Carolina, USA
| | - Sasha Deutsch-Link
- Division of Gastroenterology and Hepatology, University of North Carolina at Chapel Hill School of Medicine, Chapel Hill, North Carolina, USA
| | - Louise M Henderson
- Lineberger Comprehensive Cancer Center, University of North Carolina, Chapel Hill, North Carolina, USA
- Department of Radiology, University of North Carolina, Chapel Hill, North Carolina, USA
| | - Hanna K Sanoff
- Lineberger Comprehensive Cancer Center, University of North Carolina, Chapel Hill, North Carolina, USA
- Department of Medicine, Division of Oncology, University of North Carolina at Chapel Hill School of Medicine, Chapel Hill, North Carolina, USA
| | - Ted K Yanagihara
- Lineberger Comprehensive Cancer Center, University of North Carolina, Chapel Hill, North Carolina, USA
- Department of Radiation Oncology, University of North Carolina, Chapel Hill, North Carolina, USA
| | - Nima Kokabi
- Division of Interventional Radiology, University of North Carolina at Chapel Hill School of Medicine, Chapel Hill, North Carolina, USA
| | - David M Mauro
- Division of Interventional Radiology, University of North Carolina at Chapel Hill School of Medicine, Chapel Hill, North Carolina, USA
| | - A Sidney Barritt
- Division of Gastroenterology and Hepatology, University of North Carolina at Chapel Hill School of Medicine, Chapel Hill, North Carolina, USA
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Johnson CR, Muhimpundu S, Han X, Mumma MT, Shrubsole MJ, Zheng W, Spalluto LB, Lipworth L, Sudenga SL. The Influence of Residential Segregation, Urbanicity, and Population Density on Hepatocellular Carcinoma Incidence among a Low Socioeconomic Population. Cancer Epidemiol Biomarkers Prev 2025; 34:348-354. [PMID: 39625692 PMCID: PMC11932245 DOI: 10.1158/1055-9965.epi-24-1119] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/31/2024] [Revised: 10/01/2024] [Accepted: 11/25/2024] [Indexed: 02/07/2025] Open
Abstract
BACKGROUND Hepatocellular carcinoma (HCC) is becoming a leading cause of cancer-related mortality in the United States, with notable disparities observed among racial and ethnic minorities. The objective of this study is to examine the association between social determinants of health (SDoH) and HCC incidence by race (White and Black individuals) using data from the Southern Community Cohort Study. METHODS The Southern Community Cohort Study is a prospective cohort study with participants recruited from 2002 to 2009. Incident HCC cases were identified during follow-up. Exposure measures, including residential segregation, social vulnerability, population density, rurality, and poverty, were assessed at baseline. Cox proportional hazards regression models were used to estimate HRs associated with SDoH by race with the adjustment of known HCC risk factors. RESULTS Among the 79,367 eligible participants, there were 491 incident HCC cases diagnosed, 378 of whom were in Black individuals. In Black individuals, increased population density and urban residency were associated with an increased risk of HCC, even after adjusting for potential confounders [HR = 1.49; 95% confidence interval (CI), 1.04-2.13; HR = 1.70; 95% CI, 1.20-2.41, respectively]. White individuals living in the least segregated areas (HR = 2.83; 95% CI, 1.39-5.78) and in urban settings (HR = 2.34; 95% CI, 1.17-4.65) had an increased HCC risk, whereas population density was not associated with risk. CONCLUSIONS We found that individuals residing in urban populations had an increased risk of HCC. These findings underscore the complex interplay of SDoH factors and geographic influences on HCC disparities. IMPACT Our findings highlight the need for targeted interventions and further research to address HCC health inequities.
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Affiliation(s)
- Corianne R. Johnson
- Department of Medicine, Vanderbilt University Medical Center, Nashville, TN, USA
| | - Sylvie Muhimpundu
- Department of Medicine, Vanderbilt University Medical Center, Nashville, TN, USA
| | - Xijing Han
- International Epidemiology Institute, Rockville, MD, USA
| | | | - Martha J. Shrubsole
- Department of Medicine, Vanderbilt University Medical Center, Nashville, TN, USA
- Vanderbilt-Ingram Cancer Center, Nashville, TN, USA
| | - Wei Zheng
- Department of Medicine, Vanderbilt University Medical Center, Nashville, TN, USA
- Vanderbilt-Ingram Cancer Center, Nashville, TN, USA
| | - Lucy B. Spalluto
- Vanderbilt-Ingram Cancer Center, Nashville, TN, USA
- Department of Radiology and Radiological Sciences, Vanderbilt University Medical Center, Nashville, TN, USA
- VA Tennessee Valley Healthcare System, Geriatric Research, Education, and Clinical Center, Nashville, TN, USA
| | - Loren Lipworth
- Department of Medicine, Vanderbilt University Medical Center, Nashville, TN, USA
- Vanderbilt-Ingram Cancer Center, Nashville, TN, USA
| | - Staci L. Sudenga
- Department of Medicine, Vanderbilt University Medical Center, Nashville, TN, USA
- Vanderbilt-Ingram Cancer Center, Nashville, TN, USA
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Ebrahim A, Sinha S, Adedipe I, Ahmad A, Amyotte M, Yang L, Elsewify O, Sachal SS, Fraulin FOG, Gabriel VA, Perez G, Johnston A. Rurality predisposes departure from gold-standard care, leading to delayed or accelerated access to surgery: insights from a scoping review. Can J Surg 2025; 68:E17-E31. [PMID: 39753325 PMCID: PMC11684926 DOI: 10.1503/cjs.000124] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Accepted: 09/17/2024] [Indexed: 01/23/2025] Open
Abstract
BACKGROUND Because tertiary centres are generally situated at urban sites, it is unclear whether patients in rural areas have the same access to surgical services that patients in urban areas do. We sought to map the North American evidence landscape of how rurality affects access to medically indicated surgeries and identify system-, patient-, and provider-level barriers that preclude urban-comparable care. METHODS We carried out a systematic search adhering to PRISMA for Scoping Reviews methodology across PubMed, MEDLINE, Scopus, and Web of Science, encompassing literature from the last 26 years (January 2023). Search terms included "rural population," "health care access," "surgical procedures," and "health disparities." We synthesized our findings using a narrative approach. RESULTS Of 13 897 identified studies, we included 71 publications, spanning a wide spectrum of surgical disciplines. Of these, 83% reported diminished and 17% reported accelerated access to surgery, and 30% reported an interaction between rurality with other social determinants of health, particularly age, sex and gender, and race and ethnicity. Of the studies that reported diminished access, top cited reasons included primary and specialist provider density, differences in patients' socioeconomic profiles, and provision of comparable counselling during surgical decisionmaking. Strikingly, a key driver of enhanced surgical access was an absence of specialized medical interventions leading to an overreliance on surgical alternatives. CONCLUSION Whether surgical access was diminished or accelerated, the net impact of rurality was a deviation from guideline-concordant care. A key implication of these findings is that reliance on surgical wait times alone can skew perception of surgical access, advocating for adoption of integrated quality-of-care metrics that better reflect access to comprehensive medical and surgical treatment programs. CONTEXTE Étant donné que les centres de soins tertiaires se trouvent généralement en milieu urbain, on peut se demander si l'accès aux services chirurgicaux est le même en région rurale qu'en milieu urbain. Nous avons voulu cartographier, preuve à l'appui, l'impact de la ruralité sur l'accès à des chirurgies médicalement indiquées en Amérique du Nord et identifier les obstacles, propres au système, à la patientèle et aux équipes soignantes, qui nuisent à la prestation des soins équivalents à ceux des milieux urbains. MÉTHODES: Nous avons procédé à une interrogation systématique (conforme à la Norme de réalisation de revue systématique de la littérature PRISMA) des bases de données PubMed, MEDLINE, Scopus et Web of Science regroupant la littérature des 26 dernières années (janvier 2023). Les mots clés de langue anglaise utilisés incluaient : « rural population », « health care access », « surgical procedures » et « health disparities ». Nous avons synthétisé nos observations au moyen d'une approche narrative. RÉSULTATS: Des 13 897 études recensées, nous avons retenu 71 publications abordant un vaste éventail de disciplines chirurgicales. Parmi ces publications, 83 % faisaient état d'un accès diminué, 17 % d'un accès plus rapide à la chirurgie, et 30 % d'un lien entre la ruralité et d'autres déterminants sociaux de la santé, notamment l'âge, le sexe et le genre, ainsi que la race et l'ethnicité. Selon les études ayant fait état d'un accès diminué, les principales raisons incluaient la densité des effectifs en médecine primaire et de spécialité, les différences de profils socioéconomiques de la patientèle et l'offre d'un counselling comparable lors du processus décisionnel concernant la chirurgie. À noter, l'un des principaux facteurs d'amélioration de l'accès aux soins chirurgicaux était l'absence d'interventions médicales spécialisées associées à une dépendance indue à l'endroit des solutions chirurgicales. CONCLUSION Que l'accès à la chirurgie ait été diminué ou accéléré, l'impact net de la ruralité a pris la forme d'un écart par rapport aux soins préconisés par les lignes directrices. Ces observations indiquent principalement que la dépendance à l'égard des temps d'attente en chirurgie seule peut fausser la perception quant à l'accès aux soins chirurgicaux, ce qui milite en faveur de l'adoption de paramètres de qualité de soins intégrés qui reflèteraient plus fidèlement l'accès à des programmes de traitements médicaux et chirurgicaux complets.
