Skip to main content

Advertisement

SpringerLink
Log in

Allergy and brain tumors in the INTERPHONE study: pooled results from Australia, Canada, France, Israel, and New Zealand

  • Original paper
  • Published:
Cancer Causes & Control Aims and scope Submit manuscript

Abstract

Purpose

A history of allergy has been inversely associated with several types of cancer although the evidence is not entirely consistent. We examined the association between allergy history and risk of glioma, meningioma, acoustic neuroma, and parotid gland tumors using data on a large number of cases and controls from five INTERPHONE study countries (Australia, Canada, France, Israel, New Zealand), to better understand potential sources of bias in brain tumor case–control studies and to examine associations between allergy and tumor sites where few studies exist.

Methods

A total of 793 glioma, 832 meningioma, 394 acoustic neuroma, and 84 parotid gland tumor cases were analyzed with 2,520 controls recruited during 2000–2004. Conditional logistic regression models were used to obtain odds ratios (ORs) and 95 % confidence intervals (CIs) for associations between self-reported allergy and tumor risk.

Results

A significant inverse association was observed between a history of any allergy and glioma (OR = 0.73, 95 % CI 0.60–0.88), meningioma (OR = 0.77, 95 % CI 0.63–0.93), and acoustic neuroma (OR = 0.64, 95 % CI 0.49–0.83). Inverse associations were also observed with specific allergic conditions. However, inverse associations with asthma and hay fever strengthened with increasing age of allergy onset and weakened with longer time since onset. No overall association was observed for parotid gland tumors (OR = 1.21, 95 % CI 0.73–2.02).

Conclusions

While allergy history might influence glioma, meningioma, and acoustic neuroma risk, the observed associations could be due to information or selection bias or reverse causality.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Turner MC (2012) Epidemiology: allergy history, IgE and cancer. Cancer Immunol Immunother 61:1493–1510

    Article  PubMed  CAS  Google Scholar 

  2. Linos E, Raine T, Alosno A, Michaud D (2007) Atopy and risk of brain tumors: a meta-analysis. J Natl Cancer Inst 99:1544–1550

    Article  PubMed  Google Scholar 

  3. Berg-Beckhoff G, Schuz J, Blettner M, Munster E, Schlaefer K, Wahrendorf J, Schlehofer B (2009) History of allergic disease and epilepsy and risk of glioma and meningioma (INTERPHONE study group, Germany). Eur J Epidemiol 24:433–440

    Article  PubMed  Google Scholar 

  4. Schlehofer B, Schlaefer K, Blettner M, Berg G, Bohler E, Hettinger I, Kunna-Grass K, Wahrendorf J, Schuz J, Interphone Study Group (2007) Environmental risk factors for sporadic acoustic neuroma (Interphone Study Group, Germany). Eur J Cancer 43:1741–1747

    Article  PubMed  CAS  Google Scholar 

  5. Schoemaker MJ, Swerdlow AJ, Hepworth SJ, McKinney PA, van Tongeren M, Muir KR (2006) History of allergies and risk of glioma in adults. Int J Cancer 119:2165–2172

    Article  PubMed  CAS  Google Scholar 

  6. Schoemaker MJ, Swerdlow AJ, Hepworth SJ, van Tongeren M, Muir KR, McKinney PA (2007) History of allergic disease and risk of meningioma. Am J Epidemiol 165:477–485

    Article  PubMed  CAS  Google Scholar 

  7. Wigertz A, Lonn S, Schwartzbaum J, Hall P, Auvinen A, Christensen HC, Johansen C, Klaeboe L, Salminen T, Schoemaker MJ, Swerdlow AJ, Tynes T, Feychting M (2007) Allergic conditions and brain tumor risk. Am J Epidemiol 166:941–950

    Article  PubMed  Google Scholar 

  8. Schoemaker MJ, Swerdlow AJ, Auvinen A, Christensen HC, Feychting M, Johansen C, Klaeboe L, Lonn S, Salminen T, Tynes T (2006) Medical history, cigarette smoking and risk of acoustic neuroma: an international case–control study. Int J Cancer 120:103–110

