{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,18]],"date-time":"2026-09-18T11:05:28Z","timestamp":1789729528131,"version":"4.0.1"},"reference-count":37,"publisher":"Oxford University Press (OUP)","issue":"1","license":[{"start":{"date-parts":[[2007,2,7]],"date-time":"2007-02-07T00:00:00Z","timestamp":1170806400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/academic.oup.com\/journals\/pages\/open_access\/funder_policies\/chorus\/standard_publication_model"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2007,2,7]]},"abstract":"<jats:title>Summary<\/jats:title>\n               <jats:p>Epidemiological data have indicated that some infections are associated with a low risk of allergic diseases, thus supporting the idea (hygiene hypothesis) that the microbial load is an important environmental factor conferring protection against the development of allergies. We set out to test the hygiene hypothesis in a unique epidemiological setting in two socio-economically and culturally markedly different, although genetically related, populations living in geographically adjacent areas. The study cohorts included 266 schoolchildren from the Karelian Republic in Russia and 266 schoolchildren from Finland. The levels of total IgE and allergen-specific IgE for birch, cat and egg albumen were measured. Microbial antibodies were analysed against enteroviruses (coxsackievirus B4), hepatitis A virus, Helicobacter pylori and Toxoplasma gondii. Although total IgE level was higher in Russian Karelian children compared to their Finnish peers, the prevalence of allergen-specific IgE was lower among Russian Karelian children. The prevalence of microbial antibodies was, in turn, significantly more frequent in the Karelian children, reflecting the conspicuous difference in socio-economic background factors. Microbial infections were associated with lower risk of allergic sensitization in Russian Karelian children, enterovirus showing the strongest protective effect in a multivariate model. The present findings support the idea that exposure to certain infections, particularly in childhood, may protect from the development of atopy. Enterovirus infections represent a new candidate to the list of markers of such a protective environment. However, possible causal relationship needs to be confirmed in further studies.<\/jats:p>","DOI":"10.1111\/j.1365-2249.2007.03333.x","type":"journal-article","created":{"date-parts":[[2010,8,12]],"date-time":"2010-08-12T13:57:29Z","timestamp":1281621449000},"page":"47-52","source":"Crossref","is-referenced-by-count":101,"title":["Allergic sensitization and microbial load\u2003\u2013\u2003a comparison between Finland and Russian Karelia"],"prefix":"10.1093","volume":"148","author":[{"name":"The EPIVIR study group","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"T","family":"Seiskari","sequence":"additional","affiliation":[{"name":"Department of Virology, University of Tampere, Finland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"A","family":"Kondrashova","sequence":"additional","affiliation":[{"name":"Department of Virology, University of Tampere, Finland"},{"name":"JDRF Centre for Prevention of Type 1 Diabetes in Finland"},{"name":"Department of Paediatrics, University of Petrozavodsk, Russia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"H","family":"Viskari","sequence":"additional","affiliation":[{"name":"Department of Virology, University of Tampere, Finland"},{"name":"JDRF Centre for Prevention of Type 1 Diabetes in Finland"},{"name":"Department of Clinical Microbiology, Centre for Laboratory Medicine, Pirkanmaa Hospital District, Tampere, Finland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"M","family":"Kaila","sequence":"additional","affiliation":[{"name":"Centre for General Practice, Pirkanmaa Hospital District, Tampere, Finland"},{"name":"Paediatric Research Centre University of Tampere, Finland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"A-M","family":"Haapala","sequence":"additional","affiliation":[{"name":"Department of Clinical Microbiology, Centre for Laboratory Medicine, Pirkanmaa Hospital District, Tampere, Finland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"J","family":"Aittoniemi","sequence":"additional","affiliation":[{"name":"Department of Clinical Microbiology, Centre for Laboratory Medicine, Pirkanmaa Hospital District, Tampere, Finland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"M","family":"Virta","sequence":"additional","affiliation":[{"name":"Department of Microbiology and Immunology, University of