Advertisement
Mayo Clinic Proceedings Home

Asthma and Proinflammatory Conditions: A Population-Based Retrospective Matched Cohort Study

Published:September 13, 2012DOI:https://doi.org/10.1016/j.mayocp.2012.05.020

      Abstract

      Objective

      To determine the association between asthma and proinflammatory conditions.

      Participants and Methods

      This population-based retrospective matched cohort study enrolled all asthmatic patients among Rochester, Minnesota, residents between January 1, 1964, and December 31, 1983. For each asthmatic patient, 2 age-and sex-matched nonasthmatic individuals were drawn from the same population. The asthmatic and nonasthmatic cohorts were followed forward in the Rochester Epidemiology Project diagnostic index for inflammatory bowel disease (IBD), rheumatoid arthritis (RA), diabetes mellitus (DM), and coronary heart disease (CHD) as outcome events. Data were fitted to Cox proportional hazards models.

      Results

      We identified 2392 asthmatic patients and 4784 nonasthmatic controls. Of the asthmatic patients, 1356 (57%) were male, and mean age at asthma onset was 15.1 years. Incidence rates of IBD, RA, DM, and CHD in nonasthmatic controls were 32.8, 175.9, 132.0, and 389.7 per 100,000 person-years, respectively; those for asthmatic patients were 41.4, 227.9, 282.6, and 563.7 per 100,000 person-years, respectively. Asthma was associated with increased risks of DM (hazard ratio, 2.11; 95% confidence interval, 1.43-3.13; P<.001) and CHD (hazard ratio, 1.47; 95% confidence interval, 1.05-2.06; P=.02) but not with increased risks of IBD or RA.

      Conclusion

      Although asthma is a helper T cell type 2–predominant condition, it may increase the risks of helper T cell type 1–polarized proinflammatory conditions, such as CHD and DM. Physicians who care for asthmatic patients need to address these unrecognized risks in asthmatic patients.

      Abbreviations and Acronyms:

      CHD (coronary heart disease), CI (confidence interval), DM (diabetes mellitus), HR (hazard ratio), IBD (inflammatory bowel disease), ICD (International Classification of Diseases), RA (rheumatoid arthritis), REP (Rochester Epidemiology Project), TH (helper T cell)
      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'

      Subscribe:

      Subscribe to Mayo Clinic Proceedings
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

        • Lethbridge-Cejku M.
        • Vickerie J.
        Summary of Health Statistics for US Adults: National Health Interview Survey, 2003.
        National Center for Health Statistics, Hyattsville, MD2005
        • Centers for Disease Control and Prevention (CDC)
        Forecasted state-specific estimates of self-reported asthma prevalence—United States, 1998.
        MMWR Morb Mortal Wkly Rep. 1998; 47: 1022-1025
        • World Health Organization
        Fact sheet for asthma No. 307.
        (Accessed October 26, 2006)
        • Anandan C.
        • Nurmatov U.
        • van Schayck O.C.P.
        • Sheikh A.
        Is the prevalence of asthma declining? systematic review of epidemiological studies.
        Allergy. 2010; 65: 152-167
        • Centers for Disease Control and Prevention (CDC)
        Vital signs: asthma prevalence, disease characteristics, and self-management education—United States, 2001-2009.
        MMWR Morb Mortal Wkly Rep. 2011; 60: 547-552
        • Barnett S.B.
        • Nurmagambetov T.A.
        Costs of asthma in the United States: 2002-2007.
        J Allergy Clin Immunol. 2011; 127: 145-152
        • de Roos A.J.
        • Cooper G.S.
        • Alavanja M.C.
        • Sandler D.P.
        Personal and family medical history correlates of rheumatoid arthritis.
        Ann Epidemiol. 2008; 18: 433-439
        • Kero J.
        • Gissler M.
        • Hemminki E.
        • Isolauri E.
        Could TH1 and TH2 diseases coexist? evaluation of asthma incidence in children with coeliac disease, type 1 diabetes, or rheumatoid arthritis: a register study.
        J Allergy Clin Immunol. 2001; 108: 781-783
        • Tirosh A.
        • Mandel D.
        • Mimouni F.B.
        • Zimlichman E.
        • Shochat T.
        • Kochba I.
        Autoimmune diseases in asthma.
        Ann Intern Med. 2006; 144: 877-883
        • Bernstein C.N.
        • Wajda A.
        • Blanchard J.F.
        The clustering of other chronic inflammatory diseases in inflammatory bowel disease: a population-based study.
        Gastroenterology. 2005; 129: 827-836
      1. Fenta YA, Tello N, Jung JA, et al. Inflammatory bowel disease and asthma: a population-based, case-control study. Inflamm Bowel Dis. 16(11):1957-1962.

