1
|
Herling A, Perluk TM, Freund O, Maharshak N, Cohen NA. Pulmonary Manifestations of IBD: Case Report and Review of the Literature. J Clin Med 2024; 13:5401. [PMID: 39336887 PMCID: PMC11432544 DOI: 10.3390/jcm13185401] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/28/2024] [Revised: 09/03/2024] [Accepted: 09/10/2024] [Indexed: 09/30/2024] Open
Abstract
This article explores the pulmonary complications associated with inflammatory bowel disease (IBD). It presents a detailed case study of a 22-year-old male with Crohn's disease exhibiting pulmonary symptoms. The review delves into the spectrum of pulmonary involvement in IBD, covering clinical presentations, diagnostic challenges, underlying pathophysiology, and management strategies. It highlights the significance of these extraintestinal manifestations on patient outcomes and quality of life. The article underscores the need for heightened clinical awareness and a systematic approach to diagnosis and management, integrating the expertise of multiple specialists. The review identifies gaps in current research, suggesting avenues for future investigation to enhance the understanding and treatment of these complex manifestations.
Collapse
Affiliation(s)
- Amit Herling
- Faculty of Medicine, Ben-Gurion University of the Negev, Be'er Sheva 8410501, Israel
| | - Tal Moshe Perluk
- Faculty of Medical and Health Sciences, Tel Aviv University, Tel Aviv 6139001, Israel
- The Pulmonary Institute, Tel Aviv Medical Center, Tel Aviv 6423906, Israel
| | - Ophir Freund
- Faculty of Medical and Health Sciences, Tel Aviv University, Tel Aviv 6139001, Israel
- The Pulmonary Institute, Tel Aviv Medical Center, Tel Aviv 6423906, Israel
| | - Nitsan Maharshak
- Faculty of Medical and Health Sciences, Tel Aviv University, Tel Aviv 6139001, Israel
- IBD Unit, Department of Gastroenterology and Liver Diseases, Tel Aviv Medical Center, Tel Aviv 6423906, Israel
| | - Nathaniel Aviv Cohen
- Faculty of Medical and Health Sciences, Tel Aviv University, Tel Aviv 6139001, Israel
- IBD Unit, Department of Gastroenterology and Liver Diseases, Tel Aviv Medical Center, Tel Aviv 6423906, Israel
| |
Collapse
|
2
|
Cassius De Linval Q, Barat M, Aissaoui M, Talabard MP, Martin C, Malamut G, Canniff E, Soyer P, Revel MP, Chassagnon G. Imaging findings of thoracic manifestations of Crohn's disease and ulcerative colitis. Insights Imaging 2024; 15:197. [PMID: 39112694 PMCID: PMC11306860 DOI: 10.1186/s13244-024-01742-4] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/30/2024] [Accepted: 06/16/2024] [Indexed: 08/10/2024] Open
Abstract
Thoracic manifestations of inflammatory bowel disease (IBD) are rare, occurring in less than 1% of patients. Unlike most other extra-intestinal manifestations, they predominate in patients with ulcerative colitis rather than in Crohn's disease. In most patients, thoracic involvement follows the onset of IBD by several years. However, thoracic involvement may also occur synchronously or even precede the onset of digestive symptoms. The thoracic manifestations of IBD include airway involvement and parenchymal lung abnormalities. Airways are the most frequent anatomical site for thoracic involvement in IBD. Airway manifestations usually develop several years after the onset of intestinal manifestations, preferentially when the latter are stable or in remission. Airway manifestations include bronchial wall thickening, bronchiectasis, small airway disease, and tracheal wall thickening. Parenchymal lung abnormalities are less prevalent in IBD and include organizing pneumonia, necrobiotic nodules, noncaseating granulomatous nodules, drug-induced pneumonia, and rarely interstitial lung diseases. The differential diagnosis between organizing pneumonia, necrobiotic nodules, and noncaseating granulomatous nodules is difficult and usually requires histopathological analysis for a definite diagnosis. Radiologists play a key role in the detection of thoracic manifestations of Crohn's disease and ulcerative colitis and, therefore, need to be familiar with their imaging findings. This article aims to offer an overview of the imaging findings of thoracic manifestations in patients with Crohn's disease or ulcerative colitis. CRITICAL RELEVANCE STATEMENT: Thoracic manifestations of Crohn's disease and ulcerative colitis include tracheal involvement, bronchiectasis, small airway disease, and parenchymal lung abnormalities such as organizing pneumonia and necrobiotic nodules. These rare manifestations (< 1% of patients) more often affect patients with ulcerative colitis. KEY POINTS: Thoracic manifestations of inflammatory bowel disease are rare, occurring in less than 1% of patients. Thoracic manifestations are more frequent in patients with ulcerative colitis than Crohn's disease. Bronchial disease is the most frequent thoracic manifestation of Crohn's disease and ulcerative colitis.
Collapse
Affiliation(s)
- Quentin Cassius De Linval
- Department of Radiology, Hôpital Cochin, AP-HP.Centre Université Paris Cité, 27 rue du Faubourg Saint-Jacques, 75014, Paris, France
| | - Maxime Barat
- Department of Radiology, Hôpital Cochin, AP-HP.Centre Université Paris Cité, 27 rue du Faubourg Saint-Jacques, 75014, Paris, France
- Université Paris Cité, 85 Boulevard Saint-Germain, 75006, Paris, France
| | - Mathilde Aissaoui
- Department of Radiology, Hôpital Cochin, AP-HP.Centre Université Paris Cité, 27 rue du Faubourg Saint-Jacques, 75014, Paris, France
- Université Paris Cité, 85 Boulevard Saint-Germain, 75006, Paris, France
| | - Marie-Pauline Talabard
- Department of Radiology, Hôpital Cochin, AP-HP.Centre Université Paris Cité, 27 rue du Faubourg Saint-Jacques, 75014, Paris, France
| | - Clémence Martin
- Université Paris Cité, 85 Boulevard Saint-Germain, 75006, Paris, France
- Respiratory Medicine and Cystic Fibrosis National Reference Center, Hôpital Cochin, AP-HP.Centre Université Paris Cité, 27 rue du Faubourg Saint-Jacques, 75014, Paris, France
| | - Georgia Malamut
- Université Paris Cité, 85 Boulevard Saint-Germain, 75006, Paris, France
- Department of Gastroenterology, Hôpital Cochin, AP-HP.Centre Université Paris Cité, 27 rue du Faubourg Saint-Jacques, 75014, Paris, France
| | - Emma Canniff
- Department of Radiology, Hôpital Cochin, AP-HP.Centre Université Paris Cité, 27 rue du Faubourg Saint-Jacques, 75014, Paris, France
- Université Paris Cité, 85 Boulevard Saint-Germain, 75006, Paris, France
| | - Philippe Soyer
- Department of Radiology, Hôpital Cochin, AP-HP.Centre Université Paris Cité, 27 rue du Faubourg Saint-Jacques, 75014, Paris, France
- Université Paris Cité, 85 Boulevard Saint-Germain, 75006, Paris, France
| | - Marie-Pierre Revel
- Department of Radiology, Hôpital Cochin, AP-HP.Centre Université Paris Cité, 27 rue du Faubourg Saint-Jacques, 75014, Paris, France
- Université Paris Cité, 85 Boulevard Saint-Germain, 75006, Paris, France
| | - Guillaume Chassagnon
- Department of Radiology, Hôpital Cochin, AP-HP.Centre Université Paris Cité, 27 rue du Faubourg Saint-Jacques, 75014, Paris, France.
- Université Paris Cité, 85 Boulevard Saint-Germain, 75006, Paris, France.
| |
Collapse
|
3
|
Zeng Q, Hu D, Li Y, Zhou Z, Wu J, Li X, Yu X. Evaluating the causal association between bronchiectasis and different types of inflammatory bowel disease: a two-sample Mendelian randomization study. Front Immunol 2024; 15:1365108. [PMID: 38638444 PMCID: PMC11024297 DOI: 10.3389/fimmu.2024.1365108] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/10/2024] [Accepted: 03/22/2024] [Indexed: 04/20/2024] Open
Abstract
Background and objectives Previous observational studies have established a connection between bronchiectasis and inflammatory bowel disease (IBD), but none of these studies have provided a clear explanation for the underlying cause of this relationship. The present study thus implemented Mendelian randomization (MR) design to explore possible bidirectional relationships between IBD and bronchiectasis risk, with an additional focus on Crohn's disease (CD) and ulcerative colitis (UC) as IBD subtypes. Materials and methods A large genome-wide association study (GWAS)-derived data pool was leveraged to examine the relationships between bronchiectasis and IBD, CD, and UC. Two-sample MR analyses were performed with an inverse variance weighted (IVW) approach supplemented with the MR-Egger and weighted median methods. Sensitivity analyses were used to further assess the reliability of the main MR study findings. The possibility of reverse causation was also evaluated using a reverse MR approach. Results The IVW MR analytical approach revealed that IBD (p = 0.074), UC (p = 0.094), and CD (p = 0.644) had no significant impact on the incidence of bronchiectasis, with the converse also being true (p = 0.471, p = 0.700, and p = 0.099, respectively). Conclusion This MR analysis demonstrated that the higher occurrence of bronchiectasis in patients with IBD is not caused by genetic predisposition.
