Allergy Asthma Immunol Res.  2012 May;4(3):122-131. 10.4168/aair.2012.4.3.122.

Influence of Asthma Epidemiology on the Risk for Other Diseases

Affiliations
  • 1Division of Community Pediatric and Adolescent Medicine, Department of Pediatric and Adolescent Medicine and Division of Allergy, Department of Internal Medicine, Mayo Clinic, Rochester, MN, USA. juhn.young@mayo.edu

Abstract

Asthma is a multifactorial chronic disease affecting a significant proportion of people in the United States and worldwide. Numerous laboratory and epidemiological studies have attempted to understand the etiology and underlying mechanisms of asthma and to identify effective therapies. However, the impact of asthma on the risk for other diseases has drawn little attention. This paper discusses the potential effects of asthma as a risk factor for other diseases, explores the potential mechanisms, and reviews the implications of the findings to clinical practice, public health, and research.

Keyword

Asthma; epidemiology; population; chronic diseases; risk; susceptibility

MeSH Terms

Asthma
Chronic Disease
Epidemiologic Studies
Public Health Practice
Risk Factors
United States

Reference

1. Valet RS, Gebretsadik T, Carroll KN, Wu P, Dupont WD, Mitchel EF, Hartert TV. High asthma prevalence and increased morbidity among rural children in a Medicaid cohort. Ann Allergy Asthma Immunol. 2011. 106:467–473.
2. 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.
3. Lethbridge-Çejku M, Vickerie J. Vital Health Stat 10. Summary of health statistics for U.S. adults: National Health Interview Survey, 2003. 2005. National Center for Health Statistics.
4. Asthma. Fact Sheet N°307. World Health Organization (WHO). 2006. Accessed Oct 26. Geneva, Switzerland: WHO;Available from: http://www.who.int/mediacentre/factsheets/fs307/en/index.html.
5. Yunginger JW, Reed CE, O'Connell EJ, Melton LJ 3rd, O'Fallon WM, Silverstein MD. A community-based study of the epidemiology of asthma. Incidence rates, 1964-1983. Am Rev Respir Dis. 1992. 146:888–894.
6. Yawn BP, Wollan P, Kurland M, Scanlon P. A longitudinal study of the prevalence of asthma in a community population of school-age children. J Pediatr. 2002. 140:576–581.
7. Akinbami L. Asthma Prevalence, Health Care Use and Mortality: United States, 2003-05. 2006. Accessed Oct 18 2008. Hyattsville, MD: National Center for Health Statistics;Available from: http://www.cdc.gov/nchs/data/hestat/asthma03-05/asthma03-05.htm.
8. Weiss KB, Gergen PJ, Wagener DK. Breathing better or wheezing worse? The changing epidemiology of asthma morbidity and mortality. Annu Rev Public Health. 1993. 14:491–513.
9. Arrighi HM. US asthma mortality: 1941 to 1989. Ann Allergy Asthma Immunol. 1995. 74:321–326.
10. Anandan C, Nurmatov U, van Schayck OC, Sheikh A. Is the prevalence of asthma declining? Systematic review of epidemiological studies. Allergy. 2010. 65:152–167.
11. Schultz Larsen F, Diepgen T, Svensson A. The occurrence of atopic dermatitis in North Europe: an international questionnaire study. J Am Acad Dermatol. 1996. 34:760–764.
12. Williams HC. Is the prevalence of atopic dermatitis increasing? Clin Exp Dermatol. 1992. 17:385–391.
13. Hanifin JM, Reed ML. Eczema Prevalence and Impact Working Group. A population-based survey of eczema prevalence in the United States. Dermatitis. 2007. 18:82–91.
14. Nathan RA, Meltzer EO, Derebery J, Campbell UB, Stang PE, Corrao MA, Allen G, Stanford R. The prevalence of nasal symptoms attributed to allergies in the United States: findings from the burden of rhinitis in an America survey. Allergy Asthma Proc. 2008. 29:600–608.
15. Gordon B, Blaiss M, Meltzer E, Mahr T, Boyle J. Prevalence of seasonal and perennial allergic rhinitis in children and adults. J Allergy Clin Immunol. 2008. 121:S209.
16. Meltzer EO, Blaiss MS, Derebery MJ, Mahr TA, Gordon BR, Sheth KK, Simmons AL, Wingertzahn MA, Boyle JM. Burden of allergic rhinitis: results from the Pediatric Allergies in America survey. J Allergy Clin Immunol. 2009. 124:S43–S70.