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Affiliation(s)
- Alisha Ebrahim
- From the Cumming School of Medicine, University of Calgary, Calgary, Alta. (Ebrahim, Sinha, Adedipe, Ahmad, Amyotte, Yang); the Canadian Global Surgery Trainees' Association affiliated with the International Student Surgical Network - InciSioN (Ebrahim, Sinha, Adedipe, Ahmad, Amyotte, Yang, Elsewify); the Faculty of Medicine and Health Sciences, Laval University, Québec City, Que. (Elsewify); the Division of Plastic and Reconstructive Surgery, University of Western Ontario, London, Ont. (Sachal); the Sections of Pediatric Surgery and Plastic Surgery, Department of Surgery, University of Calgary, Calgary, Alta. (Fraulin); the Departments of Clinical Neurosciences and Surgery, University of Calgary, Calgary, Alta. (Gabriel); the Department of Distributed Learning and Rural Initiatives, Cumming School of Medicine, University of Calgary, Calgary, Alta. (Perez, Johnston)
| | - Sarthak Sinha
- From the Cumming School of Medicine, University of Calgary, Calgary, Alta. (Ebrahim, Sinha, Adedipe, Ahmad, Amyotte, Yang); the Canadian Global Surgery Trainees' Association affiliated with the International Student Surgical Network - InciSioN (Ebrahim, Sinha, Adedipe, Ahmad, Amyotte, Yang, Elsewify); the Faculty of Medicine and Health Sciences, Laval University, Québec City, Que. (Elsewify); the Division of Plastic and Reconstructive Surgery, University of Western Ontario, London, Ont. (Sachal); the Sections of Pediatric Surgery and Plastic Surgery, Department of Surgery, University of Calgary, Calgary, Alta. (Fraulin); the Departments of Clinical Neurosciences and Surgery, University of Calgary, Calgary, Alta. (Gabriel); the Department of Distributed Learning and Rural Initiatives, Cumming School of Medicine, University of Calgary, Calgary, Alta. (Perez, Johnston)
| | - Ifeoluwa Adedipe
- From the Cumming School of Medicine, University of Calgary, Calgary, Alta. (Ebrahim, Sinha, Adedipe, Ahmad, Amyotte, Yang); the Canadian Global Surgery Trainees' Association affiliated with the International Student Surgical Network - InciSioN (Ebrahim, Sinha, Adedipe, Ahmad, Amyotte, Yang, Elsewify); the Faculty of Medicine and Health Sciences, Laval University, Québec City, Que. (Elsewify); the Division of Plastic and Reconstructive Surgery, University of Western Ontario, London, Ont. (Sachal); the Sections of Pediatric Surgery and Plastic Surgery, Department of Surgery, University of Calgary, Calgary, Alta. (Fraulin); the Departments of Clinical Neurosciences and Surgery, University of Calgary, Calgary, Alta. (Gabriel); the Department of Distributed Learning and Rural Initiatives, Cumming School of Medicine, University of Calgary, Calgary, Alta. (Perez, Johnston)
| | - Abeer Ahmad
- From the Cumming School of Medicine, University of Calgary, Calgary, Alta. (Ebrahim, Sinha, Adedipe, Ahmad, Amyotte, Yang); the Canadian Global Surgery Trainees' Association affiliated with the International Student Surgical Network - InciSioN (Ebrahim, Sinha, Adedipe, Ahmad, Amyotte, Yang, Elsewify); the Faculty of Medicine and Health Sciences, Laval University, Québec City, Que. (Elsewify); the Division of Plastic and Reconstructive Surgery, University of Western Ontario, London, Ont. (Sachal); the Sections of Pediatric Surgery and Plastic Surgery, Department of Surgery, University of Calgary, Calgary, Alta. (Fraulin); the Departments of Clinical Neurosciences and Surgery, University of Calgary, Calgary, Alta. (Gabriel); the Department of Distributed Learning and Rural Initiatives, Cumming School of Medicine, University of Calgary, Calgary, Alta. (Perez, Johnston)
| | - Madison Amyotte
- From the Cumming School of Medicine, University of Calgary, Calgary, Alta. (Ebrahim, Sinha, Adedipe, Ahmad, Amyotte, Yang); the Canadian Global Surgery Trainees' Association affiliated with the International Student Surgical Network - InciSioN (Ebrahim, Sinha, Adedipe, Ahmad, Amyotte, Yang, Elsewify); the Faculty of Medicine and Health Sciences, Laval University, Québec City, Que. (Elsewify); the Division of Plastic and Reconstructive Surgery, University of Western Ontario, London, Ont. (Sachal); the Sections of Pediatric Surgery and Plastic Surgery, Department of Surgery, University of Calgary, Calgary, Alta. (Fraulin); the Departments of Clinical Neurosciences and Surgery, University of Calgary, Calgary, Alta. (Gabriel); the Department of Distributed Learning and Rural Initiatives, Cumming School of Medicine, University of Calgary, Calgary, Alta. (Perez, Johnston)
| | - Lucy Yang
- From the Cumming School of Medicine, University of Calgary, Calgary, Alta. (Ebrahim, Sinha, Adedipe, Ahmad, Amyotte, Yang); the Canadian Global Surgery Trainees' Association affiliated with the International Student Surgical Network - InciSioN (Ebrahim, Sinha, Adedipe, Ahmad, Amyotte, Yang, Elsewify); the Faculty of Medicine and Health Sciences, Laval University, Québec City, Que. (Elsewify); the Division of Plastic and Reconstructive Surgery, University of Western Ontario, London, Ont. (Sachal); the Sections of Pediatric Surgery and Plastic Surgery, Department of Surgery, University of Calgary, Calgary, Alta. (Fraulin); the Departments of Clinical Neurosciences and Surgery, University of Calgary, Calgary, Alta. (Gabriel); the Department of Distributed Learning and Rural Initiatives, Cumming School of Medicine, University of Calgary, Calgary, Alta. (Perez, Johnston)
| | - Omar Elsewify
- From the Cumming School of Medicine, University of Calgary, Calgary, Alta. (Ebrahim, Sinha, Adedipe, Ahmad, Amyotte, Yang); the Canadian Global Surgery Trainees' Association affiliated with the International Student Surgical Network - InciSioN (Ebrahim, Sinha, Adedipe, Ahmad, Amyotte, Yang, Elsewify); the Faculty of Medicine and Health Sciences, Laval University, Québec City, Que. (Elsewify); the Division of Plastic and Reconstructive Surgery, University of Western Ontario, London, Ont. (Sachal); the Sections of Pediatric Surgery and Plastic Surgery, Department of Surgery, University of Calgary, Calgary, Alta. (Fraulin); the Departments of Clinical Neurosciences and Surgery, University of Calgary, Calgary, Alta. (Gabriel); the Department of Distributed Learning and Rural Initiatives, Cumming School of Medicine, University of Calgary, Calgary, Alta. (Perez, Johnston)
| | - Sukhmeet S Sachal
- From the Cumming School of Medicine, University of Calgary, Calgary, Alta. (Ebrahim, Sinha, Adedipe, Ahmad, Amyotte, Yang); the Canadian Global Surgery Trainees' Association affiliated with the International Student Surgical Network - InciSioN (Ebrahim, Sinha, Adedipe, Ahmad, Amyotte, Yang, Elsewify); the Faculty of Medicine and Health Sciences, Laval University, Québec City, Que. (Elsewify); the Division of Plastic and Reconstructive Surgery, University of Western Ontario, London, Ont. (Sachal); the Sections of Pediatric Surgery and Plastic Surgery, Department of Surgery, University of Calgary, Calgary, Alta. (Fraulin); the Departments of Clinical Neurosciences and Surgery, University of Calgary, Calgary, Alta. (Gabriel); the Department of Distributed Learning and Rural Initiatives, Cumming School of Medicine, University of Calgary, Calgary, Alta. (Perez, Johnston)
| | - Frankie O G Fraulin