Collapse
Affiliation(s)
- Qian Zeng
- Department of General Practice, Shenzhen Luohu Hospital Group Luohu People’s Hospital, The Third Affiliated Hospital of Shenzhen University, Shenzhen, Guangdong, China
| | - Da Hu
- Department of General Practice, Shenzhen Luohu Hospital Group Luohu People’s Hospital, The Third Affiliated Hospital of Shenzhen University, Shenzhen, Guangdong, China
| | - Yuan Li
- Department of General Practice, Shenzhen Luohu Hospital Group Luohu People’s Hospital, The Third Affiliated Hospital of Shenzhen University, Shenzhen, Guangdong, China
| | - Zhiwei Zhou
- Department of Gastroenterology, Shenzhen Luohu Hospital Group Luohu People’s Hospital, The Third Affiliated Hospital of Shenzhen University, Shenzhen, Guangdong, China
| | - Jinfeng Wu
- Department of Gastroenterology, Shenzhen Luohu Hospital Group Luohu People’s Hospital, The Third Affiliated Hospital of Shenzhen University, Shenzhen, Guangdong, China
| | - Xiaodong Li
- Department of Gastroenterology, Shenzhen Luohu Hospital Group Luohu People’s Hospital, The Third Affiliated Hospital of Shenzhen University, Shenzhen, Guangdong, China
| | - Xiqiu Yu
- Department of Gastroenterology, Shenzhen Luohu Hospital Group Luohu People’s Hospital, The Third Affiliated Hospital of Shenzhen University, Shenzhen, Guangdong, China
| |
Collapse
|
4
|
Cavalli CAM, Gabbiadini R, Dal Buono A, Quadarella A, De Marco A, Repici A, Bezzio C, Simonetta E, Aliberti S, Armuzzi A. Lung Involvement in Inflammatory Bowel Diseases: Shared Pathways and Unwanted Connections. J Clin Med 2023; 12:6419. [PMID: 37835065 PMCID: PMC10573999 DOI: 10.3390/jcm12196419] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 08/29/2023] [Revised: 10/01/2023] [Accepted: 10/06/2023] [Indexed: 10/15/2023] Open
Abstract
Inflammatory bowel diseases (IBDs) are chronic, relapsing inflammatory disorders of the gastrointestinal tract, frequently associated with extraintestinal manifestations (EIMs) that can severely affect IBD patients' quality of life, sometimes even becoming life-threatening. Respiratory diseases have always been considered a rare and subsequently neglected extraintestinal manifestations of IBD. However, increasing evidence has demonstrated that respiratory involvement is frequent in IBD patients, even in the absence of respiratory symptoms. Airway inflammation is the most common milieu of IBD-related involvement, with bronchiectasis being the most common manifestation. Furthermore, significant differences in prevalence and types of involvement are present between Crohn's disease and ulcerative colitis. The same embryological origin of respiratory and gastrointestinal tissue, in addition to exposure to common antigens and cytokine networks, may all play a potential role in the respiratory involvement. Furthermore, other causes such as drug-related toxicity and infections must always be considered. This article aims at reviewing the current evidence on the association between IBD and respiratory diseases. The purpose is to raise awareness of respiratory manifestation among IBD specialists and emphasize the need for identifying respiratory diseases in early stages to promptly treat these conditions, avoid worsening morbidity, and prevent lung damage.
Collapse
Affiliation(s)
- Carolina Aliai Micol Cavalli
- IBD Center, IRCCS Humanitas Research Hospital, Via Manzoni 56, Rozzano, 20089 Milan, Italy; (C.A.M.C.); (R.G.); (A.D.B.); (A.Q.); (A.D.M.); (C.B.)
- Department of Biomedical Sciences, Humanitas University, Via Rita Levi Montalcini 4, Pieve Emanuele, 20072 Milan, Italy; (A.R.); (S.A.)
| | - Roberto Gabbiadini
- IBD Center, IRCCS Humanitas Research Hospital, Via Manzoni 56, Rozzano, 20089 Milan, Italy; (C.A.M.C.); (R.G.); (A.D.B.); (A.Q.); (A.D.M.); (C.B.)
| | - Arianna Dal Buono
- IBD Center, IRCCS Humanitas Research Hospital, Via Manzoni 56, Rozzano, 20089 Milan, Italy; (C.A.M.C.); (R.G.); (A.D.B.); (A.Q.); (A.D.M.); (C.B.)
| | - Alessandro Quadarella
- IBD Center, IRCCS Humanitas Research Hospital, Via Manzoni 56, Rozzano, 20089 Milan, Italy; (C.A.M.C.); (R.G.); (A.D.B.); (A.Q.); (A.D.M.); (C.B.)
- Department of Biomedical Sciences, Humanitas University, Via Rita Levi Montalcini 4, Pieve Emanuele, 20072 Milan, Italy; (A.R.); (S.A.)
| | - Alessandro De Marco
- IBD Center, IRCCS Humanitas Research Hospital, Via Manzoni 56, Rozzano, 20089 Milan, Italy; (C.A.M.C.); (R.G.); (A.D.B.); (A.Q.); (A.D.M.); (C.B.)
- Department of Biomedical Sciences, Humanitas University, Via Rita Levi Montalcini 4, Pieve Emanuele, 20072 Milan, Italy; (A.R.); (S.A.)
| | - Alessandro Repici
- Department of Biomedical Sciences, Humanitas University, Via Rita Levi Montalcini 4, Pieve Emanuele, 20072 Milan, Italy; (A.R.); (S.A.)
- Division of Gastroenterology and Digestive Endoscopy, Department of Gastroenterology, IRCCS Humanitas Research Hospital, Via Manzoni 56, Rozzano, 20089 Milan, Italy
| | - Cristina Bezzio
- IBD Center, IRCCS Humanitas Research Hospital, Via Manzoni 56, Rozzano, 20089 Milan, Italy; (C.A.M.C.); (R.G.); (A.D.B.); (A.Q.); (A.D.M.); (C.B.)
- Department of Biomedical Sciences, Humanitas University, Via Rita Levi Montalcini 4, Pieve Emanuele, 20072 Milan, Italy; (A.R.); (S.A.)
| | - Edoardo Simonetta
- Respiratory Unit, IRCCS Humanitas Research Hospital, Via Manzoni 56, Rozzano, 20089 Milan, Italy;
| | - Stefano Aliberti
- Department of Biomedical Sciences, Humanitas University, Via Rita Levi Montalcini 4, Pieve Emanuele, 20072 Milan, Italy; (A.R.); (S.A.)
- Respiratory Unit, IRCCS Humanitas Research Hospital, Via Manzoni 56, Rozzano, 20089 Milan, Italy;
| | - Alessandro Armuzzi
- IBD Center, IRCCS Humanitas Research Hospital, Via Manzoni 56, Rozzano, 20089 Milan, Italy; (C.A.M.C.); (R.G.); (A.D.B.); (A.Q.); (A.D.M.); (C.B.)
- Department of Biomedical Sciences, Humanitas University, Via Rita Levi Montalcini 4, Pieve Emanuele, 20072 Milan, Italy; (A.R.); (S.A.)
| |
Collapse
|
5
|
Liu J, Zong C, Yu X, Ding Y, Chang B, Wang R, Sang L. Alanyl-Glutamine (Ala-Gln) Ameliorates Dextran Sulfate Sodium (DSS)-Induced Acute Colitis by Regulating the Gut Microbiota, PI3K-Akt/NF-κB/STAT3 Signaling, and Associated Pulmonary Injury. ACS Infect Dis 2023; 9:979-992. [PMID: 36917734 DOI: 10.1021/acsinfecdis.3c00014] [Citation(s) in RCA: 6] [Impact Index Per Article: 3.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 03/15/2023]
Abstract
The aim of this study was to investigate the protective effect of alanyl-glutamine (Ala-Gln) on acute colitis complicated by pulmonary injury induced by dextran sulfate sodium (DSS) in C57BL/6 mice. The results showed that Ala-Gln intervention alleviated weight loss, the disease activity index (DAI), colon shortening, and pathological injury and regulated the absolute number of CD4+T-cell subsets in mesenteric lymph nodes (MLNs). In addition, Ala-Gln intervention significantly ameliorated the composition of the gut microbiota in mice with DSS- induced acute colitis, significantly decreasing the relative abundance of Desulfovibrionaceae and increasing the abundances of Gastranaerophilales, Clostridia-vadinBB60, and Alistipes. Moreover, Ala-Gln treatment significantly inhibited the activation of the PI3K-Akt/NF-κB/STAT3 inflammatory signaling pathways in the colon of mice with DSS-induced acute colitis. Notably, Ala-Gln intervention also alleviated the pulmonary injury as well as the imbalance in levels of CD4+T-cell subsets in pulmonary tissue in mice with DSS-induced acute colitis. In conclusion, Ala-Gln alleviates DSS-induced acute colitis by regulating the gut microflora and PI3K-Akt/NF-κB/STAT3 signaling pathways, as well as by alleviating accompanying pulmonary injury.