        • Weng X.
        • Liu L.
        • Barcellos L.F.
        • Allison J.E.
        • Herrinton L.J.
        Clustering of inflammatory bowel disease with immune mediated diseases among members of a northern California-managed care organization.
        Am J Gastroenterol. 2007; 102: 1429-1435
        • EURODIAB Substudy 2 Study Group
        Decreased prevalence of atopic diseases in children with diabetes.
        J Pediatr. 2000; 137: 470-474
        • Prosser R.
        • Carleton B.
        • Smith A.
        The comorbidity burden of the treated asthma patient population in British Columbia.
        Chronic Dis Can. 2010; 30: 46-55
        • Adams R.J.
        • Wilson D.H.
        • Taylor A.W.
        • et al.
        Coexistent chronic conditions and asthma quality of life: a population-based study.
        Chest. 2006; 129: 285-291
        • Zhang T.
        • Carleton B.C.
        • Prosser R.J.
        • Smith A.M.
        The added burden of comorbidity in patients with asthma.
        J Asthma. 2009; 46: 1021-1026
        • van Den Broek J.
        • Bachmann M.
        • Kohler G.
        • et al.
        IL-4 and IL-10 antagonize IL-12-mediated protection against acute vaccine in a virus infection with a limited role of IFN-γ and nitric oxide synthetase 2.
        J Immunol. 2000; 164: 371-378
        • Romagnani S.
        The Th1/Th2 paradigm.
        Immunol Today. 1997; 18: 263-266
        • US Census Bureau
        1980 and 1990 Census of Population and Housing.
        US Census Bureau, Washington, DC1983 and 1993
        • Katusic S.K.
        • Colligan R.C.
        • Barbaresi W.J.
        • Schaid D.J.
        • Jacobsen S.J.
        Potential influence of migration bias in birth cohort studies.
        Mayo Clin Proc. 1998; 73: 1053-1061
        • Yunginger J.W.
        • Reed C.E.
        • O'Connell E.J.
        • Melton III, L.J.
        • O'Fallon W.M.
        • Silverstein M.D.
        A community-based study of the epidemiology of asthma: incidence rates, 1964-1983.
        Am Rev Respir Dis. 1992; 146: 888-894
        • Kurland L.T.
        • Molgaard C.A.
        The patient record in epidemiology.
        Sci Am. 1981; 245: 54-63
        • Melton L.
        History of the Rochester Epidemiology Project.
        Mayo Clinic Proc. 1996; 71: 266-274
        • Broder I.
        • Higgins M.W.
        • Mathews K.P.
        • Keller J.B.
        Epidemiology of asthma and allergic rhinitis in a total community, Tecumseh, Michigan, IV: natural history.
        J Allergy Clin Immunol. 1974; 54: 100-110
        • Juhn Y.J.
        • Kita H.
        • Yawn B.P.
        • et al.
        Increased risk of serious pneumococcal disease in patients with asthma.
        J Allergy Clin Immunol. 2008; 122: 719-723
        • Stonnington C.M.
        • Phillips S.F.
        • Melton III, L.J.
        • Zinsmeister A.R.
        Chronic ulcerative colitis: incidence and prevalence in a community.
        Gut. 1987; 28: 402-409
        • Gollop J.H.
        • Phillips S.F.
        • Melton III, L.J.
        • Zinsmeister A.R.
        Epidemiologic aspects of Crohn's disease: a population based study in Olmsted County, Minnesota, 1943-1982.
        Gut. 1988; 29: 49-56
        • Loftus Jr, E.V.
        • Silverstein M.D.
        • Sandborn W.J.
        • Tremaine W.J.
        • Harmsen W.S.
        • Zinsmeister A.R.
        Crohn's disease in Olmsted County, Minnesota, 1940-1993: incidence, prevalence, and survival.
        Gastroenterology. 1998; 114: 1161-1168
        • Loftus C.G.
        • Loftus Jr, E.V.
        • Harmsen W.S.
        • et al.
        Update on the incidence and prevalence of Crohn's disease and ulcerative colitis in Olmsted County, Minnesota, 1940-2000.
        Inflamm Bowel Dis. 2007; 13: 254-261
        • Loftus Jr, E.V.
        • Silverstein M.
        • Sandborn W.
        • Tremaine W.
        • Harmsen W.
        • Zinsmeister A.
        Ulcerative colitis in Olmsted County, Minnesota, 1940-1993: incidence, prevalence, and survival.
        Gut. 2000; 46: 336-343
        • Leibson C.
        • Milton III, L.J.
        • Palumbo P.J.
        Temporal trends in diabetes incidence and prevalence.
        Diabetes Care. 1997; 20: 460-462
        • Dinneen S.F.
        • Maldonado III, D.
        • Leibson C.L.
        • et al.
        Effects of changing diagnostic criteria on the risk of developing diabetes.
        Diabetes Care. 1998; 21: 1408-1413
        • Burke J.P.
        • O'Brien P.
        • Ransom J.
        • et al.
        Impact of case ascertainment on recent trends in diabetes incidence in Rochester, Minnesota.
        Am J Epidemiol. 2002; 155: 859-865
        • Thomas R.J.