- From the Cumming School of Medicine, University of Calgary, Calgary, Alta. (Ebrahim, Sinha, Adedipe, Ahmad, Amyotte, Yang); the Canadian Global Surgery Trainees' Association affiliated with the International Student Surgical Network - InciSioN (Ebrahim, Sinha, Adedipe, Ahmad, Amyotte, Yang, Elsewify); the Faculty of Medicine and Health Sciences, Laval University, Québec City, Que. (Elsewify); the Division of Plastic and Reconstructive Surgery, University of Western Ontario, London, Ont. (Sachal); the Sections of Pediatric Surgery and Plastic Surgery, Department of Surgery, University of Calgary, Calgary, Alta. (Fraulin); the Departments of Clinical Neurosciences and Surgery, University of Calgary, Calgary, Alta. (Gabriel); the Department of Distributed Learning and Rural Initiatives, Cumming School of Medicine, University of Calgary, Calgary, Alta. (Perez, Johnston)
| | - Vincent A Gabriel
- From the Cumming School of Medicine, University of Calgary, Calgary, Alta. (Ebrahim, Sinha, Adedipe, Ahmad, Amyotte, Yang); the Canadian Global Surgery Trainees' Association affiliated with the International Student Surgical Network - InciSioN (Ebrahim, Sinha, Adedipe, Ahmad, Amyotte, Yang, Elsewify); the Faculty of Medicine and Health Sciences, Laval University, Québec City, Que. (Elsewify); the Division of Plastic and Reconstructive Surgery, University of Western Ontario, London, Ont. (Sachal); the Sections of Pediatric Surgery and Plastic Surgery, Department of Surgery, University of Calgary, Calgary, Alta. (Fraulin); the Departments of Clinical Neurosciences and Surgery, University of Calgary, Calgary, Alta. (Gabriel); the Department of Distributed Learning and Rural Initiatives, Cumming School of Medicine, University of Calgary, Calgary, Alta. (Perez, Johnston)
| | - Grace Perez
- From the Cumming School of Medicine, University of Calgary, Calgary, Alta. (Ebrahim, Sinha, Adedipe, Ahmad, Amyotte, Yang); the Canadian Global Surgery Trainees' Association affiliated with the International Student Surgical Network - InciSioN (Ebrahim, Sinha, Adedipe, Ahmad, Amyotte, Yang, Elsewify); the Faculty of Medicine and Health Sciences, Laval University, Québec City, Que. (Elsewify); the Division of Plastic and Reconstructive Surgery, University of Western Ontario, London, Ont. (Sachal); the Sections of Pediatric Surgery and Plastic Surgery, Department of Surgery, University of Calgary, Calgary, Alta. (Fraulin); the Departments of Clinical Neurosciences and Surgery, University of Calgary, Calgary, Alta. (Gabriel); the Department of Distributed Learning and Rural Initiatives, Cumming School of Medicine, University of Calgary, Calgary, Alta. (Perez, Johnston)
| | - Aaron Johnston
- From the Cumming School of Medicine, University of Calgary, Calgary, Alta. (Ebrahim, Sinha, Adedipe, Ahmad, Amyotte, Yang); the Canadian Global Surgery Trainees' Association affiliated with the International Student Surgical Network - InciSioN (Ebrahim, Sinha, Adedipe, Ahmad, Amyotte, Yang, Elsewify); the Faculty of Medicine and Health Sciences, Laval University, Québec City, Que. (Elsewify); the Division of Plastic and Reconstructive Surgery, University of Western Ontario, London, Ont. (Sachal); the Sections of Pediatric Surgery and Plastic Surgery, Department of Surgery, University of Calgary, Calgary, Alta. (Fraulin); the Departments of Clinical Neurosciences and Surgery, University of Calgary, Calgary, Alta. (Gabriel); the Department of Distributed Learning and Rural Initiatives, Cumming School of Medicine, University of Calgary, Calgary, Alta. (Perez, Johnston)
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Suraju MO, Kahl AR, Nayyar A, Turaczyk-Kolodziej D, McCracken A, Gordon D, Freischlag K, Borbon L, Nash S, Aziz H. Patterns of care and outcomes for hepatocellular carcinoma and pancreatic cancer based on rurality of patient's residence in a rural midwestern state. J Gastrointest Surg 2024; 28:1994-2000. [PMID: 39293732 DOI: 10.1016/j.gassur.2024.09.013] [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: 06/27/2024] [Revised: 08/20/2024] [Accepted: 09/13/2024] [Indexed: 09/20/2024]
Abstract
BACKGROUND Although advancements in surgical planning and multidisciplinary care have improved the survival of patients with hepatopancreatic cancers in recent years, the impact of the rurality of patient residence on care received and survival is not well known. We aimed to assess the association between the rurality of a patient's residence and cancer-specific survival outcomes among patients with hepatocellular carcinoma (HCC) and pancreatic cancer (PC) in Iowa, hypothesizing that patients in rural areas would experience lower survival. METHODS Adult patients diagnosed with HCC or PC between 2010 and 2020 were identified using the Iowa Cancer Registry. Chi-square tests were used to compare categorical variables by rural/urban status. Logistic regression was used to examine factors associated with receiving surgery. Multivariable-adjusted Cox proportional hazards regression was used to determine associations with cancer-specific mortality. RESULTS Of 1877 patients with HCC, 58%, 27%, and 16% resided in metropolitan, micropolitan, and rural areas, respectively. Approximately 70% of patients in rural areas traveled ≥50 miles for definitive care. Additionally, those residing in rural areas had the highest proportion of patients receiving definitive care at non-Commission on Cancer (CoC) centers (12.6% metro vs 14% micro vs 22.2% rural, P < .001). In a multivariable-adjusted analysis of patients with stage I to III disease, definitive care at a non-CoC center was independently associated with lower odds of surgery (odds ratio [OR] = 0.23; 95% CI, 0.12-0.45; P < .0001) and higher mortality risk (OR = 1.39; 95% CI, 1.07-1.79; P = .01), though rural residence was not. For PC, 5465 patients were diagnosed, and 51%, 28%, and 20% resided in metropolitan, micropolitan, and rural areas, respectively. Similar to HCC, although rural residence was neither associated with odds of surgery nor with mortality risk, receiving definitive care at non-CoC accredited centers was associated with significantly lower odds of receiving surgery (OR = 0.17; 95% CI, 0.11-0.26; P < .0001) and higher mortality risk (OR = 1.48; 95% CI, 1.23-1.77; P < .0001). CONCLUSION Rural residents with hepatopancreatic cancer have the highest proportion of patients receiving definitive care at non-CoC centers, which is associated with lower odds of receiving surgery and higher odds of mortality. This highlights the importance of standardizing complex cancer care and the need to foster collaboration between specialized and non-specialized centers.
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Affiliation(s)
- Mohammed O Suraju
- Department of Surgery, University of Iowa Hospitals and Clinics, Iowa City, IA, United States
| | - Amanda R Kahl
- Iowa Cancer Registry, Iowa City, IA, United States; Department of Epidemiology, University of Iowa, Iowa City, IA, United States
| | - Apoorve Nayyar
- Department of Surgery, University of Iowa Hospitals and Clinics, Iowa City, IA, United States
| | | | - Ana McCracken
- Department of Surgery, University of Iowa Hospitals and Clinics, Iowa City, IA, United States
| | - Darren Gordon
- Department of Surgery, University of Iowa Hospitals and Clinics, Iowa City, IA, United States
| | - Kyle Freischlag
- Department of Surgery, University of Iowa Hospitals and Clinics, Iowa City, IA, United States
| | - Luis Borbon
- Department of Surgery, University of Iowa Hospitals and Clinics, Iowa City, IA, United States
| | - Sarah Nash
- Iowa Cancer Registry, Iowa City, IA, United States; Department of Epidemiology, University of Iowa, Iowa City, IA, United States
| | - Hassan Aziz
- Department of Surgery, University of Iowa Hospitals and Clinics, Iowa City, IA, United States.