Collapse
Affiliation(s)
- Jing Liu
- Clinical Laboratory, Affiliated Zhongshan Hospital of Dalian University, No. 6 Jiefang Street, Dalian 110006 Liaoning, China
| | - Chengguo Zong
- Clinical Laboratory, Affiliated Zhongshan Hospital of Dalian University, No. 6 Jiefang Street, Dalian 110006 Liaoning, China
| | - Xin Yu
- Clinical Laboratory, Affiliated Zhongshan Hospital of Dalian University, No. 6 Jiefang Street, Dalian 110006 Liaoning, China
| | - Yan Ding
- Clinical Laboratory, Affiliated Zhongshan Hospital of Dalian University, No. 6 Jiefang Street, Dalian 110006 Liaoning, China
| | - Bing Chang
- Department of Gastroenterology, The First Affiliated Hospital of China Medical University, No. 155 Nanjing North Street, Shenyang 110001, Liaoning, China
| | - Ruoyu Wang
- Affiliated Zhongshan Hospital of Dalian University, No. 6 Jiefang Street, Dalian 110006, Liaoning, China.,The Key Laboratory of Biomarker High Throughput Screening and Target Translation of Breast and Gastrointestinal Tumor, Dalian 116001, Liaoning, China
| | - Lixuan Sang
- Department of Gastroenterology, Shengjing Hospital of China Medical University, No. 36 Sanhao Street, Shenyang 110022, Liaoning, China
| |
Collapse
|
6
|
Moda M, Suga M, Kasai S, Okochi Y, Yoshimura N, Fukata M, Tokuda H. Incidence, Characteristics, Clinical Course, and Risk Factors of Ulcerative Colitis-related Lung Diseases. Chest 2022; 162:1310-1323. [PMID: 35691329 DOI: 10.1016/j.chest.2022.05.037] [Citation(s) in RCA: 3] [Impact Index Per Article: 1.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/31/2022] [Revised: 04/27/2022] [Accepted: 05/19/2022] [Indexed: 12/14/2022] Open
Abstract
BACKGROUND Ulcerative colitis (UC) is a chronic GI inflammatory disorder involving various extraintestinal organs, including the lungs. Although UC-related lung diseases (UC-LDs) have been widely recognized, much remains unclear. RESEARCH QUESTION What are the incidence, characteristics, clinical course, and risk factors of UC-LD? STUDY DESIGN AND METHODS This study retrospectively identified and classified UC-LDs by reviewing the medical records of consecutive patients with UC. The incidence, characteristics, and clinical course of each UC-LD type were investigated, and the clinical characteristics of patients with and without each UC-LD type were compared. RESULTS Among 563 patients with UC, 28 (5.0%) developed UC-LD during a mean follow-up period of 77 months. A majority of them displayed airway disease (AD) (n = 13 [2.3%]) or organizing pneumonia (OP) (n = 10 [1.8%]); there were six cases of interstitial pneumonias other than OP (IP) (0.8%) and one of pleuritis (0.2%). All 13 patients with AD responded favorably to inhaled or systemic corticosteroids, although five experienced frequent exacerbations. Older age and a history of colectomy were identified as the risk factors for developing AD. Nine of the 10 cases of OP were possibly due to drug-induced pathogenesis. Only one case showed recurrence, and all cases of OP exhibited a favorable clinical course with discontinuation of the suspicious drug and/or initiation of corticosteroid. The clinical course of IP depended on the existence of fibrosis, and IP with fibrosis was associated with gradual deterioration. Older age was associated with the development of IP. INTERPRETATION A nonnegligible number of patients with UC may develop UC-LD. AD, OP, and IP without fibrosis show good prognosis following steroid therapy along with the specific management for each UC-LD type, whereas IP with fibrosis shows gradual deterioration with poor prognosis. Our results provide cues to establish better management of UC-LDs.
Collapse
Affiliation(s)
- Mitsuhiro Moda
- Department of Respiratory Medicine, National Hospital Organization Kinki-chuo Chest Medical Center, Osaka, Japan; Department of Respiratory Medicine, Japan Community Health Care Organization Tokyo Yamate Medical Center, Tokyo, Japan.
| | - Miyuri Suga
- Department of Respiratory Medicine, Japan Community Health Care Organization Tokyo Yamate Medical Center, Tokyo, Japan; Department of Respiratory Medicine, Graduate School of Medicine Nippon Medical School, Tokyo, Japan
| | - Shogo Kasai
- Department of Respiratory Medicine, Japan Community Health Care Organization Tokyo Yamate Medical Center, Tokyo, Japan
| | - Yasumi Okochi
- Department of Respiratory Medicine, Japan Community Health Care Organization Tokyo Yamate Medical Center, Tokyo, Japan
| | - Naoki Yoshimura
- Center for Inflammatory Bowel Disease, Division of Gastroenterology, Department of Internal Medicine, Japan Community Health Care Organization Tokyo Yamate Medical Center, Tokyo, Japan
| | - Masayuki Fukata
- Center for Inflammatory Bowel Disease, Division of Gastroenterology, Department of Internal Medicine, Japan Community Health Care Organization Tokyo Yamate Medical Center, Tokyo, Japan
| | - Hitoshi Tokuda
- Department of Respiratory Medicine, Japan Community Health Care Organization Tokyo Yamate Medical Center, Tokyo, Japan
| |
Collapse
|
7
|
Progressive stridor: extraintestinal airway manifestations in a pediatric patient with inflammatory bowel disease. Clin J Gastroenterol 2022; 15:929-933. [DOI: 10.1007/s12328-022-01674-w] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 03/30/2022] [Accepted: 06/29/2022] [Indexed: 02/07/2023]
|
8
|
Bezzio C, Della Corte C, Vernero M, Di Luna I, Manes G, Saibeni S. Inflammatory bowel disease and immune-mediated inflammatory diseases: looking at the less frequent associations. Therap Adv Gastroenterol 2022; 15:17562848221115312. [PMID: 35924080 PMCID: PMC9340394 DOI: 10.1177/17562848221115312] [Citation(s) in RCA: 29] [Impact Index Per Article: 9.7] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 02/12/2022] [Accepted: 07/06/2022] [Indexed: 02/04/2023] Open
Abstract
Patients with inflammatory bowel disease (IBD) often have other immune-mediated inflammatory diseases (IMIDs), and the prevalence of any IMID is higher in IBD patients than in the general population. IBD and other IMIDs involve alterations in innate and adaptive immune responses. Their co-occurrence depends on shared immune and inflammatory processes, pathogenic mechanisms, and genetic and environmental risk factors, including drugs, especially tumor necrosis factor inhibitors. The more common IMIDs associated with IBD have been widely described, so this review focuses on the less frequent associations. The IMIDs discussed here are skin disorders (psoriasis, atopic dermatitis, vitiligo, epidermolysis bullosa acquisita, cutaneous polyarteritis nodosa, and hidradenitis suppurativa), hepato-pancreatic diseases (autoimmune hepatitis, granulomatous hepatitis, and autoimmune pancreatitis), endocrine diseases (autoimmune thyroid diseases, and type 1 diabetes mellitus), multiple sclerosis, and respiratory diseases (asthma, bronchiectasis, and interstitial pneumonia). The early detection of IMIDs in IBD patients is important to prevent their deleterious clinical course and limit their psychological impact. Care for IBD patients with IMIDs should be multispecialist, with a single therapeutic strategy instead of treating each disease separately.