    Article  Google Scholar 

  9. Jensen-Jarolim E, Achatz G, Turner MC, Karagiannis S, Legrand F, Capron M, Penichet ML, Rodriguez JA, Siccardi AG, Vangelista L, Riemer AB, Gould H (2008) AllergoOncology: the role of IgE-mediated allergy in cancer. Allergy 63:1255–1266

    Article  PubMed  CAS  Google Scholar 

  10. Schwartzbaum J, Jonsson F, Ahlbom A, Preston-Martin S, Lonn S, Soderberg KC, Feychting M (2003) Cohort studies of association between self-reported allergic conditions, immune-related diagnoses and glioma and meningioma risk. Int J Cancer 106:423–428

    Article  PubMed  CAS  Google Scholar 

  11. Turner MC, Chen Y, Krewski D, Ghadirian P, Thun MJ, Calle EE (2005) Cancer mortality among US men and women with asthma and hay fever. Am J Epidemiol 162:212–221

    Article  PubMed  Google Scholar 

  12. Cardis E, Richardson L, Deltour I, Armstrong B, Feychting M, Johansen C, Kilkenny M, McKinney P, Modan B, Sadetzki S, Schuz J, Swerdlow A, Vrijheid M, Auvinen A, Berg G, Blettner M, Bowman J, Brown J, Chetrit A, Christensen HC, Cook A, Hepworth S, Giles G, Hours M, Iavarone I, Jarus-Hakak A, Klaeboe L, Krewski D, Lagorio S, Lonn S et al (2007) The INTERPHONE study: design, epidemiological methods, and description of the study population. Eur J Epidemiol 22:647–664

    Article  PubMed  Google Scholar 

  13. Cardis E, Armstrong BK, Bowman JD, Giles GG, Hours M, Krewski D, McBride M, Parent ME, Sadetzki S, Woodward A, Brown J, Chetrit A, Figuerola J, Hoffmann C, Jarus-Hakak A, Montestruq L, Nadon L, Richardson L, Villegas R, Virjheid M (2011) Risk of brain tumours in relation to estimated RF dose from mobile phones: results from five Interphone countries. Occup Environ Med 68:631–640

    Article  PubMed  CAS  Google Scholar 

  14. SAS Institute, Inc (2008) SAS, version 9.2. SAS Institute, Inc., Cary

  15. Schlehofer B, Blettner M, Preston-Martin S, Niehoff D, Wahrendorf J, Arslan A, Ahlbom A, Choi WN, Giles GG, Howe GR, Little J, Menegoz F, Ryan P (1999) Role of medical history in brain tumor development. Results from the International Adult Brain Tumor Study. Int J Cancer 82:155–160

    Article  PubMed  CAS  Google Scholar 

  16. McCarthy BJ, Rankin K, Il’yasova D, Erdal S, Vick N, Ali-Osman F, Bigner DD, Davis F (2011) Assessment of type of allergy and antihistamine use in the development of glioma. Cancer Epidemiol Biomarkers Prev 20:370–378

    Article  PubMed  Google Scholar 

  17. Brenner AV, Linet MS, Fine HA, Shapiro WR, Selker RG, Black PM, Inskip PD (2002) History of allergies and autoimmune diseases and risk of brain tumors in adults. Int J Cancer 99:252–259

    Article  PubMed  CAS  Google Scholar 

  18. Wiemels JL, Wiencke JK, Patoka J, Moghadassi M, Chew T, McMillan A, Miike R, Barger G, Wrensch M (2004) Reduced immunoglobulin E and allergy among adults with glioma compared with controls. Cancer Res 64:8468–8473

    Article  PubMed  CAS  Google Scholar 

  19. Schwartzbaum JA, Huang K, Lawler S, Ding B, Yu J, Chiocca EA (2010) Allergy and inflammatory transcriptome is predominantly negatively correlated with CD133 expression in glioblastoma. Neuro Oncol 12:320–327

    Article  PubMed  CAS  Google Scholar 

  20. Avril T, Vauleon E, Tanguy-Royer S, Mosser J, Quillien V (2011) Mechanisms of immunomodulation in human glioblastoma. Immunotherapy 3(4 Suppl):42–44