17. Whitney CG, Farley MM, Hadler J, Harrison LH, Bennett NM, Lynfield R, Reingold A, Cieslak PR, Pilishvili T, Jackson D, Facklam RR, Jorgensen JH, Schuchat A. Active Bacterial Core Surveillance of the Emerging Infections Program Network. Decline in invasive pneumococcal disease after the introduction of protein-polysaccharide conjugate vaccine. N Engl J Med. 2003. 348:1737–1746.
18. Huang SS, Platt R, Rifas-Shiman SL, Pelton SI, Goldmann D, Finkelstein JA. Post-PCV7 changes in colonizing pneumococcal serotypes in 16 Massachusetts communities, 2001 and 2004. Pediatrics. 2005. 116:e408–e413.
19. Kaplan SL, Mason EO Jr, Wald ER, Schutze GE, Bradley JS, Tan TQ, Hoffman JA, Givner LB, Yogev R, Barson WJ. Decrease of invasive pneumococcal infections in children among 8 children's hospitals in the United States after the introduction of the 7-valent pneumococcal conjugate vaccine. Pediatrics. 2004. 113:443–449.
20. Weinberger DM, Malley R, Lipsitch M. Serotype replacement in disease after pneumococcal vaccination. Lancet. 2011. 378:1962–1973.
21. Prevention of pneumococcal disease: recommendations of the Advisory Committee on Immunization Practices (ACIP). MMWR Recomm Rep. 1997. 46:1–24.
22. Obaro S, Adegbola R. The pneumococcus: carriage, disease and conjugate vaccines. J Med Microbiol. 2002. 51:98–104.
23. Robinson KA, Baughman W, Rothrock G, Barrett NL, Pass M, Lexau C, Damaske B, Stefonek K, Barnes B, Patterson J, Zell ER, Schuchat A, Whitney CG. Active Bacterial Core Surveillance (ABCs)/Emerging Infections Program Network. Epidemiology of invasive Streptococcus pneumoniae infections in the United States, 1995-1998: Opportunities for prevention in the conjugate vaccine era. JAMA. 2001. 285:1729–1735.
24. Talbot TR, Hartert TV, Mitchel E, Halasa NB, Arbogast PG, Poehling KA, Schaffner W, Craig AS, Griffin MR. Asthma as a risk factor for invasive pneumococcal disease. N Engl J Med. 2005. 352:2082–2090.
25. Juhn YJ, Kita H, Yawn BP, Boyce TG, Yoo KH, McGree ME, Weaver AL, Wollan P, Jacobson RM. Increased risk of serious pneumococcal disease in patients with asthma. J Allergy Clin Immunol. 2008. 122:719–723.
26. Black S. Epidemiology of pertussis. Pediatr Infect Dis J. 1997. 16:S85–S89.
27. Güriş D, Strebel PM, Bardenheier B, Brennan M, Tachdjian R, Finch E, Wharton M, Livengood JR. Changing epidemiology of pertussis in the United States: increasing reported incidence among adolescents and adults, 1990-1996. Clin Infect Dis. 1999. 28:1230–1237.
28. Tanaka M, Vitek CR, Pascual FB, Bisgard KM, Tate JE, Murphy TV. Trends in pertussis among infants in the United States, 1980-1999. JAMA. 2003. 290:2968–2975.
29. Pertussis report. 2010. Sacramento, CA: California Department of Public Health.
30. Bisgard KM, Pascual FB, Ehresmann KR, Miller CA, Cianfrini C, Jennings CE, Rebmann CA, Gabel J, Schauer SL, Lett SM. Infant pertussis: who was the source? Pediatr Infect Dis J. 2004. 23:985–989.
31. Capili CR, Hettinger AS, Ringelman-Hedberg NE, Fink LR, Boyce T, Lahr B, Juhn YJ. Increased risk of pertussis in patients with asthma. J Allergy Clin Immunol. Forthcoming 2011.
32. De Serres G, Shadmani R, Duval B, Boulianne N, Déry P, Douville Fradet M, Rochette L, Halperin SA. Morbidity of pertussis in adolescents and adults. J Infect Dis. 2000. 182:174–179.
33. Kendirli SG, Yilmaz M, Bayram I, Altintas DU, Inal A, Karakoc G. Potential association between allergic diseases and pertussis infection in schoolchildren: results of two cross-sectional studies seven years apart. Allergol Immunopathol (Madr). 2009. 37:21–25.