        • Palumbo P.J.
        • Melton III, L.J.
        • et al.
        Trends in the mortality burden associated with diabetes mellitus: a population-based study in Rochester, Minn, 1970-1994.
        Arch Intern Med. 2003; 163: 445-451
        • Goraya T.Y.
        • Jacobsen S.J.
        • Kottke T.E.
        • Frye R.L.
        • Weston S.A.
        • Roger V.L.
        Coronary heart disease death and sudden cardiac death: a 20-year population-based study.
        Am J Epidemiol. 2003; 157: 763-770
        • Elveback L.R.
        • Connolly D.C.
        • Kurland L.T.
        Coronary heart disease in residents of Rochester, Minnesota, II: mortality, incidence, and survivorship, 1950-1975.
        Mayo Clin Proc. 1981; 56: 665-672
        • Roger V.L.
        • Jacobsen S.J.
        • Weston S.A.
        • Bailey K.R.
        • Kottke T.E.
        • Frye R.L.
        Trends in heart disease deaths in Olmsted County, Minnesota, 1979-1994.
        Mayo Clin Proc. 1999; 74: 651-657
        • Doran M.F.
        • Pond G.R.
        • Crowson C.S.
        • O'Fallon W.M.
        • Gabriel S.E.
        Trends in incidence and mortality in rheumatoid arthritis in Rochester, Minnesota, over a forty-year period.
        Arthritis Rheum. 2002; 46: 625-631
        • Arnett F.C.
        • Edworthy S.M.
        • Bloch D.A.
        • et al.
        The American Rheumatism Association 1987 revised criteria for the classification of rheumatoid arthritis.
        Arthritis Rheum. 1988; 31: 315-324
        • Gabriel S.E.
        • Crowson C.S.
        • O'Fallon W.M.
        The epidemiology of rheumatoid arthritis in Rochester, Minnesota, 1955-1985.
        Arthritis Rheum. 1999; 42: 415-420
        • Juhn Y.J.
        • Johnson S.K.
        • Hashikawa A.H.
        • et al.
        The potential biases in studying the relationship between asthma and microbial infection.
        J Asthma. 2007; 44: 827-832
        • Frey D.
        • Jacobson R.
        • Poland G.
        • Li X.
        • Juhn Y.
        Assessment of the association between pediatric asthma and Streptococcus pyogenes upper respiratory infection.
        Allergy Asthma Proc. 2009; 30: 540-545
        • Lynch B.A.
        • Fenta Y.
        • Jacobson R.
        • Li X.
        • Juhn Y.J.
        Impact of delay in asthma diagnosis on chest x-ray and antibiotic utilization by clinicians.
        J Asthma. 2012; 49: 23-28
        • Lynch B.A.
        • Van Norman C.A.
        • Jacobson R.A.
        • Weaver A.L.
        • Juhn Y.J.
        Impact of delay in asthma diagnosis on health care service utilization.
        Allergy Asthma Proc. 2010; 31: 48-52
        • Wong C.K.
        • Ho C.Y.
        • Ko F.W.
        • et al.
        Proinflammatory cytokines (IL-17, IL-6, IL-18 and IL-12) and Th cytokines (IFN-γ, IL-4, IL-10 and IL-13) in patients with allergic asthma.
        Clin Exp Immunol. 2001; 125: 177-183
        • Wu T.L.
        • Chang P.Y.
        • Tsao K.C.
        • Sun C.F.
        • Wu L.L.
        • Wu J.T.
        A panel of multiple markers associated with chronic systemic inflammation and the risk of atherogenesis is detectable in asthma and chronic obstructive pulmonary disease.
        J Clin Lab Anal. 2007; 21: 367-371
        • Zhao Y.
        • Yang J.
        • Gao Y.D.
        • Guo W.
        Th17 immunity in patients with allergic asthma.
        Int Arch Allergy Immunol. 2010; 151: 297-307
        • Patterson C.C.
        • Smith A.E.
        • Yarnell J.W.
        • Rumley A.
        • Ben-Shlomo Y.
        • Lowe G.D.
        The associations of interleukin-6 (IL-6) and downstream inflammatory markers with risk of cardiovascular disease: the Caerphilly Study.
        Atherosclerosis. 2010; 209: 551-557
        • Pradhan A.D.
        • Manson J.E.
        • Rifai N.
        • Buring J.E.
        • Ridker P.M.
        C-reactive protein, interleukin 6, and risk of developing type 2 diabetes mellitus.
        JAMA. 2001; 286: 327-334

      Linked Article

      • Should We Consider Asthma as a Risk Factor for Diabetes Mellitus?
        Mayo Clinic ProceedingsVol. 88Issue 2
        • Preview
          We read the recently published article by Yun et al1 with great interest. The authors retrospectively studied 2392 patients with reactive airway disease and 4784 matched controls to investigate the potential association between asthma and various proinflammatory chronic disorders, including diabetes mellitus (DM). The authors found that the retrospective diagnosis of asthma was related to a significantly greater risk of DM compared with controls (unadjusted hazard ratio, 2.11; 95% CI, 1.43-3.13).
        • Full-Text
        • PDF