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Radu IP. Is mailed outreach and patient navigation a perfect solution to improve HCC screening? Gut 2024; 73:1929-1930. [PMID: 39179371 DOI: 10.1136/gutjnl-2024-332920] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Key Words] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 07/01/2024] [Accepted: 07/31/2024] [Indexed: 08/26/2024]
Affiliation(s)
- Iuliana Pompilia Radu
- Department of Visceral Surgery and Medicine, Inselspital, Bern University Hospital, University of Bern, Bern, Switzerland
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Ozturk NB, Pham HN, Mouhaffel R, Ibrahim R, Alsaqa M, Gurakar A, Saberi B. A Longitudinal Analysis of Mortality Related to Chronic Viral Hepatitis and Hepatocellular Carcinoma in the United States. Viruses 2024; 16:694. [PMID: 38793576 PMCID: PMC11125803 DOI: 10.3390/v16050694] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 03/19/2024] [Revised: 04/25/2024] [Accepted: 04/27/2024] [Indexed: 05/26/2024] Open
Abstract
(1) Background: Hepatocellular carcinoma (HCC) contributes to the significant burden of cancer mortality in the United States (US). Despite highly efficacious antivirals, chronic viral hepatitis (CVH) remains an important cause of HCC. With advancements in therapeutic modalities, along with the aging of the population, we aimed to assess the contribution of CVH in HCC-related mortality in the US between 1999-2020. (2) Methods: We queried all deaths related to CVH and HCC in the multiple-causes-of-death files from the CDC Wide-ranging Online Data for Epidemiologic Research (WONDER) database between 1999-2020. Using the direct method of standardization, we adjusted all mortality information for age and compared the age-adjusted mortality rates (AAMRs) across demographic populations and by percentile rankings of social vulnerability. Temporal shifts in mortality were quantified using log-linear regression models. (3) Results: A total of 35,030 deaths were identified between 1999-2020. The overall crude mortality increased from 0.27 in 1999 to 8.32 in 2016, followed by a slight reduction to 7.04 in 2020. The cumulative AAMR during the study period was 4.43 (95% CI, 4.39-4.48). Males (AAMR 7.70) had higher mortality rates compared to females (AAMR 1.44). Mortality was higher among Hispanic populations (AAMR 6.72) compared to non-Hispanic populations (AAMR 4.18). Higher mortality was observed in US counties categorized as the most socially vulnerable (AAMR 5.20) compared to counties that are the least socially vulnerable (AAMR 2.53), with social vulnerability accounting for 2.67 excess deaths per 1,000,000 person-years. (4) Conclusions: Our epidemiological analysis revealed an overall increase in CVH-related HCC mortality between 1999-2008, followed by a stagnation period until 2020. CVH-related HCC mortality disproportionately affected males, Hispanic populations, and Black/African American populations, Western US regions, and socially vulnerable counties. These insights can help aid in the development of strategies to target vulnerable patients, focus on preventive efforts, and allocate resources to decrease HCC-related mortality.
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Affiliation(s)
- N Begum Ozturk
- Department of Medicine, Beaumont Hospital, Royal Oak, MI 48073, USA
| | - Hoang Nhat Pham
- Department of Medicine, University of Arizona Tucson, Tucson, AZ 85721, USA
| | - Rama Mouhaffel
- Department of Medicine, University of Arizona Tucson, Tucson, AZ 85721, USA
| | - Ramzi Ibrahim
- Department of Medicine, University of Arizona Tucson, Tucson, AZ 85721, USA
| | - Marwan Alsaqa
- Division of Gastroenterology and Hepatology, Beth Israel Deaconess Medical Center, Harvard Medical School, Boston, MA 02130, USA
| | - Ahmet Gurakar
- Division of Gastroenterology and Hepatology, Johns Hopkins University School of Medicine, 720 Rutland Avenue, Ross Research Building, Suite 918, Baltimore, MD 21205, USA
| | - Behnam Saberi
- Division of Gastroenterology and Hepatology, Beth Israel Deaconess Medical Center, Harvard Medical School, Boston, MA 02130, USA
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7
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Arnett A, Siegel DA, Dai S, Thompson TD, Foster J, di Pierro EJ, Momin B, Lupo PJ, Heczey A. Incidence and survival of pediatric and adult hepatocellular carcinoma, United States, 2001-2020. MEDRXIV : THE PREPRINT SERVER FOR HEALTH SCIENCES 2024:2024.03.25.24304564. [PMID: 38633779 PMCID: PMC11023662 DOI: 10.1101/2024.03.25.24304564] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Grants] [Track Full Text] [Subscribe] [Scholar Register] [Indexed: 04/19/2024]
Abstract
Importance Hepatocellular carcinoma accounts for approximately 80% of liver neoplasms. Globally, hepatocellular carcinoma ranks as the third most lethal cancer, with the number of deaths expected to further increase by 2040. In adults, disparities in incidence and survival are well described while pediatric epidemiology is not well characterized. Objective To describe incidence and survival for pediatric (ages 0-19 years) hepatocellular carcinoma cases and compare these measures to adults (ages ≥20 years) diagnosed with hepatocellular carcinoma. We evaluated demographic factors and clinical characteristics that influence incidence and outcomes. Design Population-based cohort study. Setting Incidence data from the US Cancer Statistics database from 2003 to 2020 and 5-year relative survival from the National Program of Cancer Registries from 2001 to 2019, covering 97% and 83% of the US population, respectively. Participants 355,349 US Cancer Statistics and 257,406 the National Program of Cancer Registries patients were identified using ICD-O-3 C22.0 and 8170-5 codes. Main Outcomes and Measures Incidence annual percent change (APC) and average APC (AAPC) using joinpoint regression. Five-year relative survival. All-cause survival estimated using multivariate Cox modeling. Corresponding 95% confidence intervals (CI) were calculated. Results Incidence rate per 100,000 persons was 0.056 (95%CI:0.052-0.060) for pediatric cases and 7.793 (7.767-7.819) for adults. Incidence was stable in the pediatric population (0.3 AAPC, -1.1-1.7). In contrast, after periods of increase, incidence declined in adults after 2015 (-1.5 APC). Relative survival increased over time for both pediatric and adult ages and was higher for children and adolescents (46.4%, 95%CI:42.4-50.3) than adults (20.7%, 95%CI:20.5-20.9) overall and when stratified by stage. Regression modeling showed that non-Hispanic Black race and ethnicity was associated with higher risk of death in children and adolescents (1.48, 95%CI:1.07-2.05) and adults (1.11, 95%CI:1.09-1.12) compared to non-Hispanic white race and ethnicity. Conclusions and Relevance Between 2003 and 2020 in the United States, pediatric incidence was stable while incidence in adults began to decline after 2015. Survival was higher across all stages for children and adolescents compared to adults. Non-Hispanic Black race and ethnicity showed a higher risk of death for both age groups. Further studies could explore the factors that influence these outcome disparities.
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Affiliation(s)
- Azlann Arnett
- Cancer and Hematology Centers, Texas Children’s Hospital, Houston, Texas
- Division of Hematology-Oncology, Department of Pediatrics, Baylor College of Medicine, Houston, Texas
| | - David A. Siegel
- Division of Cancer Prevention and Control, National Center for Chronic Disease Prevention and Health Promotion, Centers for Disease Control and Prevention, Atlanta, Georgia
| | - Shifan Dai
- Cyberdata Technologies, Inc., Herndon, Virginia
| | - Trevor D. Thompson
- Division of Cancer Prevention and Control, National Center for Chronic Disease Prevention and Health Promotion, Centers for Disease Control and Prevention, Atlanta, Georgia
| | - Jennifer Foster
- Cancer and Hematology Centers, Texas Children’s Hospital, Houston, Texas
- Division of Hematology-Oncology, Department of Pediatrics, Baylor College of Medicine, Houston, Texas
| | - Erika J. di Pierro
- Cancer and Hematology Centers, Texas Children’s Hospital, Houston, Texas
- Division of Hematology-Oncology, Department of Pediatrics, Baylor College of Medicine, Houston, Texas
| | - Behnoosh Momin
- Division of Cancer Prevention and Control, National Center for Chronic Disease Prevention and Health Promotion, Centers for Disease Control and Prevention, Atlanta, Georgia
| | - Philip J. Lupo
- Cancer and Hematology Centers, Texas Children’s Hospital, Houston, Texas
- Cnter for Epidemiology and Population Health, Department of Pediatrics, Baylor College of Medicine, Houston, Texas
- Division of Hematology-Oncology, Department of Pediatrics, Baylor College of Medicine, Houston, Texas
| | - Andras Heczey
- Cancer and Hematology Centers, Texas Children’s Hospital, Houston, Texas
- Division of Hematology-Oncology, Department of Pediatrics, Baylor College of Medicine, Houston, Texas
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8
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El-Serag HB, Ward JW, Asrani SK, Singal AG, Rich N, Thrift AP, Deshpande S, Turner BJ, Kaseb AO, Harrison AC, Fortune BE, Kanwal F. Prevention of Hepatocellular Carcinoma (HCC). White Paper of the Texas Collaborative Center for Hepatocellular Cancer (TeCH) Multi-stakeholder Conference. Clin Gastroenterol Hepatol 2023; 21:2183-2192. [PMID: 37086825 PMCID: PMC10524305 DOI: 10.1016/j.cgh.2023.03.029] [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: 02/02/2023] [Revised: 03/17/2023] [Accepted: 03/17/2023] [Indexed: 04/24/2023]
Abstract
BACKGROUND & AIMS Texas has the highest age-adjusted incidence rate of hepatocellular carcinoma (HCC) in the United States. The Cancer Prevention and Research Institute of Texas has funded the Texas Collaborative Center for Hepatocellular Cancer (TeCH) to facilitate HCC research, education, and advocacy activities with the overall goal of reducing HCC mortality in Texas through coordination, collaboration, and advocacy. METHODS On September 17, 2022, TeCH co-sponsored a multi-stakeholder conference on HCC with the Baker Institute Center for Health and Biosciences. This conference was attended by HCC researchers, policy makers, payers, members from pharmaceutical industry and patient advocacy groups in and outside of Texas. This report summarizes the results of the conference. RESULTS The goal of this meeting was to identify different strategies for preventing HCC and evaluate their readiness for implementation. CONCLUSIONS We call for a statewide (1) viral hepatitis elimination program; (2) program to increase nonalcoholic steatohepatitis and obesity awareness; (3) research program to develop health care models that integrate alcohol associated liver disease treatment and treatment for alcohol use disorder; and (4) demonstration projects to evaluate the effectiveness of identifying and linking patient with advanced fibrosis and cirrhosis to clinical care.