Collapse
|
9
|
Sofia C, Adiletta V, Iovene B, Sgalla G, Richeldi L. Acute Respiratory Distress Syndrome and Lung Fibrosis Complicating Surgery in a Patient With Crohn's Disease. Inflamm Bowel Dis 2022; 28:e31-e32. [PMID: 34730805 DOI: 10.1093/ibd/izab255] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.3] [Reference Citation Analysis] [MESH Headings] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Indexed: 12/09/2022]
Affiliation(s)
- Carmelo Sofia
- Fondazione Policlinico Universitario A. Gemelli IRCCS, Rome, Italy
| | | | - Bruno Iovene
- Fondazione Policlinico Universitario A. Gemelli IRCCS, Rome, Italy
| | - Giacomo Sgalla
- Fondazione Policlinico Universitario A. Gemelli IRCCS, Rome, Italy
| | - Luca Richeldi
- Fondazione Policlinico Universitario A. Gemelli IRCCS, Rome, Italy
- Università Cattolica del Sacro Cuore, Rome, Italy
| |
Collapse
|
10
|
Cohen R, Shteinberg M. Diagnosis and Evaluation of Bronchiectasis. Clin Chest Med 2022; 43:7-22. [DOI: 10.1016/j.ccm.2021.11.001] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/29/2022]
|
11
|
The Spectrum of Airway Involvement in Inflammatory Bowel Disease. Clin Chest Med 2022; 43:141-155. [DOI: 10.1016/j.ccm.2021.12.003] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/19/2022]
|
12
|
Jochmann A, Trachsel D, Hammer J. Inflammatory bowel disease and the lung in paediatric patients. Breathe (Sheff) 2021; 17:200269. [PMID: 34295391 PMCID: PMC8291939 DOI: 10.1183/20734735.0269-2020] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.3] [Reference Citation Analysis] [Abstract] [Download PDF] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/28/2020] [Accepted: 04/15/2021] [Indexed: 02/06/2023] Open
Abstract
The prevalence of inflammatory bowel disease (IBD) has increased over the past 20 years. Pulmonary involvement in paediatric IBD is rare but may be missed since the spectrum of symptoms is broad and mimics other diseases. The most important differential diagnoses of pulmonary manifestations of IBD are infections and therapy-related side-effects. There is no gold standard to diagnose respiratory manifestations in children with IBD. Diagnostic tests should be chosen according to history and clinical presentation. Treatment of respiratory manifestations of IBD includes inhaled or oral corticosteroids and initiation or step-up of immunomodulatory IBD therapies. Pulmonary involvement in paediatric IBD is rare but may be underdiagnosed. The spectrum of symptoms is broad and mimics other diseases. The differentiation between IBD-related and drug-induced pulmonary manifestation can be challenging.https://bit.ly/3uZBvpA
Collapse
Affiliation(s)
- Anja Jochmann
- Division of Respiratory and Critical Care Medicine, University Children's Hospital Basel (UKBB), University of Basel, Basel, Switzerland
| | - Daniel Trachsel
- Division of Respiratory and Critical Care Medicine, University Children's Hospital Basel (UKBB), University of Basel, Basel, Switzerland
| | - Jürg Hammer
- Division of Respiratory and Critical Care Medicine, University Children's Hospital Basel (UKBB), University of Basel, Basel, Switzerland
| |
Collapse
|
13
|
Trivedi S, Grossmann AH, Jensen O, Cody MJ, Wahlig TA, Hayakawa Serpa P, Langelier C, Warren KJ, Yost CC, Leung DT. Intestinal Infection Is Associated With Impaired Lung Innate Immunity to Secondary Respiratory Infection. Open Forum Infect Dis 2021; 8:ofab237. [PMID: 34189172 PMCID: PMC8231398 DOI: 10.1093/ofid/ofab237] [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: 03/11/2021] [Accepted: 05/05/2021] [Indexed: 11/23/2022] Open
Abstract
Background Pneumonia and diarrhea are among the leading causes of death worldwide, and epidemiological studies have demonstrated that diarrhea is associated with an increased risk of subsequent pneumonia. Our aim was to determine the impact of intestinal infection on innate immune responses in the lung. Methods Using a mouse model of intestinal infection by Salmonella enterica serovar Typhimurium (S. Typhimurium [ST]), we investigated associations between gastrointestinal infections and lung innate immune responses to bacterial (Klebsiella pneumoniae) challenge. Results We found alterations in frequencies of innate immune cells in the lungs of intestinally infected mice compared with uninfected mice. On subsequent challenge with K. pneumoniae, we found that mice with prior intestinal infection have higher lung bacterial burden and inflammation, increased neutrophil margination, and neutrophil extracellular traps, but lower overall numbers of neutrophils, compared with mice without prior intestinal infection. Total numbers of dendritic cells, innate-like T cells, and natural killer cells were not different between mice with and without prior intestinal infection. Conclusions Together, these results suggest that intestinal infection impacts lung innate immune responses, most notably neutrophil characteristics, potentially resulting in increased susceptibility to secondary pneumonia.
Collapse
Affiliation(s)
- Shubhanshi Trivedi
- Division of Infectious Disease, Department of Internal Medicine, University of Utah, Salt Lake City, Utah, USA
| | - Allie H Grossmann
- Huntsman Cancer Institute, University of Utah, Salt Lake City, Utah, USA.,Division of Anatomic Pathology, Department of Pathology, University of Utah, Salt Lake City, Utah, USA.,Molecular Medicine Program, University of Utah, Salt Lake City, Utah, USA
| | - Owen Jensen
- Division of Infectious Disease, Department of Internal Medicine, University of Utah, Salt Lake City, Utah, USA
| | - Mark J Cody
- Division of Neonatology, Department of Pediatrics, University of Utah, Salt Lake City, Utah, USA
| | - Taylor A Wahlig
- Division of Infectious Disease, Department of Internal Medicine, University of Utah, Salt Lake City, Utah, USA
| | - Paula Hayakawa Serpa
- Chan Zuckerberg Biohub, San Francisco, California, USA.,Division of Infectious Diseases, Department of Medicine, University of California-San Francisco, San Francisco, California, USA
| | - Charles Langelier
- Chan Zuckerberg Biohub, San Francisco, California, USA.,Division of Infectious Diseases, Department of Medicine, University of California-San Francisco, San Francisco, California, USA
| | - Kristi J Warren
- Division of Pulmonary Medicine, Department of Internal Medicine, University of Utah, Salt Lake City, Utah, USA
| | - Christian C Yost
- Division of Neonatology, Department of Pediatrics, University of Utah, Salt Lake City, Utah, USA.,Molecular Medicine Program, University of Utah, Salt Lake City, Utah, USA
| | - Daniel T Leung
- Division of Infectious Disease, Department of Internal Medicine, University of Utah, Salt Lake City, Utah, USA.,Division of Microbiology and Immunology, Department of Pathology, University of Utah, Salt Lake City, Utah, USA
| |
Collapse
|
14
|
Barfield E, Deshmukh F, Slighton E, Lentine J, Lu Y, Ma X, Christos P, Sockolow R, Loughlin G, Pillai S. Pulmonary Manifestations in Adolescents With Inflammatory Bowel Disease. Clin Pediatr (Phila) 2020; 59:573-579. [PMID: 32146830 PMCID: PMC8359570 DOI: 10.1177/0009922820910821] [Citation(s) in RCA: 4] [Impact Index Per Article: 0.8] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Indexed: 12/26/2022]
Abstract
Objectives. The available literature on pulmonary disease in pediatric inflammatory bowel disease is limited. We evaluated the prevalence of pulmonary manifestations in pediatric inflammatory bowel disease and their association with disease severity. Methods. Patients completed the St. George's Respiratory Questionnaire (SGRQ), a self-reported measure of quality of life in patients with pulmonary disease. Chart review provided demographic information and Pediatric Crohn's Disease Activity Index (PCDAI) and Pediatric Ulcerative Colitis Activity Index scores. Regression models were utilized to evaluate associations between SGRQ score and clinical risk factors. Results. The prevalence of pulmonary manifestations was 9.62% (95% confidence interval = 5.48% to -15.36%). PCDAI scores in Crohn's disease patients with pulmonary symptoms were significantly higher (SGRQ mean = 10.71 ± 10.94) than in patients without such symptoms. SGRQ score was also higher in patients with indeterminate colitis (8.64, 95% confidence interval = 0.72-16.57, P = .03), when compared with Crohn's disease. Conclusions. Additional investigations including pulmonary function tests and imaging could provide further insight into this issue.
Collapse
Affiliation(s)
- Elaine Barfield
- Division of Pediatric Gastroenterology and Nutrition, New York-Presbyterian/Weill Cornell Medicine, New York, NY
| | - Farah Deshmukh
- Division of Pediatric Gastroenterology and Nutrition, New York-Presbyterian/Weill Cornell Medicine, New York, NY
| | - Elisabeth Slighton
- Division of Pediatric Gastroenterology and Nutrition, New York-Presbyterian/Weill Cornell Medicine, New York, NY
| | - Jennifer Lentine
- Division of Pediatric Gastroenterology and Nutrition, New York-Presbyterian/Weill Cornell Medicine, New York, NY
| | - Yao Lu
- Division of Biostatistics and Epidemiology, Department of Healthcare Policy & Research, Weill Cornell Medicine, New York, NY
| | - Xiaoyue Ma
- Division of Biostatistics and Epidemiology, Department of Healthcare Policy & Research, Weill Cornell Medicine, New York, NY
| | - Paul Christos
- Division of Biostatistics and Epidemiology, Department of Healthcare Policy & Research, Weill Cornell Medicine, New York, NY
| | - Robbyn Sockolow
- Division of Pediatric Gastroenterology and Nutrition, New York-Presbyterian/Weill Cornell Medicine, New York, NY
| | - Gerald Loughlin
- Division of Pediatric Pulmonology, New York-Presbyterian/Weill Cornell Medicine, New York, NY
| | - Sophia Pillai
- Division of Pediatrics and Adolescent Medicine, Mayo Clinic, Rochester, Minnesota
| |
Collapse
|
15
|
Abstract
We report a unique case of ulcerative colitis-associated bronchiectasis in a pediatric patient 6 years after colectomy. The patient presented with a chronic cough and had a computed tomography demonstrating bronchiectasis. She was treated with sputum expectoration (airway clearance) via chest physiotherapy and pulse-dose steroids with a prolonged oral taper. Her initial response was excellent; however, she experienced a recurrence of symptoms with de-escalation of airway clearance. Pulmonary extraintestinal manifestations of inflammatory bowel disease are most often diagnosed later in life. Both the severity of this patient's presentation and her age are unique to this case.