34. Centers for Disease Control and Prevention (CDC). Update: mumps outbreak - New York and New Jersey, June 2009-January 2010. MMWR Morb Mortal Wkly Rep. 2010. 59:125–129.
35. Dayan GH, Quinlisk MP, Parker AA, Barskey AE, Harris ML, Schwartz JM, Hunt K, Finley CG, Leschinsky DP, O'Keefe AL, Clayton J, Kightlinger LK, Dietle EG, Berg J, Kenyon CL, Goldstein ST, Stokley SK, Redd SB, Rota PA, Rota J, Bi D, Roush SW, Bridges CB, Santibanez TA, Parashar U, Bellini WJ, Seward JF. Recent resurgence of mumps in the United States. N Engl J Med. 2008. 358:1580–1589.
36. Noseworthy ME, Henderson AM, Kanzira P, Ratnam S, Hamed AA. Measles, mumps and mycoplasma antibody profile in children with asthma. Proceedings of American Thoracic Society Annual Meeting. 2005. San Diego, CA.
37. Yoo KH, Agarwal K, Butterfield M, Jacobson RM, Poland GA, Juhn YJ. Assessment of humoral and cell-mediated immune response to measles-mumps-rubella vaccine viruses among patients with asthma. Allergy Asthma Proc. 2010. 31:499–506.
38. Kremer JR, Schneider F, Muller CP. Waning antibodies in measles and rubella vaccinees--a longitudinal study. Vaccine. 2006. 24:2594–2601.
39. Yoo KH, Jacobson R, Poland G, Juhn YJ. The impact of asthma status on durability of measles vaccine response in children. Proceedings of 2011 Annual European Allergy, Asthma and Clinical Immunology. 2011. Istanbul, Turkey.
40. Pandemic (H1N1) 2009 - update 111. Disease Outbreak News. World Health Organization (WHO). 2010. Accessed 2010 Sep 22. Geneva, Switzerland: WHO;Available from: http://www.who.int/csr/don/2010_07_30/en/index.html.
41. 2008-2009 Influenza Season Week 39 ending October 3, 2009. Fluview 2009. Centers for Disease Control and Prevention (CDC). 2010. Accessed 2010 Sep 22. Available from: http://www.cdc.gov/flu/weekly/weeklyarchives2008-2009/weekly39.htm.
42. Eickhoff TC. 2009 pandemic H1N1 influenza: A retrospective. Commentary. 2010. Accessed 2010 Oct 5. Available from: http://www.infectiousdiseasenews.com/article.aspx?id=67575.
43. Jain S, Kamimoto L, Bramley AM, Schmitz AM, Benoit SR, Louie J, Sugerman DE, Druckenmiller JK, Ritger KA, Chugh R, Jasuja S, Deutscher M, Chen S, Walker JD, Duchin JS, Lett S, Soliva S, Wells EV, Swerdlow D, Uyeki TM, Fiore AE, Olsen SJ, Fry AM, Bridges CB, Finelli L. 2009 Pandemic Influenza A (H1N1) Virus Hospitalizations Investigation Team. Hospitalized patients with 2009 H1N1 influenza in the United States, April-June 2009. N Engl J Med. 2009. 361:1935–1944.
44. ANZIC Influenza Investigators. Webb SA, Pettilä V, Seppelt I, Bellomo R, Bailey M, Cooper DJ, Cretikos M, Davies AR, Finfer S, Harrigan PW, Hart GK, Howe B, Iredell JR, McArthur C, Mitchell I, Morrison S, Nichol AD, Paterson DL, Peake S, Richards B, Stephens D, Turner A, Yung M. Critical care services and 2009 H1N1 influenza in Australia and New Zealand. N Engl J Med. 2009. 361:1925–1934.
45. Kloepfer KM, Olenec JP, Lee W, Pappas TE, Liu G, Vrtis RF, Evans MD, Gangnon RE, Gern JE. Increased H1N1 infection rate in asthmatic children. J Allergy Clin Immunol. 2011. 127:AB147.
46. Jung JA, Kita H, Yawn BP, Boyce TG, Yoo KH, McGree ME, Weaver AL, Wollan P, Jacobson RM, Juhn YJ. Increased risk of serious pneumococcal disease in patients with atopic conditions other than asthma. J Allergy Clin Immunol. 2010. 125:217–221.
47. 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.
48. Juhn YJ, Frey D, Jacobson RM, Li X, Poland G. S. pyogenes upper respiratory infection and atopic conditions other than asthma. Prim Care Respir J. Forthcoming 2011.