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Affiliation(s)
| | - John W Ward
- The Coalition for Global Hepatitis Elimination, The Task Force for Global Health, Decatur, Georgia
| | | | - Amit G Singal
- Department of Medicine, University of Texas Southwestern Medical Center Dallas, Texas
| | - Nicole Rich
- Department of Medicine, University of Texas Southwestern Medical Center Dallas, Texas
| | - Aaron P Thrift
- Section of Epidemiology and Population Sciences, Department of Medicine, Baylor College of Medicine, Houston, Texas; Dan L. Duncan Comprehensive Cancer Center, Baylor College of Medicine, Houston, Texas
| | | | - Barbara J Turner
- Department of Medicine, Keck School of Medicine of USC, Los Angeles, California
| | - Ahmed O Kaseb
- Department of Gastrointestinal Medical Oncology, Division of Cancer Medicine, The University of Texas MD Anderson Cancer Center, Houston, Texas
| | - Ariel C Harrison
- Department of Medicine, Baylor College of Medicine, Houston, Texas
| | - Brett E Fortune
- Department of Medicine, Montefiore Medical Center, Bronx, New York
| | - Fasiha Kanwal
- Department of Medicine, Baylor College of Medicine, Houston, Texas
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9
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Zhou K, Song Z, Rostomian N, Dodge JL, Stern MC, Setiawan VW, Terrault NA, Cockburn MG, Liu L. Association of nativity with survival among adults with hepatocellular carcinoma. J Natl Cancer Inst 2023; 115:861-869. [PMID: 37160726 PMCID: PMC10323898 DOI: 10.1093/jnci/djad067] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/20/2022] [Revised: 02/13/2023] [Accepted: 04/13/2023] [Indexed: 05/11/2023] Open
Abstract
INTRODUCTION Immigrants comprise a considerable proportion of those diagnosed with hepatocellular carcinoma (HCC) in the United States. Nativity or birthplace affects incidence and risk factors for HCC, but little is known about its influence on survival after diagnosis. METHODS We identified 51 533 adults with HCC with available birthplace in the California Cancer Registry between 1988 and 2017. HCC cases were categorized as foreign born or US born and stratified by mutually exclusive race and ethnicity groups. Primary outcome was all-cause mortality. Race and ethnicity-specific Cox regression propensity score-weighted models evaluated the relationship between nativity and death as well as region of birth among foreign-born patients. RESULTS A total of 40% of all HCC cases were foreign born, and 92.2%, 45.2%, 9.1%, and 5.8% of Asian/Pacific Islander (API), Hispanic, White, and Black patients were foreign born, respectively. Five-year survival rates were higher in foreign-born patients compared with US-born patients: 12.9% vs 9.6% for White patients, 11.7% vs 9.8% for Hispanic patients, 12.8% vs 8.1% for Black patients, and 16.4% vs 12.4% for API patients. Nativity was associated with survival, with better survival in foreign-born patients: White patients: hazard ratio (HR) = 0.86 (95% confidence interval [CI] = 0.81 to 0.90), Hispanic patients: HR = 0.90 (95% CI = 0.86 to 0.93), Black patients: HR = 0.89 (95% CI = 0.76 to 1.05), and API patients: HR = 0.94 (95% CI = 0.88 to 1.00). Among foreign-born patients, lower mortality was observed in those from Central and South America compared with Mexico for Hispanic patients, East Asia compared with Southeast Asia for API patients, and East Europe and Greater Middle East compared with West/South/North Europe for White patients. CONCLUSION Foreign-born patients with HCC have better survival than US-born patients. Further investigation into the mechanisms of this survival disparity by nativity is needed.
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Affiliation(s)
- Kali Zhou
- Department of Medicine, Keck School of Medicine, University of Southern California, Los Angeles, CA, USA
- Research Center for Liver Diseases, Keck School of Medicine, University of Southern California, Los Angeles, CA, USA
| | - Ziwei Song
- Department of Population and Public Health Sciences, Keck School of Medicine, University of Southern California, Los Angeles, CA, USA
| | | | - Jennifer L Dodge
- Department of Medicine, Keck School of Medicine, University of Southern California, Los Angeles, CA, USA
- Research Center for Liver Diseases, Keck School of Medicine, University of Southern California, Los Angeles, CA, USA
- Department of Population and Public Health Sciences, Keck School of Medicine, University of Southern California, Los Angeles, CA, USA
| | - Mariana C Stern
- Department of Population and Public Health Sciences, Keck School of Medicine, University of Southern California, Los Angeles, CA, USA
- Norris Comprehensive Cancer Center, Keck School of Medicine, University of Southern California, Los Angeles, CA, USA
| | - V Wendy Setiawan
- Department of Population and Public Health Sciences, Keck School of Medicine, University of Southern California, Los Angeles, CA, USA
- Norris Comprehensive Cancer Center, Keck School of Medicine, University of Southern California, Los Angeles, CA, USA
| | - Norah A Terrault
- Department of Medicine, Keck School of Medicine, University of Southern California, Los Angeles, CA, USA
- Research Center for Liver Diseases, Keck School of Medicine, University of Southern California, Los Angeles, CA, USA
| | - Myles G Cockburn
- Department of Population and Public Health Sciences, Keck School of Medicine, University of Southern California, Los Angeles, CA, USA
- Norris Comprehensive Cancer Center, Keck School of Medicine, University of Southern California, Los Angeles, CA, USA
| | - Lihua Liu
- Department of Population and Public Health Sciences, Keck School of Medicine, University of Southern California, Los Angeles, CA, USA
- Norris Comprehensive Cancer Center, Keck School of Medicine, University of Southern California, Los Angeles, CA, USA
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10
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Jones PD, Lai JC, Bajaj JS, Kanwal F. Actionable Solutions to Achieve Health Equity in Chronic Liver Disease. Clin Gastroenterol Hepatol 2023; 21:1992-2000. [PMID: 37061105 PMCID: PMC10330625 DOI: 10.1016/j.cgh.2023.03.043] [Citation(s) in RCA: 20] [Impact Index Per Article: 10.0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 10/28/2022] [Revised: 02/08/2023] [Accepted: 03/26/2023] [Indexed: 04/17/2023]
Abstract
There are well-described racial and ethnic disparities in the burden of chronic liver diseases. Hispanic persons are at highest risk for developing nonalcoholic fatty liver disease, the fastest growing cause of liver disease. Hepatitis B disproportionately affects persons of Asian or African descent. The highest rates of hepatitis C occur in American Indian and Alaskan Native populations. In addition to disparities in disease burden, there are also marked racial and ethnic disparities in access to treatments, including liver transplantation. Disparities also exist by gender and geography, especially in alcohol-related liver disease. To achieve health equity, we must address the root causes that drive these inequities. Understanding the role that social determinants of health play in the disparate health outcomes that are currently observed is critically important. We must forge and/or strengthen collaborations between patients, community members, other key stakeholders, health care providers, health care institutions, professional societies, and legislative bodies. Herein, we provide a high-level review of current disparities in chronic liver disease and describe actionable strategies that have potential to bridge gaps, improve quality, and promote equity in liver care.