Collapse
|
16
|
Camus P, Colby TV. Airway and lung involvement in inflammatory bowel disease. PULMONARY MANIFESTATIONS OF SYSTEMIC DISEASES 2019. [DOI: 10.1183/2312508x.10015019] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Track Full Text] [Subscribe] [Scholar Register] [Indexed: 01/06/2025]
|
17
|
Hill AT, Sullivan AL, Chalmers JD, De Soyza A, Elborn SJ, Floto AR, Grillo L, Gruffydd-Jones K, Harvey A, Haworth CS, Hiscocks E, Hurst JR, Johnson C, Kelleher PW, Bedi P, Payne K, Saleh H, Screaton NJ, Smith M, Tunney M, Whitters D, Wilson R, Loebinger MR. British Thoracic Society Guideline for bronchiectasis in adults. Thorax 2019; 74:1-69. [PMID: 30545985 DOI: 10.1136/thoraxjnl-2018-212463] [Citation(s) in RCA: 284] [Impact Index Per Article: 47.3] [Reference Citation Analysis] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 12/27/2022]
Affiliation(s)
- Adam T Hill
- Respiratory Medicine, Royal Infirmary of Edinburgh and University of Edinburgh, Edinburgh, UK
| | - Anita L Sullivan
- Department of Respiratory Medicine, University Hospitals Birmingham NHS Foundation Trust (Queen Elizabeth Hospital), Birmingham, UK
| | - James D Chalmers
- Scottish Centre for Respiratory Research, University of Dundee, Ninewells Hospital, Dundee, UK
| | - Anthony De Soyza
- Institute of Cellular Medicine, NIHR Biomedical Research Centre for Aging and Freeman Hospital Adult Bronchiectasis service, Newcastle upon Tyne Hospitals NHS Foundation Trust, Newcastle, UK
| | - Stuart J Elborn
- Royal Brompton Hospital and Imperial College London, and Queens University Belfast
| | - Andres R Floto
- Department of Medicine, University of Cambridge, Cambridge UK.,Cambridge Centre for Lung Infection, Royal Papworth Hospital, Cambridge UK
| | | | | | - Alex Harvey
- Department of Clinical Sciences, Brunel University London, London, UK
| | - Charles S Haworth
- Cambridge Centre for Lung Infection, Royal Papworth Hospital, Cambridge UK
| | | | - John R Hurst
- UCL Respiratory, University College London, London, UK
| | | | - Peter W Kelleher
- Centre for Immunology and Vaccinology, Chelsea &Westminster Hospital Campus, Department of Medicine, Imperial College London.,Host Defence Unit, Department of Respiratory Medicine, Royal Brompton Hospital and Harefield NHS Foundation Trust, London.,Chest & Allergy Clinic St Mary's Hospital, Imperial College Healthcare NHS Trust
| | - Pallavi Bedi
- University of Edinburgh MRC Centre for Inflammation Research, Edinburgh, UK
| | | | | | | | - Maeve Smith
- University of Alberta, Edmonton, Alberta, Canada
| | - Michael Tunney
- School of Pharmacy, Queens University Belfast, Belfast, UK
| | | | - Robert Wilson
- Host Defence Unit, Department of Respiratory Medicine, Royal Brompton Hospital and Harefield NHS Foundation Trust, London
| | - Michael R Loebinger
- Host Defence Unit, Department of Respiratory Medicine, Royal Brompton Hospital and Harefield NHS Foundation Trust, London
| |
Collapse
|
18
|
Chuah CS, Noble C, Leitch A. Case of steroid-resistant Crohn's-associated bronchiolitis in the setting of quiescent gastrointestinal disease treated with infliximab. BMJ Case Rep 2018; 11:11/1/e226934. [PMID: 30567117 PMCID: PMC6301768 DOI: 10.1136/bcr-2018-226934] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.1] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 12/17/2022] Open
Abstract
A fit, 36-year-old man with a history of Crohn's disease previously treated with azathioprine, presented acutely with progressive shortness of breath on exertion and pleuritic chest pain. At the time of presentation, his Crohn's disease was quiescent, supported by a normal faecal calprotectin. The initial chest CT suggested the presence of a diffuse inflammatory disorder and he was subsequently started on high dose oral steroids. Despite 4 months of steroid therapy, there was minimal improvement. Following discussion at the inflammatory bowel disease multidisciplinary team meeting, a decision was made to commence infliximab. Subsequently, he made a dramatic clinical and physiological recovery. His forced expiratory volume in 1 s improved from 2.22 L/min (50% predicted) to 3.65 L/min (93% predicted) and he returned to baseline levels of exercise.
Collapse
Affiliation(s)
- Cher Shiong Chuah
- Department of Gastroenterology, Western General Hospital, Edinburgh, UK
| | - Colin Noble
- Department of Gastroenterology, Western General Hospital, Edinburgh, UK
| | - Andrew Leitch
- Department of Respiratory Medicine, Western General Hospital, Edinburgh, UK
| |
Collapse
|
19
|
Al-Jahdali H, Alshimemeri A, Mobeireek A, Albanna AS, Al Shirawi NN, Wali S, Alkattan K, Alrajhi AA, Mobaireek K, Alorainy HS, Al-Hajjaj MS, Chang AB, Aliberti S. The Saudi Thoracic Society guidelines for diagnosis and management of noncystic fibrosis bronchiectasis. Ann Thorac Med 2017; 12:135-161. [PMID: 28808486 PMCID: PMC5541962 DOI: 10.4103/atm.atm_171_17] [Citation(s) in RCA: 26] [Impact Index Per Article: 3.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 05/29/2017] [Accepted: 05/30/2017] [Indexed: 12/14/2022] Open
Abstract
This is the first guideline developed by the Saudi Thoracic Society for the diagnosis and management of noncystic fibrosis bronchiectasis. Local experts including pulmonologists, infectious disease specialists, thoracic surgeons, respiratory therapists, and others from adult and pediatric departments provided the best practice evidence recommendations based on the available international and local literature. The main objective of this guideline is to utilize the current published evidence to develop recommendations about management of bronchiectasis suitable to our local health-care system and available resources. We aim to provide clinicians with tools to standardize the diagnosis and management of bronchiectasis. This guideline targets primary care physicians, family medicine practitioners, practicing internists and respiratory physicians, and all other health-care providers involved in the care of the patients with bronchiectasis.