49. Jung JA, Kita H, Dhillon R, Jacobson RM, Nahm MH, Park M, Tsigrelis C, Juhn YJ. Influence of asthma status on serotype-specific pneumococcal antibody levels. Postgrad Med. 2010. 122:116–124.
50. Marenholz I, Kerscher T, Bauerfeind A, Esparza-Gordillo J, Nickel R, Keil T, Lau S, Rohde K, Wahn U, Lee YA. An interaction between filaggrin mutations and early food sensitization improves the prediction of childhood asthma. J Allergy Clin Immunol. 2009. 123:911–916.
51. Weidinger S, O'Sullivan M, Illig T, Baurecht H, Depner M, Rodriguez E, Ruether A, Klopp N, Vogelberg C, Weiland SK, McLean WH, von Mutius E, Irvine AD, Kabesch M. Filaggrin mutations, atopic eczema, hay fever, and asthma in children. J Allergy Clin Immunol. 2008. 121:1203–1209.e1.
52. Contoli M, Message SD, Laza-Stanca V, Edwards MR, Wark PA, Bartlett NW, Kebadze T, Mallia P, Stanciu LA, Parker HL, Slater L, Lewis-Antes A, Kon OM, Holgate ST, Davies DE, Kotenko SV, Papi A, Johnston SL. Role of deficient type III interferon-lambda production in asthma exacerbations. Nat Med. 2006. 12:1023–1026.
53. Wark PA, Johnston SL, Bucchieri F, Powell R, Puddicombe S, Laza-Stanca V, Holgate ST, Davies DE. Asthmatic bronchial epithelial cells have a deficient innate immune response to infection with rhinovirus. J Exp Med. 2005. 201:937–947.
54. Grove DI, Burston TO, Wellby ML, Ford RM, Forbes IJ. Humoral and cellular immunity in asthma. J Allergy Clin Immunol. 1975. 55:152–163.
55. Grove DI, Reid JG, Forbes IJ. Humoral and cellular immunity in atopic eczema. Br J Dermatol. 1975. 92:611–618.
56. Schneider LC, Weinberg A, Boguniewicz M, Zaccaro D, Taylor P, Coughlin-Borras I, Heughan L, Samuels R, Leung D. Abnormal immune response to varicella vaccine in subjects with atopic dermatitis compared to non-atopic controls. J Allergy Clin Immunol. 2008. 121:S272–S273.
57. Bisgaard H, Hermansen MN, Buchvald F, Loland L, Halkjaer LB, Bønnelykke K, Brasholt M, Heltberg A, Vissing NH, Thorsen SV, Stage M, Pipper CB. Childhood asthma after bacterial colonization of the airway in neonates. N Engl J Med. 2007. 357:1487–1495.
58. Holt PG, Clough JB, Holt BJ, Baron-Hay MJ, Rose AH, Robinson BW, Thomas WR. Genetic 'risk' for atopy is associated with delayed postnatal maturation of T-cell competence. Clin Exp Allergy. 1992. 22:1093–1099.
59. Juhn YJ, Johnson SK, Hashikawa AH, Voigt RG, Campeau LJ, Yawn BP, Williams AR. The potential biases in studying the relationship between asthma and microbial infection. J Asthma. 2007. 44:827–832.
60. Scott K, Johnson SK, Hashikawa AH, Voigt RG, Juhn YJ. The incidence of medical evaluations for acute illnesses in asthmatic and non-asthmatic children. Proceedings of Annual European Academy of Allergy and Clinical Immunology. 2008. Barcelona, Spain.
61. Welch MJ. Inhaled steroids and severe viral infections. J Asthma. 1994. 31:43–50.
62. Patel H, Macarthur C, Johnson D. Recent corticosteroid use and the risk of complicated varicella in otherwise immunocompetent children. Arch Pediatr Adolesc Med. 1996. 150:409–414.
63. Lahood N, Emerson SS, Kumar P, Sorensen RU. Antibody levels and response to pneumococcal vaccine in steroid-dependent asthma. Ann Allergy. 1993. 70:289–294.
64. Lee HJ, Kang JH, Henrichsen J, Konradsen HB, Jang SH, Shin HY, Ahn HS, Choi Y, Hessel L, Nam SW. Immunogenicity and safety of a 23-valent pneumococcal polysaccharide vaccine in healthy children and in children at increased risk of pneumococcal infection. Vaccine. 1995. 13:1533–1538.