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Affiliation(s)
- Patricia D Jones
- Division of Digestive Health and Liver Diseases, Department of Medicine, University of Miami Miller School of Medicine, Miami, Florida; Sylvester Comprehensive Cancer Center, University of Miami Miller School of Medicine, Miami, Florida.
| | - Jennifer C Lai
- Division of Gastroenterology and Hepatology, Department of Medicine, University of California-San Francisco, San Francisco, California
| | - Jasmohan S Bajaj
- Virginia Commonwealth University and Central Virginia Veterans Health Care System, Richmond, Virginia
| | - Fasiha Kanwal
- Section of Gastroenterology and Hepatology, Department of Medicine, Baylor College of Medicine, Houston, Texas; Section of Health Services Research, Department of Medicine, Baylor College of Medicine, Houston, Texas; VA HSR&D Center for Innovations in Quality, Effectiveness, and Safety (IQuESt), Michael E. DeBakey VA Medical Center, Houston, Texas
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11
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Kim NJ, Cravero A, VoPham T, Vutien P, Carr R, Issaka RB, Johnston J, McMahon B, Mera J, Ioannou GN. Addressing racial and ethnic disparities in US liver cancer care. Hepatol Commun 2023; 7:e00190. [PMID: 37347221 PMCID: PMC10289716 DOI: 10.1097/hc9.0000000000000190] [Citation(s) in RCA: 11] [Impact Index Per Article: 5.5] [Reference Citation Analysis] [Abstract] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 10/31/2022] [Accepted: 05/09/2023] [Indexed: 06/23/2023] Open
Abstract
HCC, the most common form of primary liver cancer, is the fastest rising cause of cancer-related death in the United States. HCC disproportionately affects racial and ethnic minorities in the United States. A practical framework is needed to organize the complex patient, provider, health system, and societal factors that drive these racial and ethnic disparities. In this narrative review, we adapted and applied the National Institute on Minority Health and Health Disparities (NIMHD) Research Framework to the HCC care continuum, as a step toward better understanding and addressing existing HCC-related disparities. We first summarize the literature on HCC-related disparities by race and ethnicity organized by the framework's 5 domains (biological, behavioral, physical/built environment, sociocultural environment, and health care system) and 4 levels (individual, interpersonal, community, and societal) of influence. We then offer strategies to guide future research initiatives toward promotion of health equity in HCC care. Clinicians and researchers may help mitigate further inequities and better address racial and ethnic disparities in HCC care by prioritizing the following in HCC research: (1) increasing racial and ethnic minority representation, (2) collecting and reporting HCC-related data by racial and ethnic subgroups, (3) assessing the patient experience of HCC care by race and ethnicity, and (4) evaluating HCC-specific social determinants of health by race and ethnicity. These 4 priorities will help inform the development of future programs and interventions that are tailored to the unique experiences of each racial and ethnic group.
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Affiliation(s)
- Nicole J. Kim
- Division of Gastroenterology, Department of Medicine, University of Washington, Seattle, Washington, USA
| | - Anne Cravero
- Department of Medicine, University of Washington, Seattle, Washington, USA
| | - Trang VoPham
- Epidemiology Program, Public Health Sciences Division, Fred Hutchinson Cancer Center, Seattle, Washington, USA
- Department of Epidemiology, University of Washington School of Public Health, Seattle, Washington, USA
| | - Philip Vutien
- Division of Gastroenterology, Department of Medicine, University of Washington, Seattle, Washington, USA
| | - Rotonya Carr
- Division of Gastroenterology, Department of Medicine, University of Washington, Seattle, Washington, USA
| | - Rachel B. Issaka
- Division of Gastroenterology, Department of Medicine, University of Washington, Seattle, Washington, USA
- Clinical Research Division, Fred Hutchinson Cancer Center, Seattle, Washington, USA
| | - Janet Johnston
- Liver Disease and Hepatitis Program, Alaska Native Tribal Health Consortium, Anchorage, Alaska
| | - Brian McMahon
- Liver Disease and Hepatitis Program, Alaska Native Tribal Health Consortium, Anchorage, Alaska
| | - Jorge Mera
- Cherokee Nation Health Services, Tahlequah, Oklahoma
| | - George N. Ioannou
- Division of Gastroenterology, Department of Medicine, University of Washington, Seattle, Washington, USA
- Division of Gastroenterology, Department of Medicine, Veterans Affairs Puget Sound Health Care System, Seattle, Washington, USA
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12
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Da BL, Suchman KI, Lau L, Rabiee A, He AR, Shetty K, Yu H, Wong LL, Amdur RL, Crawford JM, Fox SS, Grimaldi GM, Shah PK, Weinstein J, Bernstein D, Satapathy SK, Chambwe N, Xiang X, Mishra L. Pathogenesis to management of hepatocellular carcinoma. Genes Cancer 2022; 13:72-87. [PMID: 36533190 PMCID: PMC9746873 DOI: 10.18632/genesandcancer.226] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 09/07/2022] [Accepted: 11/17/2022] [Indexed: 12/15/2022] Open
Abstract
Hepatocellular carcinoma (HCC) is the most common primary liver cancer whose incidence continues to rise in many parts of the world due to a concomitant rise in many associated risk factors, such as alcohol use and obesity. Although early-stage HCC can be potentially curable through liver resection, liver-directed therapies, or transplantation, patients usually present with intermediate to advanced disease, which continues to be associated with a poor prognosis. This is because HCC is a cancer with significant complexities, including substantial clinical, histopathologic, and genomic heterogeneity. However, the scientific community has made a major effort to better characterize HCC in those aspects via utilizing tissue sampling and histological classification, whole genome sequencing, and developing viable animal models. These efforts ultimately aim to develop clinically relevant biomarkers and discover molecular targets for new therapies. For example, until recently, there was only one approved systemic therapy for advanced or metastatic HCC in the form of sorafenib. Through these efforts, several additional targeted therapies have gained approval in the United States, although much progress remains to be desired. This review will focus on the link between characterizing the pathogenesis of HCC with current and future HCC management.
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Affiliation(s)
- Ben L. Da
- Department of Internal Medicine, Division of Hepatology, Sandra Atlas Bass Center for Liver Diseases and Transplantation, Donald and Barbara Zucker School of Medicine at Hofstra/Northwell Health, Manhasset, NY 11030, USA
| | - Kelly I. Suchman
- Department of Internal Medicine, Donald and Barbara Zucker School of Medicine at Hofstra/Northwell Health, Manhasset, NY 11030, USA
| | - Lawrence Lau
- Department of Surgery, North Shore University Hospital, Northwell Health, Manhasset, NY 11030, USA
| | - Atoosa Rabiee
- Department of Gastroenterology and Hepatology, VA Medical Center, Washington, DC 20422, USA
| | - Aiwu Ruth He
- Lombardi Comprehensive Cancer Center, Georgetown University Medical Center, Washington, DC 20007, USA
| | - Kirti Shetty
- Division of Gastroenterology and Hepatology, University of Maryland, Baltimore, MD 21201, USA
| | - Herbert Yu
- Department of Epidemiology, University of Hawaii Cancer Center, Honolulu, HI 96813-5516, USA
| | - Linda L. Wong
- Department of Surgery, University of Hawaii, Honolulu, HI 96813-5516, USA
| | - Richard L. Amdur
- Quantitative Intelligence, The Institutes for Health Systems Science and Bioelectronic Medicine, The Feinstein Institutes for Medical Research, Northwell Health, Manhasset, NY 10022, USA
| | - James M. Crawford
- Department of Pathology and Laboratory Medicine, Donald and Barbara Zucker School of Medicine at Hofstra/Northwell, Hempstead, NY 11549, USA
| | - Sharon S. Fox
- Department of Pathology and Laboratory Medicine, Donald and Barbara Zucker School of Medicine at Hofstra/Northwell, Hempstead, NY 11549, USA
| | - Gregory M. Grimaldi
- Department of Radiology, Northwell Health, Donald and Barbara Zucker School of Medicine at Hofstra/Northwell, Manhasset, NY 11030, USA
| | - Priya K. Shah
- Department of Radiology, Northwell Health, Donald and Barbara Zucker School of Medicine at Hofstra/Northwell, Manhasset, NY 11030, USA
| | - Jonathan Weinstein
- Division of Vascular and Interventional Radiology, Department of Radiology, Northwell Health, Donald and Barbara Zucker School of Medicine at Hofstra/Northwell, Manhasset, NY 11030, USA
| | - David Bernstein
- Department of Internal Medicine, Division of Hepatology, Sandra Atlas Bass Center for Liver Diseases and Transplantation, Donald and Barbara Zucker School of Medicine at Hofstra/Northwell Health, Manhasset, NY 11030, USA
| | - Sanjaya K. Satapathy
- Department of Internal Medicine, Division of Hepatology, Sandra Atlas Bass Center for Liver Diseases and Transplantation, Donald and Barbara Zucker School of Medicine at Hofstra/Northwell Health, Manhasset, NY 11030, USA
| | - Nyasha Chambwe
- The Institute of Molecular Medicine, The Feinstein Institutes for Medical Research, Northwell Health, Manhasset, NY 11030, USA
| | - Xiyan Xiang
- The Institute for Bioelectronic Medicine, The Feinstein Institutes for Medical Research and Cold Spring Harbor Laboratory, Department of Medicine, Division of Gastroenterology and Hepatology, Northwell Health, Manhasset, NY 11030, USA
| | - Lopa Mishra
- The Institute for Bioelectronic Medicine, The Feinstein Institutes for Medical Research and Cold Spring Harbor Laboratory, Department of Medicine, Division of Gastroenterology and Hepatology, Northwell Health, Manhasset, NY 11030, USA
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13
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Sempokuya T, Warner J, Azawi M, Nogimura A, Wong LL. Current status of disparity in liver disease. World J Hepatol 2022; 14:1940-1952. [PMID: 36483604 PMCID: PMC9724102 DOI: 10.4254/wjh.v14.i11.1940] [Citation(s) in RCA: 3] [Impact Index Per Article: 1.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 09/18/2022] [Revised: 11/09/2022] [Accepted: 11/16/2022] [Indexed: 11/24/2022] Open
Abstract
Disparities have emerged as an important issue in many aspects of healthcare in developed countries and may be based on race, ethnicity, sex, geographical location, and socioeconomic status. For liver disease specifically, these potential disparities can affect access to care and outcome in viral hepatitis, chronic liver disease, and hepatocellular carcinoma. Shortages in hepatologists and medical providers versed in liver disease may amplify these disparities by compromising early detection of liver disease, surveillance for hepatocellular carcinoma, and prompt referral to subspecialists and transplant centers. In the United States, continued efforts have been made to address some of these disparities with better education of healthcare providers, use of telehealth to enhance access to specialists, reminders in electronic medical records, and modifying organ allocation systems for liver transplantation. This review will detail the current status of disparities in liver disease and describe current efforts to minimize these disparities.