Collapse
Affiliation(s)
- Hamdan Al-Jahdali
- College of Medicine, King Saud Bin Abdulaziz University for Health Sciences, Department of Medicine, Pulmonary Division, King Abdulaziz Medical City, Riyadh, Saudi Arabia
| | - Abdullah Alshimemeri
- College of Medicine, King Saud Bin Abdulaziz University for Health Sciences, Department of Medicine, Pulmonary Division, King Abdulaziz Medical City, Riyadh, Saudi Arabia
| | - Abdullah Mobeireek
- College of Medicine, Alfaisal University, Riyadh, Saudi Arabia
- King Faisal Specialist Hospital and Research Centre, Department of Medicine, Pulmonary Division, Riyadh, Saudi Arabia
| | - Amr S. Albanna
- College of Medicine, King Saud Bin Abdulaziz University for Health Sciences, Department of Medicine, Pulmonary Division, King Abdulaziz Medical City, Jeddah, Saudi Arabia
- King Abdullah International Medical Research Center, Jeddah, Saudi Arabia
| | | | - Siraj Wali
- College of Medicine, King Abdulaziz University, Respiratory Unit, Department of Medicine, Jeddah, Saudi Arabia
| | - Khaled Alkattan
- College of Medicine, Alfaisal University, Riyadh, Saudi Arabia
| | - Abdulrahman A. Alrajhi
- College of Medicine, Alfaisal University, Riyadh, Saudi Arabia
- King Faisal Specialist Hospital and Research Centre, Department of Medicine, Infectious Disease Division, Riyadh, Saudi Arabia
| | - Khalid Mobaireek
- College of Medicine, King Saud University, King Khalid University Hospital, Pediatric Pulmonology Division, Riyadh, Saudi Arabia
| | - Hassan S. Alorainy
- King Faisal Specialist Hospital and Research Centre, Respiratory Therapy Services, Riyadh, Saudi Arabia
| | - Mohamed S. Al-Hajjaj
- Department of Clinical Sciences, College of Medicine. University of Sharjah, Sharjah, UAE
| | - Anne B. Chang
- International Reviewer, Children's Centre of Health Research Queensland University of Technology, Queensland
- International Reviewer, Brisbane and Child Health Division, Menzies School of Health Research, Darwin, Australia
| | - Stefano Aliberti
- International Reviewer, Department of Pathophysiology and Transplantation, University of MilanInternal Medicine Department, Respiratory Unit and Cystic Fibrosis Adult Center. Fondazione IRCCS Ca' Granda Ospedale Maggiore Policlinico Via Francesco Sforza 35, 20122, Milan, Italy
| |
Collapse
|
20
|
Vutcovici M, Brassard P, Bitton A. Inflammatory bowel disease and airway diseases. World J Gastroenterol 2016; 22:7735-7741. [PMID: 27678355 PMCID: PMC5016372 DOI: 10.3748/wjg.v22.i34.7735] [Citation(s) in RCA: 42] [Impact Index Per Article: 4.7] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 03/24/2016] [Revised: 06/14/2016] [Accepted: 07/06/2016] [Indexed: 02/06/2023] Open
Abstract
Airway diseases are the most commonly described lung manifestations of inflammatory bowel disease (IBD). However, the similarities in disease pathogenesis and the sharing of important environmental risk factors and genetic susceptibility suggest that there is a complex interplay between IBD and airway diseases. Recent evidence of IBD occurrence among patients with airway diseases and the higher than estimated prevalence of subclinical airway injuries among IBD patients support the hypothesis of a two-way association. Future research efforts should be directed toward further exploration of this association, as airway diseases are highly prevalent conditions with a substantial public health impact.
Collapse
|
21
|
Ongun EA, Artan R, Bingol A, Dursun O. A rare aspect of Crohn's disease: Pulmonary involvement in a child. Indian J Crit Care Med 2016; 20:114-6. [PMID: 27076713 PMCID: PMC4810924 DOI: 10.4103/0972-5229.175941] [Citation(s) in RCA: 3] [Impact Index Per Article: 0.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 12/25/2022] Open
Abstract
Crohn's disease (CD), known as the disease of gastrointestinal system, is a granulamatous systemic disorder with extraintestinal manifestations including the respiratory system. The resemblance in the embriological origins and the immunities of both organ systems' mucosae, also the circulating immune complexes and the autoantibodies are accepted as contributing factors. The shift of inflammation may become prominent when the colon is removed after colectomy and independent of the bowel disease activity; pulmonary involvement may be exarbecated. In the pediatric population, CD associated pulmonary involvement is very rare, mainly in the form of subclinical alterations and the data are limited mostly to case reports. Therefore, it is possibly overlooked since the diagnosis relies on suspicion. We represent a 5-year-old CD patient with previous bronchiolitis episodes that might have resulted from CD-associated pulmonary involvement; whom later developed severe pneumonia resulting in acute respiratory distress syndrome and bronchiectasia following a colectomy operation.
Collapse
Affiliation(s)
- Ebru Atike Ongun
- Department of Pediatrics, Division of Pediatric Critical Care, School of Medicine, Akdeniz University, Antalya, Turkey
| | - Reha Artan
- Department of Pediatrics, Division of Pediatric Gastroenterology, School of Medicine, Akdeniz University, Antalya, Turkey
| | - Aysen Bingol
- Department of Pediatrics, Division of Pediatric Pulmonology, School of Medicine, Akdeniz University, Antalya, Turkey
| | - Oguz Dursun
- Department of Pediatrics, Division of Pediatric Critical Care, School of Medicine, Akdeniz University, Antalya, Turkey
| |
Collapse
|
22
|
Brown SR, Coviello LC. Extraintestinal Manifestations Associated with Inflammatory Bowel Disease. Surg Clin North Am 2016; 95:1245-59, vii. [PMID: 26596925 DOI: 10.1016/j.suc.2015.08.002] [Citation(s) in RCA: 20] [Impact Index Per Article: 2.2] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 02/07/2023]
Abstract
Inflammatory bowel disease (IBD) affects multiple organ systems outside of the gastrointestinal tract. The clinician treating patients with IBD should be acutely aware of the diagnosis and treatment of extraintestinal manifestations in order to decrease morbidity. The management can be difficult and often times requires a multidisciplinary approach. Future research investigating the pathophysiology, diagnosis, and treatment is needed to further the care of these patients.
Collapse
Affiliation(s)
- Shaun R Brown
- Department of Colorectal Surgery, Oschner Clinic Foundation, New Orleans, LA, USA; Department of Surgery, Uniformed Services University of Health Sciences, Bethesda, MD 20814, USA
| | - Lisa C Coviello
- Department of Surgery, National Capital Region Medical Directorate, Fort Belvoir, VA 22060, USA; Department of Surgery of the Uniformed Services University of Health Sciences and the Walter Reed National Military Medical Center, Bethesda, MD 20814, USA.
| |
Collapse
|
23
|
Zhao YJ, Wang XM, Su L, Zhu CH, Zhai JS, Zheng N, Zhang M, Li N. Effect of compound dracorhodin enema on pulmonary and colonic expression of interleukin-6 in mice with distal ulcerative colitis. Shijie Huaren Xiaohua Zazhi 2015; 23:3352-3360. [DOI: 10.11569/wcjd.v23.i21.3352] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Indexed: 02/06/2023] Open
Abstract
AIM: To investigate the protective effect of compound dracorhodin enema on the lung and intestine of mice with distal ulcerative colitis (UC).
METHODS: Sixty male BALB/c mice were randomly divided into four groups (n = 15 each): a normal group, a dextran sulfate sodium (DSS) group, a compound dracorhodin enema group, and a DSS + compound dracorhodin enema group. After inducing UC, the normal group and DSS group were given 1 mL saline, and the other two groups were given compound dracorhodin enema [0.075 g/(kg•d), 1 mL] by gavage. After treatment, disease activity index (DAI) score, colonic histopathology score (HI), lung HI score, and hematoxylin-eosin (HE) staining were used to evaluate the severity of inflammation. Enzyme-linked immunosorbent assay (ELISA), immunohistochemistry, and real-time quantitative PCR (RT-QPCR) assay were used to detect the expression of interleukin (IL)-6 in the lung and colon.
RESULTS: Compared with the normal group and compound dracorhodin enema group, DAI score, colonic HI score, and lung HI score were significantly higher in the other two groups (P < 0.05). Compared with the DSS + compound dracorhodin enema group, colonic and pulmonary tissue inflammation was significantly more severe and pulmonary and colonic expression of IL-6 was significantly higher in the DSS group (P < 0.05).
CONCLUSION: Compound dracorhodin enema can decrease the expression of IL-6 and therefore alleviate UC and UC related lung injury in mice.
Collapse
|
24
|
von Wichert P, Barth P, von Wichert G. Tracheal and bronchial involvement in colitis ulcerosa - a colo-bronchitic syndrome? A case report and some additional considerations. GERMAN MEDICAL SCIENCE : GMS E-JOURNAL 2015; 13:Doc03. [PMID: 25834480 PMCID: PMC4381659 DOI: 10.3205/000207] [Citation(s) in RCA: 4] [Impact Index Per Article: 0.4] [Reference Citation Analysis] [Abstract] [Key Words] [Download PDF] [Figures] [Subscribe] [Scholar Register] [Received: 06/18/2014] [Revised: 03/23/2015] [Indexed: 12/13/2022]
Abstract
Systemic involvement is well known in patients with inflammatory bowel diseases (IBD), but there are only few data looking to Crohn’s disease (CD) and ulcerative colitis (UC) separately instead of lumping together both entities to IBD. The frequency of bronchial involvement in UC is not yet exactly analysed but reported to be rare. We asked 100 patients with UC for bronchial complaints, and found in 13 patients a bronchial affection. From reports in the literature it is known that sometimes a bronchial involvement in patients with UC can affect the whole bronchial tree including small bronchi. The involvement of bronchial system in UC is obviously more prominent than previously thought and may fulfil the criteria for a separate syndrome. These relations may have consequences for pathogenetic understanding of UC as well as bronchitis and also consequences for treatment regimes.