Tampere, Finland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"M","family":"Hurme","sequence":"additional","affiliation":[{"name":"Department of Clinical Microbiology, Centre for Laboratory Medicine, Pirkanmaa Hospital District, Tampere, Finland"},{"name":"Department of Microbiology and Immunology, University of Tampere, Finland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"R","family":"Uibo","sequence":"additional","affiliation":[{"name":"Department of Immunology, University of Tartu, Estonia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"M","family":"Knip","sequence":"additional","affiliation":[{"name":"JDRF Centre for Prevention of Type 1 Diabetes in Finland"},{"name":"Hospital for Children and Adolescents, University of Helsinki, Finland"},{"name":"Department of Paediatrics, Tampere University Hospital, Finland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"H","family":"Hy\u00f6ty","sequence":"additional","affiliation":[{"name":"Department of Virology, University of Tampere, Finland"},{"name":"JDRF Centre for Prevention of Type 1 Diabetes in Finland"},{"name":"Department of Clinical Microbiology, Centre for Laboratory Medicine, Pirkanmaa Hospital District, Tampere, Finland"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"286","published-online":{"date-parts":[[2007,2,14]]},"reference":[{"key":"2022010414514613000_b1","doi-asserted-by":"crossref","first-page":"717","DOI":"10.1136\/bmj.315.7110.717","article-title":"Investigation into the increase in hay fever and eczema at age 16 observed between the 1958 and 1970 British birth cohorts","volume":"315","author":"Butland","year":"1997","journal-title":"BMJ"},{"key":"2022010414514613000_b2","doi-asserted-by":"crossref","first-page":"873","DOI":"10.1136\/bmj.304.6831.873","article-title":"Respiratory symptoms and atopy in Aberdeen schoolchildren: evidence from two surveys 25 years apart","volume":"304","author":"Ninan","year":"1992","journal-title":"BMJ"},{"key":"2022010414514613000_b3","doi-asserted-by":"crossref","first-page":"1194","DOI":"10.1034\/j.1398-9995.1999.00180.x","article-title":"Increasing prevalence of allergic rhinitis symptoms in an adult Danish population","volume":"54","author":"Linneberg","year":"1999","journal-title":"Allergy"},{"key":"2022010414514613000_b4","doi-asserted-by":"crossref","first-page":"373","DOI":"10.1046\/j.1365-2222.2002.01330.x","article-title":"Increase of allergen-specific immunoglobulin E antibodies from 1973 to 1994 in a Finnish population and a possible relationship to Helicobacter pylori infections","volume":"32","author":"Kosunen","year":"2002","journal-title":"Clin Exp Allergy"},{"key":"2022010414514613000_b5","doi-asserted-by":"crossref","first-page":"767","DOI":"10.1034\/j.1398-9995.2000.00672.x","article-title":"The prevalence of skin-test-positive allergic rhinitis in Danish adults: two cross-sectional surveys 8 years apart","volume":"55","author":"Linneberg","year":"2000","journal-title":"Allergy"},{"key":"2022010414514613000_b6","doi-asserted-by":"crossref","first-page":"247","DOI":"10.1067\/mai.2000.108312","article-title":"Increasing prevalence of specific IgE to aeroallergens in an adult population: two cross-sectional surveys 8 years apart: the Copenhagen Allergy Study","volume":"106","author":"Linneberg","year":"2000","journal-title":"J Allergy Clin Immunol"},{"key":"2022010414514613000_b7","doi-asserted-by":"crossref","first-page":"125","DOI":"10.1016\/S0091-6749(99)70536-1","article-title":"Worldwide variations in the prevalence of symptoms of atopic eczema in the international study of asthma and allergies in childhood","volume":"103","author":"Williams","year":"1999","journal-title":"J Allergy Clin Immunol"},{"key":"2022010414514613000_b8","doi-asserted-by":"crossref","first-page":"432","DOI":"10.1183\/09031936.98.12020432","article-title":"Prevalence of childhood asthma, rhinitis and eczema in Scandinavia and Eastern Europe","volume":"12","author":"Bjorksten","year":"1998","journal-title":"Eur Respir J"},{"key":"2022010414514613000_b9","doi-asserted-by":"crossref","first-page":"643","DOI":"10.1067\/mai.2002.123307","article-title":"Allergic diseases, skin prick test responses, and IgE levels in North Karelia, Finland, and the Republic of Karelia, Russia","volume":"109","author":"Vartiainen","year":"2002","journal-title":"J Allergy Clin Immunol"},{"key":"2022010414514613000_b10","doi-asserted-by":"crossref","first-page":"886","DOI":"10.1111\/j.1365-2222.1997.tb01228.x","article-title":"Increased prevalence of sensitization against aeroallergens in adults in West compared with East Germany","volume":"27","author":"Nicolai","year":"1997","journal-title":"Clin