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Affiliation(s)
- Tomoki Sempokuya
- Division of Gastroenterology and Hepatology, Department of Internal Medicine, University of Nebraska Medical Center, Omaha, NE 68198, United States
| | - Josh Warner
- Department of Internal Medicine, University of Nebraska Medical Center, Omaha, NE 68198, United States
| | - Muaataz Azawi
- Division of Gastroenterology and Hepatology, Sanford Center for Digestive Health, Sioux Falls 57105, SD, Uruguay
| | - Akane Nogimura
- Department of Public Health, Nagoya City University Graduate School of Medical Sciences, Nagoya 467-8601, Aichi, Japan
- Division of Psychiatry and Cognitive-Behavioral Medicine, Nagoya City University Graduate School of Medical Sciences, Nagoya 467-8601, Aichi, Japan
| | - Linda L Wong
- Department of Surgery, John A. Burns School of Medicine, University of Hawaii at Manoa, Honolulu, HI 96813, United States
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14
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Bhatia S, Landier W, Paskett ED, Peters KB, Merrill JK, Phillips J, Osarogiagbon RU. Rural-Urban Disparities in Cancer Outcomes: Opportunities for Future Research. J Natl Cancer Inst 2022; 114:940-952. [PMID: 35148389 PMCID: PMC9275775 DOI: 10.1093/jnci/djac030] [Citation(s) in RCA: 114] [Impact Index Per Article: 38.0] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/10/2021] [Revised: 07/27/2021] [Accepted: 02/01/2022] [Indexed: 01/12/2023] Open
Abstract
Cancer care disparities among rural populations are increasingly documented and may be worsening, likely because of the impact of rurality on access to state-of-the-art cancer prevention, diagnosis, and treatment services, as well as higher rates of risk factors such as smoking and obesity. In 2018, the American Society of Clinical Oncology undertook an initiative to understand and address factors contributing to rural cancer care disparities. A key pillar of this initiative was to identify knowledge gaps and promote the research needed to understand the magnitude of difference in outcomes in rural vs nonrural settings, the drivers of those differences, and interventions to address them. The purpose of this review is to describe continued knowledge gaps and areas of priority research to address them. We conducted a comprehensive literature review by searching the PubMed (Medline), Embase, Web of Science, and Cochrane Library databases for studies published in English between 1971 and 2021 and restricted to primary reports from populations in the United States and abstracted data to synthesize current evidence and identify continued gaps in knowledge. Our review identified continuing gaps in the literature regarding the underlying causes of rural-urban disparities in cancer outcomes. Rapid advances in cancer care will worsen existing disparities in outcomes for rural patients without directed effort to understand and address barriers to high-quality care in these areas. Research should be prioritized to address ongoing knowledge gaps about the drivers of rurality-based disparities and preventative and corrective interventions.
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Affiliation(s)
- Smita Bhatia
- University of Alabama at Birmingham School of Medicine, Birmingham, AL, USA
| | - Wendy Landier
- University of Alabama at Birmingham School of Medicine, Birmingham, AL, USA
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15
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Asrani SK, Ghabril MS, Kuo A, Merriman RB, Morgan T, Parikh ND, Ovchinsky N, Kanwal F, Volk ML, Ho C, Serper M, Mehta S, Agopian V, Cabrera R, Chernyak V, El-Serag HB, Heimbach J, Ioannou GN, Kaplan D, Marrero J, Mehta N, Singal A, Salem R, Taddei T, Walling AM, Tapper EB. Quality measures in HCC care by the Practice Metrics Committee of the American Association for the Study of Liver Diseases. Hepatology 2022; 75:1289-1299. [PMID: 34778999 DOI: 10.1002/hep.32240] [Citation(s) in RCA: 34] [Impact Index Per Article: 11.3] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 09/29/2021] [Accepted: 09/29/2021] [Indexed: 12/14/2022]
Abstract
The burden of HCC is substantial. To address gaps in HCC care, the American Association for the Study of Liver Diseases (AASLD) Practice Metrics Committee (PMC) aimed to develop a standard set of process-based measures and patient-reported outcomes (PROs) along the HCC care continuum. We identified candidate process and outcomes measures for HCC care based on structured literature review. A 13-member panel with content expertise across the HCC care continuum evaluated candidate measures on importance and performance gap using a modified Delphi approach (two rounds of rating) to define the final set of measures. Candidate PROs based on a structured scoping review were ranked by 74 patients with HCC across 7 diverse institutions. Out of 135 measures, 29 measures made the final set. These covered surveillance (6 measures), diagnosis (6 measures), staging (2 measures), treatment (10 measures), and outcomes (5 measures). Examples included the use of ultrasound (± alpha-fetoprotein [AFP]) every 6 months, need for surveillance in high-risk populations, diagnostic testing for patients with a new AFP elevation, multidisciplinary liver tumor board (MLTB) review of Liver Imaging-Reporting and Data System 4 lesions, standard evaluation at diagnosis, treatment recommendations based on Barcelona Clinic Liver Cancer staging, MLTB discussion of treatment options, appropriate referral for evaluation of liver transplantation candidacy, and role of palliative therapy. PROs include those related to pain, anxiety, fear of treatment, and uncertainty about the best individual treatment and the future. The AASLD PMC has developed a set of explicit quality measures in HCC care to help bridge the gap between guideline recommendations and measurable processes and outcomes. Measurement and subsequent implementation of these metrics could be a central step in the improvement of patient care and outcomes in this high-risk population.