Collapse
Affiliation(s)
| | - Peter Barth
- Department of Pathology, Philipps-University of Marburg, Germany
| | | |
Collapse
|
25
|
Papanikolaou I, Kagouridis K, Papiris SA. Patterns of airway involvement in inflammatory bowel diseases. World J Gastrointest Pathophysiol 2014; 5:560-569. [PMID: 25400999 PMCID: PMC4231520 DOI: 10.4291/wjgp.v5.i4.560] [Citation(s) in RCA: 55] [Impact Index Per Article: 5.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 06/07/2014] [Revised: 08/03/2014] [Accepted: 09/10/2014] [Indexed: 02/06/2023] Open
Abstract
Extraintestinal manifestations occur commonly in inflammatory bowel diseases (IBD). Pulmonary manifestations (PM) of IBD may be divided in airway disorders, interstitial lung disorders, serositis, pulmonary vasculitis, necrobiotic nodules, drug-induced lung disease, thromboembolic lung disease and enteropulmonary fistulas. Pulmonary involvement may often be asymptomatic and detected solely on the basis of abnormal screening tests. The common embryonic origin of the intestine and the lungs from the primitive foregut, the co-existence of mucosa associated lymphoid tissue in both organs, autoimmunity, smoking and bacterial translocation from the colon to the lungs may all be involved in the pathogenesis of PM in IBD. PM are mainly detected by pulmonary function tests and high-resolution computed tomography. This review will focus on the involvement of the airways in the context of IBD, especially stenoses of the large airways, tracheobronchitis, bronchiectasis, bronchitis, mucoid impaction, bronchial granulomas, bronchiolitis, bronchiolitis obliterans syndrome and the co-existence of IBD with asthma, chronic obstructive pulmonary disease, sarcoidosis and a1-antitrypsin deficiency.
Collapse
|
26
|
Pulmonary involvement: a rare extraintestinal manifestation of ulcerative colitis. Clin J Gastroenterol 2014; 7:155-8. [PMID: 26183633 DOI: 10.1007/s12328-014-0473-7] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 12/03/2013] [Accepted: 02/22/2014] [Indexed: 10/25/2022]
Abstract
Ulcerative colitis (UC) is associated with a number of extraintestinal manifestations (EIMs) that may affect most organ systems. Among the EIMs, those involving the lung are rare. We report a case of pulmonary involvement and pyoderma gangrenosum in a patient with refractory UC. A chest computed tomography showed multiple nodular infiltrates in bilateral lungs. The patient had no respiratory symptoms. No infectious agents were detected. A transbronchial biopsy specimen showed nonspecific features. Prednisolone was initiated with significant improvement in the patient's abdominal symptoms and pyoderma gangrenosum. Subsequent imaging after steroid therapy showed improvement of the pulmonary infiltrates. The patient's abdominal symptoms relapsed when prednisolone was tapered. The patient subsequently received a proctocolectomy. Chest radiographs have shown resolution of pulmonary infiltrates. Because pulmonary involvement follows an independent course and a proctocolectomy may not be protective against a recurrence of pulmonary involvement, a careful follow-up should be continued.
Collapse
|
27
|
Lu DG, Ji XQ, Liu X, Li HJ, Zhang CQ. Pulmonary manifestations of Crohn’s disease. World J Gastroenterol 2014; 20:133-141. [PMID: 24415866 PMCID: PMC3886002 DOI: 10.3748/wjg.v20.i1.133] [Citation(s) in RCA: 36] [Impact Index Per Article: 3.3] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 10/02/2013] [Revised: 11/09/2013] [Accepted: 12/06/2013] [Indexed: 02/06/2023] Open
Abstract
Crohn’s disease (CD) is a systemic illness with a constellation of extraintestinal manifestations affecting various organs. Of these extraintestinal manifestations of CD, those involving the lung are relatively rare. However, there is a wide array of lung manifestations, ranging from subclinical alterations, airway diseases and lung parenchymal diseases to pleural diseases and drug-related diseases. The most frequent manifestation is bronchial inflammation and suppuration with or without bronchiectasis. Bronchoalveolar lavage findings show an increased percentage of neutrophils. Drug-related pulmonary abnormalities include disorders which are directly induced by sulfasalazine, mesalamine and methotrexate, and opportunistic lung infections due to immunosuppressive treatment. In most patients, the development of pulmonary disease parallels that of intestinal disease activity. Although infrequent, clinicians dealing with CD must be aware of these, sometimes life-threatening, conditions to avoid further impairment of health status and to alleviate patient symptoms by prompt recognition and treatment. The treatment of CD-related respiratory disorders depends on the specific pattern of involvement, and in most patients, steroids are required in the initial management.
Collapse
|
28
|
Stone H, Pye A, Stockley RA. Disease associations in alpha-1-antitrypsin deficiency. Respir Med 2013; 108:338-43. [PMID: 24176989 DOI: 10.1016/j.rmed.2013.10.006] [Citation(s) in RCA: 40] [Impact Index Per Article: 3.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 05/08/2013] [Revised: 10/04/2013] [Accepted: 10/06/2013] [Indexed: 12/17/2022]
Abstract
INTRODUCTION In addition to emphysema alpha-1-antitrypsin deficiency (AATD) has been shown to be associated with several inflammatory conditions, including bronchiectasis, vasculitis, (in particular Wegener's granulomatosis), and panniculitis, suggesting neutrophil proteinases also play a role in their pathophysiology. However, it remains unknown whether other inflammatory diseases are also more prevalent in AATD than the general population. The current study describes the prevalence of other co-morbidities in AATD with particular emphasis on inflammatory bowel disease. METHODS AND RESULTS The case notes of 651 PiZZ or PiZnull patients attending the UK national centre for AATD between 1996 and 2011 were reviewed. The prevalence of inflammatory bowel disease (1.5%) was higher than that predicted in the UK (0.4%). Ten patients had a confirmed diagnosis of ulcerative colitis, and 1 had Crohn's disease. In 2 cases there was a family history of inflammatory bowel disease and all but 1 patient were ex or never smokers. There was also a higher prevalence of hypothyroidism in this patient group than expected for the UK population - 26 cases (7.2% of females and 1.3% of males). CONCLUSIONS The current study of the UK cohort of patients with AATD confirmed a higher prevalence of ulcerative colitis than would be expected in the general population, providing further evidence of a potential link between these 2 conditions. In addition, the data suggested a potential link between hypothyroidism and AATD.
Collapse
Affiliation(s)
- H Stone
- ADAPT Project, Lung Function and Sleep Department, Queen Elizabeth Hospital Birmingham, Mindelsohn Way, Edgbaston, Birmingham B15 2WB, UK.
| | - A Pye
- ADAPT Project, Lung Function and Sleep Department, Queen Elizabeth Hospital Birmingham, Mindelsohn Way, Edgbaston, Birmingham B15 2WB, UK; University of Birmingham, Edgbaston, Birmingham B15 2TT, UK.
| | - R A Stockley
- ADAPT Project, Lung Function and Sleep Department, Queen Elizabeth Hospital Birmingham, Mindelsohn Way, Edgbaston, Birmingham B15 2WB, UK.
| |
Collapse
|
29
|
Trikudanathan G, Venkatesh PGK, Navaneethan U. Diagnosis and therapeutic management of extra-intestinal manifestations of inflammatory bowel disease. Drugs 2013. [PMID: 23181971 DOI: 10.2165/11638120-000000000-00000] [Citation(s) in RCA: 68] [Impact Index Per Article: 5.7] [Reference Citation Analysis] [Abstract] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 12/12/2022]
Abstract
Extra-intestinal manifestations (EIMs) are reported frequently in patients with inflammatory bowel disease (IBD) and may be diagnosed before, concurrently or after the diagnosis of IBD. EIMs in IBD may be classified based on their association with IBD disease activity. The first group has a direct relationship with the activity of the bowel disease and includes pauciarticular arthritis, oral aphthous ulcers, erythema nodosum and episcleritis. The second group of EIMs appears to follow an independent course from the underlying bowel disease activity and include ankylosing spondylitis and uveitis. The third group includes EIMs that may or may not be related to intestinal inflammation, such as pyoderma gangrenosum and probably primary sclerosing cholangitis (PSC). Genetic susceptibility, aberrant self-recognition and immunopathogenic autoantibodies against organ-specific cellular antigens shared by the colon and extra-colonic organs may contribute to the pathogenesis and development of these EIMs. The use of biological agents in the IBD armamentarium has expanded the treatment options for some of the disabling EIMs and these agents form the cornerstone in managing most of the disabling EIMs. PSC is one of the most common hepatobiliary manifestations associated with IBD in which no clear treatment options exist other than endoscopic therapy and liver transplantation. Future research targeting the pathogenesis, early diagnosis and treatment of these EIMs is required.