65. Spika JS, Halsey NA, Fish AJ, Lum GM, Lauer BA, Schiffman G, Giebink GS. Serum antibody response to pneumococcal vaccine in children with nephrotic syndrome. Pediatrics. 1982. 69:219–223.
66. Hanania NA, Sockrider M, Castro M, Holbrook JT, Tonascia J, Wise R, Atmar RL. American Lung Association Asthma Clinical Research Centers. Immune response to influenza vaccination in children and adults with asthma: effect of corticosteroid therapy. J Allergy Clin Immunol. 2004. 113:717–724.
67. Doull IJ, Lampe FC, Smith S, Schreiber J, Freezer NJ, Holgate ST. Effect of inhaled corticosteroids on episodes of wheezing associated with viral infection in school age children: randomised double blind placebo controlled trial. BMJ. 1997. 315:858–862.
68. Martin RJ, Kraft M, Chu HW, Berns EA, Cassell GH. A link between chronic asthma and chronic infection. J Allergy Clin Immunol. 2001. 107:595–601.
69. Yun H, Knoebel E, Fenta Y, Gabriel SE, Leibson C, Loftus EV Jr, Roger V, Yawn B, Li B, Juhn Y. Asthma and proinflammatory conditions: a population-based retrospective matched cohort study. J Allergy Clin Immunol. 2011. 127:AB79.
70. 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.
71. 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.
72. Adams RJ, Wilson DH, Taylor AW, Daly A, Tursan d'Espaignet E, Dal Grande E, Ruffin RE. Coexistent chronic conditions and asthma quality of life: a population-based study. Chest. 2006. 129:285–291.
73. Zhang T, Carleton BC, Prosser RJ, Smith AM. The added burden of comorbidity in patients with asthma. J Asthma. 2009. 46:1021–1026.
74. Kincy-Cain T, Bost KL. Increased susceptibility of mice to Salmonella infection following in vivo treatment with the substance P antagonist, spantide II. J Immunol. 1996. 157:255–264.
75. Beisswenger C, Kandler K, Hess C, Garn H, Felgentreff K, Wegmann M, Renz H, Vogelmeier C, Bals R. Allergic airway inflammation inhibits pulmonary antibacterial host defense. J Immunol. 2006. 177:1833–1837.
76. van Den Broek M, Bachmann MF, Köhler G, Barner M, Escher R, Zinkernagel R, Kopf M. IL-4 and IL-10 antagonize IL-12-mediated protection against acute vaccinia virus infection with a limited role of IFN-gamma and nitric oxide synthetase 2. J Immunol. 2000. 164:371–378.
77. Fischer JE, Johnson JE, Kuli-Zade RK, Johnson TR, Aung S, Parker RA, Graham BS. Overexpression of interleukin-4 delays virus clearance in mice infected with respiratory syncytial virus. J Virol. 1997. 71:8672–8677.
78. Graham MB, Braciale VL, Braciale TJ. Influenza virus-specific CD4+ T helper type 2 T lymphocytes do not promote recovery from experimental virus infection. J Exp Med. 1994. 180:1273–1282.
79. Moran TM, Isobe H, Fernandez-Sesma A, Schulman JL. Interleukin-4 causes delayed virus clearance in influenza virus-infected mice. J Virol. 1996. 70:5230–5235.
80. Locksley RM, Heinzel FP, Sadick MD, Holaday BJ, Gardner KD Jr. Murine cutaneous leishmaniasis: susceptibility correlates with differential expansion of helper T-cell subsets. Ann Inst Pasteur Immunol. 1987. 138:744–749.
81. Sjölander A, Baldwin TM, Curtis JM, Handman E. Induction of a Th1 immune response and simultaneous lack of activation of a Th2 response are required for generation of immunity to leishmaniasis. J Immunol. 1998. 160:3949–3957.
82. Lohoff M, Gessner A, Bogdan C, Röllinghoff M. The Th1/Th2 paradigm and experimental murine leishmaniasis. Int Arch Allergy Immunol. 1998. 115:191–202.
83. Chaplin DD, Zindl CL, Duffy LB, Atkinson TP, Lai J. Clearance of Mycoplasma pneumoniae is impaired in mice with established allergic airway inflammation. J Allergy Clin Immunol. 2007. 119:S132.
84. Romani L, Mocci S, Bietta C, Lanfaloni L, Puccetti P, Bistoni F. Th1 and Th2 cytokine secretion patterns in murine candidiasis: association of Th1 responses with acquired resistance. Infect Immun. 1991. 59:4647–4654.