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Affiliation(s)
| | - Marwan S Ghabril
- 12250Division of GastroenterologyDepartment of MedicineIndiana University School of MedicineIndianapolisIndianaUSA
| | - Alexander Kuo
- Division of GastroenterologyCedars-Sinai Medical CenterUniversity of California Los AngelesLos AngelesCaliforniaUSA
| | - Raphael B Merriman
- Division of General and Transplant HepatologyCalifornia Pacific Medical Center and Research InstituteSan FranciscoCaliforniaUSA
| | - Timothy Morgan
- Medicine and Research ServicesVA Long Beach Healthcare SystemLong BeachCaliforniaUSA
| | - Neehar D Parikh
- Division of Gastroenterology and HepatologyUniversity of MichiganAnn ArborMichiganUSA
| | - Nadia Ovchinsky
- Division of Pediatric GastroenterologyChildren's Hospital at MontefioreBronxNew YorkUSA
| | - Fasiha Kanwal
- Section of Gastroenterology and HepatologyDepartment of MedicineBaylor College of MedicineHoustonTexasUSA
- Center for Innovations in Quality, Effectiveness and SafetyMichael E. DeBakey Veterans Affairs Medical CenterHoustonTexasUSA
- Section of Health Services ResearchDepartment of MedicineBaylor College of MedicineHoustonTexasUSA
| | - Michael L Volk
- 4608Division of Gastroenterology and Transplantation InstituteLoma Linda UniversityLoma LindaCaliforniaUSA
| | - Chanda Ho
- Department of TransplantationCalifornia Pacific Medical CenterSan FranciscoCaliforniaUSA
| | - Marina Serper
- Division of Gastroenterology and HepatologyUniversity of Pennsylvania Perelman School of MedicinePhiladelphiaPennsylvaniaUSA
- Leonard Davis Institute of Health EconomicsPhiladelphiaPennsylvaniaUSA
| | | | - Vatche Agopian
- Division of Liver and Pancreas TransplantationDepartment of SurgeryDavid Geffen School of Medicine at University of CaliforniaLos AngelesCaliforniaUSA
| | - Roniel Cabrera
- Department of MedicineDivision of Gastroenterology, Hepatology and NutritionUniversity of FloridaGainesvilleFloridaUSA
| | | | | | - Julie Heimbach
- Division of Transplant SurgeryWilliam J. von Liebig Transplant CenterMayo ClinicRochesterMinnesotaUSA
| | - George N Ioannou
- Division of GastroenterologyDepartment of MedicineVeterans Affairs Puget Sound Health Care System and University of WashingtonSeattleWashingtonUSA
| | - David Kaplan
- Division of Gastroenterology and HepatologyPerelman University of Pennsylvania School of MedicinePhiladelphiaPennsylvaniaUSA
| | - Jorge Marrero
- Digestive and Liver Diseases DivisionDepartment of Internal MedicineUT Southwestern Medical CenterDallasTexasUSA
| | - Neil Mehta
- Division of GastroenterologyUniversity of California San FranciscoSan FranciscoCaliforniaUSA
| | - Amit Singal
- Division of Digestive and Liver DiseasesUT Southwestern Medical CenterDallasTexasUSA
| | - Riad Salem
- Division of Interventional RadiologyDepartment of RadiologyNorthwestern UniversityChicagoIllinoisUSA
| | - Tamar Taddei
- Section of Digestive DiseasesYale School of MedicineNew HavenConnecticutUSA
- VA Connecticut Healthcare SystemWest HavenConnecticutUSA
| | - Anne M Walling
- VA Greater Los Angeles Healthcare SystemLos AngelesCaliforniaUSA
- Division of General Internal Medicine and Health Services ResearchUniversity of CaliforniaLos AngelesCaliforniaUSA
| | - Elliot B Tapper
- Division of Gastroenterology and HepatologyDepartment of Internal MedicineUniversity of MichiganAnn ArborMichiganUSA
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16
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Wagle NS, Park S, Washburn D, Ohsfeldt RL, Rich NE, Singal AG, Kum H. Racial, Ethnic, and Socioeconomic Disparities in Curative Treatment Receipt and Survival in Hepatocellular Carcinoma. Hepatol Commun 2022; 6:1186-1197. [PMID: 34796703 PMCID: PMC9035560 DOI: 10.1002/hep4.1863] [Citation(s) in RCA: 42] [Impact Index Per Article: 14.0] [Reference Citation Analysis] [Abstract] [MESH Headings] [Grants] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 07/20/2021] [Revised: 10/19/2021] [Accepted: 10/30/2021] [Indexed: 12/21/2022] Open
Abstract
Hepatocellular carcinoma (HCC) disproportionately affects racial, ethnic, and low socioeconomic status (SES) populations. However, the interaction between race, ethnicity, and neighborhood SES in HCC prognosis is not well explored. This study evaluates the interaction between race and ethnicity and neighborhood SES on curative treatment utilization and overall survival among patients with HCC in the United States. We conducted a retrospective cohort study of 13,874 patients aged ≥65 years diagnosed with HCC from 2001 through 2015 using the Surveillance, Epidemiology, and End Results Medicare-linked database. We performed multivariable logistic regression to examine the association between race, ethnicity, and curative treatment receipt across SES. We also evaluated the association between curative treatment receipt and overall survival using a Cox proportional hazards model. Among 13,874 patients, only 2,617 (18.9%) patients received curative treatment. Overall, Black patients had lower odds of receiving curative treatment than White patients (odds ratio [OR], 0.76; 95% confidence interval [CI], 0.64-0.91). When stratified by neighborhood SES, Black patients living in high-poverty neighborhoods had lower odds of curative treatment receipt (OR, 0.64; 95% CI, 0.49-0.84) and worse survival (hazard ratio, 1.13; 95% CI, 1.02-1.25). Conversely, Hispanic and Asian patients had similar curative treatment receipt compared to White patients across all socioeconomic levels. Conclusion: Disparities in curative treatment receipt and overall survival are pronounced between Black and White patients. Black-White disparities appear to be moderated by neighborhood SES and are particularly evident among those living in high-poverty neighborhoods.
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Affiliation(s)
- Nikita Sandeep Wagle
- Population Informatics LabTexas A&M School of Public HealthCollege StationTXUSA
- Department of Health Policy and ManagementTexas A&M School of Public HealthCollege StationTXUSA
| | - Sulki Park
- Population Informatics LabTexas A&M School of Public HealthCollege StationTXUSA
- Department of Industrial and Systems EngineeringTexas A&M UniversityCollege StationTXUSA
| | - David Washburn
- Population Informatics LabTexas A&M School of Public HealthCollege StationTXUSA
- Department of Health Policy and ManagementTexas A&M School of Public HealthCollege StationTXUSA
| | - Robert L. Ohsfeldt
- Population Informatics LabTexas A&M School of Public HealthCollege StationTXUSA
- Department of Health Policy and ManagementTexas A&M School of Public HealthCollege StationTXUSA
| | - Nicole E. Rich
- Division of Digestive and Liver DiseasesUniversity of Texas Southwestern Medical CenterDallasTXUSA
| | - Amit G. Singal
- Division of Digestive and Liver DiseasesUniversity of Texas Southwestern Medical CenterDallasTXUSA
| | - Hye‐Chung Kum
- Population Informatics LabTexas A&M School of Public HealthCollege StationTXUSA
- Department of Health Policy and ManagementTexas A&M School of Public HealthCollege StationTXUSA
- Department of Industrial and Systems EngineeringTexas A&M UniversityCollege StationTXUSA
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17
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Zhou K, Gainey CS, Dodge JL, Setiawan VW, Liu L, Cockburn MG, Terrault NA. Diverging Incidence Trends for Hepatocellular Carcinoma in Rural and Urban Settings in the United States. Clin Gastroenterol Hepatol 2022; 20:1180-1185.e2. [PMID: 34461301 DOI: 10.1016/j.cgh.2021.08.032] [Citation(s) in RCA: 3] [Impact Index Per Article: 1.0] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 07/07/2021] [Revised: 08/10/2021] [Accepted: 08/23/2021] [Indexed: 02/07/2023]
Abstract
In the United States, hepatocellular carcinoma (HCC) is the fastest growing cause of cancer-related deaths and was the 5th most common cause in 2020.1 One in 5 Americans lives in a rural area,2 yet little is known about temporal changes in HCC incidence by rural-urban residence. Area-specific data are critical to guide public health strategies and clinical interventions. Our study compared the overall and subgroup incidence trends for HCC across rural and urban communities in the United States over the past 20 years using the North American Association of Central Cancer Registries database, which covers 93% of the United States and well-represents the rural United States (North American Association of Central Cancer Registries 14.6% rural vs United States 14.8% rural).3.
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Affiliation(s)
- Kali Zhou
- Department of Medicine, Research Center for Liver Diseases, Keck School of Medicine, University of Southern California, Los Angeles, California.
| | - Christina S Gainey
- Department of Medicine, Keck School of Medicine, University of Southern California, Los Angeles, California
| | - Jennifer L Dodge
- Department of Medicine, Research Center for Liver Diseases, Department of Population and Public Health Sciences, Keck School of Medicine, University of Southern California, Los Angeles, California
| | - V Wendy Setiawan
- Department of Population and Public Health Sciences, Norris Comprehensive Cancer Center, Keck School of Medicine, University of Southern California, Los Angeles, California
| | - Lihua Liu
- Department of Population and Public Health Sciences, Norris Comprehensive Cancer Center, Keck School of Medicine, University of Southern California, Los Angeles, California
| | - Myles G Cockburn
- Department of Population and Public Health Sciences, Norris Comprehensive Cancer Center, Keck School of Medicine, University of Southern California, Los Angeles, California
| | - Norah A Terrault
- Department of Medicine, Research Center for Liver Diseases, Keck School of Medicine, University of Southern California, Los Angeles, California
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18
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Shaddock L, Smith T. Potential for Use of Portable Ultrasound Devices in Rural and Remote Settings in Australia and Other Developed Countries: A Systematic Review. J Multidiscip Healthc 2022; 15:605-625. [PMID: 35378744 PMCID: PMC8976575 DOI: 10.2147/jmdh.s359084] [Citation(s) in RCA: 14] [Impact Index Per Article: 4.7] [Reference Citation Analysis] [Abstract] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/19/2022] [Accepted: 03/17/2022] [Indexed: 02/02/2023] Open
Abstract
Introduction Objective Methods Results Conclusion
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Affiliation(s)
- Liam Shaddock
- Medical Radiation Science, School of Health Sciences, The University of Newcastle, Newcastle, New South Wales, Australia
| | - Tony Smith
- The University of Newcastle Department of Rural Health & School of Health Sciences, The University of Newcastle, Newcastle, New South Wales, Australia
- Correspondence: Tony Smith, The University of Newcastle Department of Rural Health, C/- 69A High Street, Taree, Newcastle, NSW, Australia, Tel +61 466 440 037, Email
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