Exp Allergy"},{"key":"2022010414514613000_b11","doi-asserted-by":"crossref","first-page":"151","DOI":"10.1016\/j.jaci.2005.07.028","article-title":"Growing disparities in atopy between the Finns and the Russians: a comparison of 2 generations","volume":"117","author":"Von Hertzen","year":"2006","journal-title":"J Allergy Clin Immunol"},{"key":"2022010414514613000_b12","doi-asserted-by":"crossref","first-page":"209","DOI":"10.1136\/jech.56.3.209","article-title":"Does a higher number of siblings protect against the development of allergy and asthma? A review","volume":"56","author":"Karmaus","year":"2002","journal-title":"J Epidemiol Commun Health"},{"key":"2022010414514613000_b13","doi-asserted-by":"crossref","first-page":"S2","DOI":"10.1136\/thorax.55.suppl_1.S2","article-title":"Family size, infection and atopy: the first decade of the \u2018hygiene hypothesis\u2019","volume":"55","author":"Strachan","year":"2000","journal-title":"Thorax"},{"key":"2022010414514613000_b14","doi-asserted-by":"crossref","first-page":"194","DOI":"10.1046\/j.1365-2222.2000.00799.x","article-title":"Austrian children living on a farm have less hay fever, asthma and allergic sensitization","volume":"30","author":"Riedler","year":"2000","journal-title":"Clin Exp Allergy"},{"key":"2022010414514613000_b15","doi-asserted-by":"crossref","first-page":"201","DOI":"10.1046\/j.1365-2222.2000.00800.x","article-title":"Farm environment in childhood prevents the development of allergies","volume":"30","author":"Kilpelainen","year":"2000","journal-title":"Clin Exp Allergy"},{"key":"2022010414514613000_b16","doi-asserted-by":"crossref","first-page":"1259","DOI":"10.1136\/bmj.299.6710.1259","article-title":"Hay fever, hygiene, and household size","volume":"299","author":"Strachan","year":"1989","journal-title":"BMJ"},{"key":"2022010414514613000_b17","doi-asserted-by":"crossref","first-page":"138","DOI":"10.1016\/0167-5699(96)80606-2","article-title":"The expanding universe of T-cell subsets: Th1, Th2 and more","volume":"17","author":"Mosmann","year":"1996","journal-title":"Immunol Today"},{"key":"2022010414514613000_b18","doi-asserted-by":"crossref","first-page":"480","DOI":"10.1016\/S0091-6749(03)01869-4","article-title":"Regulatory T cells control the development of allergic disease and asthma","volume":"112","author":"Umetsu","year":"2003","journal-title":"J Allergy Clin Immunol"},{"key":"2022010414514613000_b19","doi-asserted-by":"crossref","first-page":"771","DOI":"10.1016\/S0952-7915(02)00408-9","article-title":"CD4(+) regulatory T cells in autoimmunity and allergy","volume":"14","author":"Curotto de Lafaille","year":"2002","journal-title":"Curr Opin Immunol"},{"key":"2022010414514613000_b20","doi-asserted-by":"crossref","first-page":"576","DOI":"10.1038\/425576a","article-title":"Immunology: hepatitis A virus link to atopic disease","volume":"425","author":"McIntire","year":"2003","journal-title":"Nature"},{"key":"2022010414514613000_b21","doi-asserted-by":"crossref","first-page":"999","DOI":"10.1136\/bmj.314.7086.999","article-title":"Cross sectional retrospective study of prevalence of atopy among Italian military students with antibodies against hepatitis A virus","volume":"314","author":"Matricardi","year":"1997","journal-title":"BMJ"},{"key":"2022010414514613000_b22","doi-asserted-by":"crossref","first-page":"412","DOI":"10.1136\/bmj.320.7232.412","article-title":"Exposure to foodborne and orofecal microbes versus airborne viruses in relation to atopy and allergic asthma: epidemiological study","volume":"320","author":"Matricardi","year":"2000","journal-title":"BMJ"},{"key":"2022010414514613000_b23","doi-asserted-by":"crossref","first-page":"847","DOI":"10.1067\/mai.2003.1335","article-title":"IgG antibodies against microorganisms and atopic disease in Danish adults: the Copenhagen allergy study","volume":"111","author":"Linneberg","year":"2003","journal-title":"J Allergy Clin Immunol"},{"key":"2022010414514613000_b24","doi-asserted-by":"crossref","first-page":"1652","DOI":"10.1001\/jama.284.13.1647","article-title":"Levels of environmental endotoxin and prevalence of atopic disease","volume":"284","author":"Gereda","year":"2000","journal-title":"JAMA"},{"key":"2022010414514613000_b25","doi-asserted-by":"crossref","first-page":"1680","DOI":"10.1016\/S0140-6736(00)02239-X","article-title":"Relation between house-dust endotoxin exposure, type 1 T-cell development, and allergen sensitisation in infants at high risk of asthma","volume":"355","author":"Gereda","year":"2000","journal-title":"Lancet"},{"key":"2022010414514613000_b26","doi-asserted-by":"crossref","first-page":"1230","DOI":"10.1046\/j.1365-2222.2000.00959.x","article-title":"Exposure