Collapse
Affiliation(s)
- Guru Trikudanathan
- Department of Internal Medicine, University of Connecticut Medical Center, Farmington, CT, USA
| | | | | |
Collapse
|
30
|
Trikudanathan G, Venkatesh PGK, Navaneethan U. Diagnosis and therapeutic management of extra-intestinal manifestations of inflammatory bowel disease. Drugs 2013. [PMID: 23181971 DOI: 10.165/11638120-000000000-00000] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.1] [Reference Citation Analysis] [Abstract] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 12/12/2022]
Abstract
Extra-intestinal manifestations (EIMs) are reported frequently in patients with inflammatory bowel disease (IBD) and may be diagnosed before, concurrently or after the diagnosis of IBD. EIMs in IBD may be classified based on their association with IBD disease activity. The first group has a direct relationship with the activity of the bowel disease and includes pauciarticular arthritis, oral aphthous ulcers, erythema nodosum and episcleritis. The second group of EIMs appears to follow an independent course from the underlying bowel disease activity and include ankylosing spondylitis and uveitis. The third group includes EIMs that may or may not be related to intestinal inflammation, such as pyoderma gangrenosum and probably primary sclerosing cholangitis (PSC). Genetic susceptibility, aberrant self-recognition and immunopathogenic autoantibodies against organ-specific cellular antigens shared by the colon and extra-colonic organs may contribute to the pathogenesis and development of these EIMs. The use of biological agents in the IBD armamentarium has expanded the treatment options for some of the disabling EIMs and these agents form the cornerstone in managing most of the disabling EIMs. PSC is one of the most common hepatobiliary manifestations associated with IBD in which no clear treatment options exist other than endoscopic therapy and liver transplantation. Future research targeting the pathogenesis, early diagnosis and treatment of these EIMs is required.
Collapse
Affiliation(s)
- Guru Trikudanathan
- Department of Internal Medicine, University of Connecticut Medical Center, Farmington, CT, USA
| | | | | |
Collapse
|
31
|
Lung and intestine: a specific link in an ulcerative colitis rat model. Gastroenterol Res Pract 2013; 2013:124530. [PMID: 23606829 PMCID: PMC3625615 DOI: 10.1155/2013/124530] [Citation(s) in RCA: 16] [Impact Index Per Article: 1.3] [Reference Citation Analysis] [Abstract] [Download PDF] [Figures] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 11/14/2012] [Revised: 03/02/2013] [Accepted: 03/02/2013] [Indexed: 02/07/2023] Open
Abstract
Background. To investigate the link and mechanisms between intestine and lung in the ulcerative colitis (UC) rat model. Materials and Methods. We used the UC rat model by immunological sensitization combined with local 2, 4, 6-trinitrobenzene sulfonic acid (TNBS) in 50% ethanol enema, observed dynamically animal general state and body weight, examined the histological and functional changes in the colon, lung, liver, and kidney tissues, and detected microvascular endothelium response towards inflammation characterized with the expression of iNOS, TXB2, P-selectin, ICAM-1, and vascular endothelial growth factor A (VEGF-A) in the colon and lung tissue. Results. Pulmonary function results suggested ventilator disorder, and pathological findings showed interstitial pneumonia. There were no significant changes in the liver and kidney function and histopathology. The colon and lung tissue iNOS, TXB2, P-selectin, ICAM-1, and VEGF-A expression of the model rats was significantly higher than the normal rats at both time points. Conclusions. Our study is the first to demonstrate the close association between the large intestine and lung in the immune-TNBS-ethanol-induced UC rat model. Different organs and tissues with the same embryonic origin may share the same pathological specificities in a disease. The present study provided a new way of thinking for pathological changes in clinical complex diseases manifested with multiorgan damage.
Collapse
|
32
|
Lu DG, Ji XQ, Zhao Q, Zhang CQ, Li ZF. Tracheobronchial nodules and pulmonary infiltrates in a patient with Crohn's disease. World J Gastroenterol 2012; 18:5653-7. [PMID: 23112563 PMCID: PMC3482657 DOI: 10.3748/wjg.v18.i39.5653] [Citation(s) in RCA: 8] [Impact Index Per Article: 0.6] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 11/21/2011] [Revised: 07/26/2012] [Accepted: 07/29/2012] [Indexed: 02/06/2023] Open
Abstract
Crohn’s disease is a granulomatous systemic disorder of unknown etiology. Obvious pulmonary involvement is exceptional. Tracheal involvement in Crohn’s disease is even more unusual, only a few cases have been reported to date. We herein report a rare case of tracheobronchial nodules and pulmonary infiltrates in both lungs as a complication of Crohn’s disease. A 42-year-old man underwent pancolectomy for multiple broken colon caused by Crohn’s disease. Forty days later pulmonary symptoms and radiologic abnormalities were noted. A search for bacterial (including mycobacteria) and fungal in the repeated sputum proved negative. The treatment consisted of intravenous antimicrobials for one month, but there was no improvement in pyrexia or cough and radiologic abnormalities. Fibreoptic bronchoscopy (FOB) was performed and revealed nodes in the trachea and the right upper lobe opening. Histopathology of tracheobronchial nodules and bronchial mucosa biopsy specimen both showed granulomatous inflammation with proliferation of capillaries and inflammatory cells. Oral steroid and salicylazosulfapyridine were commenced and led to marked improvement in symptoms and an almost complete resolution of his chest radiograph. Repeated FOB showed that nodes in the trachea disappeared and the ones in the right upper lobe opening diminished obviously. Crohn’s disease can be associated with several respiratory manifestations. The form of tracheal and bronchopulmonary involvement in Crohn’s disease is rare and responded well to steroids.
Collapse
|
33
|
Lazebnik LB, Lychkova AE, Mikhailova ZF. Polymorbidity in Inflammatory Bowel Diseases. Bull Exp Biol Med 2012; 153:29-31. [DOI: 10.1007/s10517-012-1635-6] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/24/2022]
|
34
|
Gut G, Sivan Y. Respiratory Involvement in Children with Inflammatory Bowel Disease. PEDIATRIC ALLERGY IMMUNOLOGY AND PULMONOLOGY 2011; 24:197-206. [DOI: 10.1089/ped.2011.0086] [Citation(s) in RCA: 3] [Impact Index Per Article: 0.2] [Reference Citation Analysis] [Track Full Text] [Subscribe] [Scholar Register] [Indexed: 02/06/2023]
Affiliation(s)
- Guy Gut
- Department of Pediatric Pulmonology, Critical Care and Sleep Medicine, Dana Children's Hospital, Tel Aviv Sourasky Medical Center, Sackler Faculty of Medicine, Tel Aviv University, Tel Aviv, Israel
| | - Yakov Sivan
- Department of Pediatric Pulmonology, Critical Care and Sleep Medicine, Dana Children's Hospital, Tel Aviv Sourasky Medical Center, Sackler Faculty of Medicine, Tel Aviv University, Tel Aviv, Israel
| |
Collapse
|
35
|
Respiratory involvement in inflammatory bowel diseases. Multidiscip Respir Med 2010; 5:173-82. [PMID: 22958334 PMCID: PMC3463044 DOI: 10.1186/2049-6958-5-3-173] [Citation(s) in RCA: 19] [Impact Index Per Article: 1.3] [Reference Citation Analysis] [Abstract] [Track Full Text] [Download PDF] [Journal Information] [Subscribe] [Scholar Register] [Received: 03/16/2010] [Accepted: 04/15/2010] [Indexed: 12/21/2022] Open
Abstract
Inflammatory bowel diseases (IBD) include ulcerative colitis (UC) and Crohn's disease (CD) and are due to a dysregulation of the antimicrobial defense normally provided by the intestinal mucosa. This inflammatory process may extend outside the bowel to many organs and also to the respiratory tract. The respiratory involvement in IBD may be completely asymptomatic and detected only at lung function assessment, or it may present as bronchial disease or lung parenchymal alterations. Corticosteroids, both systemic and aerosolized, are the mainstay of the therapeutical approach, while antibiotics must be also administered in the case of infectious and suppurative processes, whose sequels sometimes require surgical intervention. The relatively high incidence of bronchopulmonary complications in IBD suggests the need for a careful investigation of these patients in order to detect a possible respiratory involvement, even when they are asymptomatic.
Collapse
|
36
|
Abstract
Extra-intestinal manifestations occur in at least 25% of Crohn's disease patients. Some extra-intestinal manifestations, such as erythema nodusum and peripheral arthropathy, will wax and wane in keeping with bowel inflammation. The more severe cutaneous ulcerations, uveitis, and axial arthropathy may precede bowel disease or persist after it subsides. Screening may be appropriate for eye disease and for osteoporosis to prevent complications. Medical management for extra-intestinal manifestations is similar to treatment for the bowel symptoms of Crohn's disease, with corticosteroids the mainstay. Pain and depression are associated with inflammatory bowel disease, and their control benefits patients. Recent small studies with anti-tumor necrosis factor (TNF) agents are promising for most extra-intestinal manifestations of Crohn's disease, and may permit more steroid-sparing disease control in the future.
Collapse
Affiliation(s)
- Kimberly Ephgrave
- Department of Surgery, University of Iowa Hospitals and Clinics, 200 Hawkins Drive, Iowa City IA, 52242, USA.
| |
Collapse
|