85. Juhn YJ, Kita H, Lee LA, Smith RW, Bagniewski SM, Weaver AL, Pankratz VS, Jacobson RM, Poland GA. Childhood asthma and human leukocyte antigen type. Tissue Antigens. 2007. 69:38–46.
86. Hanchard NA, Jacobson RM, Poland GA, Juhn YJ. Refining the role of the HLA DRB1*03 asthma susceptibility locus through linkage disequilibrium and haplotype analysis. Proceedings of 2009 Pediatric Academic Societies' Annual Meeting. 2009. 2009 May 2-5; Baltimore, MD:
87. Rajagopalan G, Tilahun AY, Iijima K, David CS, Kita H, Juhn YJ. HLA-DR polymorphism modulates response to house dust mites in a transgenic mouse model of airway inflammation. Tissue Antigens. 2011. 77:589–592.
88. Lara-Marquez ML, Yunis JJ, Layrisse Z, Ortega F, Carvallo-Gil E, Montagnani S, Makhatadze NJ, Pocino M, Granja C, Yunis E. Immunogenetics of atopic asthma: association of DRB1*1101 DQA1*0501 DQB1*0301 haplotype with Dermatophagoides spp.-sensitive asthma in a sample of the Venezuelan population. Clin Exp Allergy. 1999. 29:60–71.
89. Torío A, Sánchez-Guerrero I, Muro M, Herrero N, Pagán J, Minguela A, Marín L, Moya-Quiles MR, Sanchís MJ, Alvarez-López MR. Analysis of the phenotypic distribution of HLA class I and class II in atopic and non-atopic asthma patients. Eur J Immunogenet. 2000. 27:81–85.
90. Young RP, Dekker JW, Wordsworth BP, Schou C, Pile KD, Matthiesen F, Rosenberg WM, Bell JI, Hopkin JM, Cookson WO. HLA-DR and HLA-DP genotypes and immunoglobulin E responses to common major allergens. Clin Exp Allergy. 1994. 24:431–439.
91. Yssel H, Johnson KE, Schneider PV, Wideman J, Terr A, Kastelein R, De Vries JE. T cell activation-inducing epitopes of the house dust mite allergen Der p I. Proliferation and lymphokine production patterns by Der p I-specific CD4+ T cell clones. J Immunol. 1992. 148:738–745.
92. Li X, Howard TD, Zheng SL, Haselkorn T, Peters SP, Meyers DA, Bleecker ER. Genome-wide association study of asthma identifies RAD50-IL13 and HLA-DR/DQ regions. J Allergy Clin Immunol. 2010. 125:328–335.e11.
93. Poland GA, Ovsyannikova IG, Jacobson RM, Vierkant RA, Jacobsen SJ, Pankratz VS, Schaid DJ. Identification of an association between HLA class II alleles and low antibody levels after measles immunization. Vaccine. 2001. 20:430–438.
94. Alper CA, Kruskall MS, Marcus-Bagley D, Craven DE, Katz AJ, Brink SJ, Dienstag JL, Awdeh Z, Yunis EJ. Genetic prediction of nonresponse to hepatitis B vaccine. N Engl J Med. 1989. 321:708–712.
95. Feehally J, Brenchley PE, Coupes BM, Mallick NP, Morris DM, Short CD. Impaired IgG response to tetanus toxoid in human membranous nephropathy: association with HLA-DR3. Clin Exp Immunol. 1986. 63:376–384.
96. Kinsman OS, McKenna R, Noble WC. Association between histocompatability antigens (HLA) and nasal carriage of Staphylococcus aureus. J Med Microbiol. 1983. 16:215–220.
97. Mangalam AK, Rajagopalan G, Taneja V, David CS. HLA class II transgenic mice mimic human inflammatory diseases. Adv Immunol. 2008. 97:65–147.
98. Deshmukh US, Sim DL, Dai C, Kannapell CJ, Gaskin F, Rajagopalan G, David CS, Fu SM. HLA-DR3 restricted T cell epitope mimicry in induction of autoimmune response to lupus-associated antigen SmD. J Autoimmun. 2011. 37:254–262.
Full Text Links
  • AAIR
Actions
Cited
CITED
export Copy
Close
Share
  • Twitter
  • Facebook
Similar articles
Copyright © 2024 by Korean Association of Medical Journal Editors. All rights reserved.     E-mail: koreamed@kamje.or.kr