to endotoxin or other bacterial components might protect against the development of atopy","volume":"30","author":"Von Mutius","year":"2000","journal-title":"Clin Exp Allergy"},{"key":"2022010414514613000_b27","doi-asserted-by":"crossref","first-page":"413","DOI":"10.1097\/00130832-200110000-00006","article-title":"Are infections protecting from atopy?","volume":"1","author":"Matricardi","year":"2001","journal-title":"Curr Opin Allergy Clin Immunol"},{"key":"2022010414514613000_b28","doi-asserted-by":"crossref","first-page":"67","DOI":"10.1080\/07853890410018952","article-title":"A six-fold gradient in the incidence of type 1 diabetes at the eastern border of Finland\u2003\u2212\u2003evidence of a critical role of environment in the disease pathogenesis","volume":"37","author":"Kondrashova","year":"2005","journal-title":"Ann Med"},{"key":"2022010414514613000_b29","doi-asserted-by":"crossref","first-page":"2517","DOI":"10.1056\/NEJMoa021687","article-title":"Prevalence of celiac disease among children in Finland","volume":"348","author":"M\u00e4ki","year":"2003","journal-title":"N Engl J Med"},{"key":"2022010414514613000_b30","doi-asserted-by":"crossref","first-page":"91","DOI":"10.1002\/jmv.10260","article-title":"Enterovirus infections are associated with the induction of beta-cell autoimmunity in a prospective birth cohort study","volume":"69","author":"Salminen","year":"2003","journal-title":"J Med Virol"},{"key":"2022010414514613000_b31","volume-title":"Statistics with confidence","author":"Altman","year":"2000"},{"key":"2022010414514613000_b32","doi-asserted-by":"crossref","first-page":"956","DOI":"10.1183\/09031936.03.00039102","article-title":"Can early infection explain the sibling effect in adult atopy?","volume":"22","author":"Cullinan","year":"2003","journal-title":"Eur Respir J"},{"key":"2022010414514613000_b33","doi-asserted-by":"crossref","first-page":"1223","DOI":"10.1136\/bmj.38069.512245.FE","article-title":"Cohort study of sibling effect, infectious diseases, and risk of atopic dermatitis during first 18 months of life","volume":"328","author":"Benn","year":"2004","journal-title":"BMJ"},{"key":"2022010414514613000_b34","doi-asserted-by":"crossref","first-page":"379","DOI":"10.1136\/thorax.57.5.379","article-title":"Age at childhood infections and risk of atopy","volume":"57","author":"Bager","year":"2002","journal-title":"Thorax"},{"key":"2022010414514613000_b35","doi-asserted-by":"crossref","first-page":"1280","DOI":"10.1007\/s00125-005-1780-9","article-title":"Relationship between the incidence of type 1 diabetes and maternal enterovirus antibodies: time trends and geographical variation","volume":"48","author":"Viskari","year":"2005","journal-title":"Diabetologia"},{"key":"2022010414514613000_b36","doi-asserted-by":"crossref","first-page":"16","DOI":"10.1046\/j.1365-2249.2000.01338.x","article-title":"Atopic eczema is associated with delayed maturation of the antibody response to pneumococcal vaccine","volume":"122","author":"Arkwright","year":"2000","journal-title":"Clin Exp Immunol"},{"key":"2022010414514613000_b37","doi-asserted-by":"crossref","first-page":"465","DOI":"10.1046\/j.1398-9995.2003.00371.x","article-title":"Occurrence of atopy among russian and finnish schoolchildren","volume":"59","author":"Klemola","year":"2004","journal-title":"Allergy"}],"container-title":["Clinical and Experimental Immunology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/api.wiley.com\/onlinelibrary\/tdm\/v1\/articles\/10.1111%2Fj.1365-2249.2007.03333.x","content-type":"unspecified","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/academic.oup.com\/cei\/article-pdf\/148\/1\/47\/42054554\/j.1365-2249.2007.03333.x.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/cei\/article-pdf\/148\/1\/47\/42054554\/j.1365-2249.2007.03333.x.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,1,4]],"date-time":"2022-01-04T14:56:34Z","timestamp":1641308194000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/cei\/article\/148\/1\/47\/6457863"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2007,2,7]]},"references-count":37,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2007,2,14]]},"published-print":{"date-parts":[[2007,2,7]]}},"URL":"https:\/\/doi.org\/10.1111\/j.1365-2249.2007.03333.x","relation":{},"ISSN":["0009-9104","1365-2249"],"issn-type":[{"value":"0009-9104","type":"print"},{"value":"1365-2249","type":"electronic"}],"subject":[],"published-other":{"date-parts":[[2007,4]]},"published":{"date-parts":[[2007,2,7]]}}}