    Article  PubMed  Google Scholar 

  21. Anto JM, Pinart M, Akdis M, Auffray C, Bachert C, Basagana X, Carlsen KH, Guerra S, von Hertzen L, Illi S, Kauffmann F, Keil T, Kiley JP, Koppelman GH, Lupinek C, Martinez FD, Nawijn MC, Postma DS, Siroux V, Smit HA, Sterk PJ, Sunyer J, Valenta R, Valverde S, Akdis CA, Annesi-Maesano I, Ballester F, Benet M, Cambon-Thomsen A, Chatzi L et al (2012) Understanding the complexity of IgE-related phenotypes from childhood to young adulthood: a mechanisms of the development of allergy (MeDALL) seminar. J Allergy Clin Immunol 129:943–954

    Article  PubMed  Google Scholar 

  22. Novak N, Bieber T (2003) Allergic and nonallergic forms of atopic diseases. J Allergy Clin Immunol 112:252–262

    Article  PubMed  Google Scholar 

  23. Il’yasova D, McCarthy B, Marcello J, Schildkraut JM, Moorman PG, Krishnamachari B, Ali-Osman F, Bigner DD, Davis F (2009) Association between glioma and history of allergies, asthma, and eczema: a case–control study with three groups of controls. Cancer Epidemiol Biomarkers Prev 18:1232–1238

    Article  PubMed  Google Scholar 

  24. Wiemels JL, Wrensch M, Sison JD, Zhou M, Bondy M, Calvocoressi L, Black PM, Yu H, Schildkraut JM, Claus EB (2011) Reduced allergy and immunoglobulin E among adults with intracranial meningioma compared to controls. Int J Cancer 129:1932–1939

    Article  PubMed  CAS  Google Scholar 

  25. Wiemels JL, Wilson D, Patil C, Patoka J, McCoy L, Rice T, Schwartzbaum J, Heimberger A, Samson JH, Chang S, Prados M, Wiencke JK, Wrensch M (2009) IgE, allergy, and risk of glioma: update from the San Francisco Bay Area Adult Glioma Study in the Temozolomide era. Int J Cancer 125:680–687

    Article  PubMed  CAS  Google Scholar 

  26. Calboli FC, Cox DG, Buring JE, Gaziano JM, Ma J, Stampfer M, Willett WC, Tworoger SS, Hunter DJ, Camargo CA Jr, Michaud DS (2011) Prediagnostic plasma IgE levels and risk of adult glioma in four prospective cohort studies. J Natl Cancer Inst 103:1588–1595

    Article  PubMed  CAS  Google Scholar 

  27. Schlehofer B, Siegmund B, Linseisen J, Schuz J, Rohrmann S, Becker S, Michaud D, Melin B, Bas Bueno-de-Mesquita H, Peeters PH, Vineis P, Tjonneland A, Olsen A, Overvad K, Romieu I, Boeing H, Aleksandrova K, Trichopoulou A, Bamia C, Lagiou P, Sacerdote C, Palli D, Panico S, Sieri S, Tumino R, Sanchez MJ, Rodriguez L, Dorronsoro M, Duell EJ, Chirlaque MD et al (2011) Primary brain tumours and specific serum immunoglobulin E: a case–control study nested in the European prospective investigation into cancer and nutrition cohort. Allergy 66:1434–1441

    Article  PubMed  CAS  Google Scholar 

  28. Schwartzbaum J, Ding B, Johannesen TB, Osnes LTN, Karavodin L, Ahlbom A, Feychting M, Grimsrud TK (2012) Association between prediagnostic IgE levels and risk of glioma. J Natl Cancer Inst 104:1251–1259

    Article  PubMed  CAS  Google Scholar 

  29. Carosso A, Bugiani M, Migliore E, Anto JM, DeMarco R (2007) Reference values of total serum IgE and their significance in the diagnosis of allergy in young European adults. Int Arch Allergy Immunol 142:230–238

    Article  PubMed  CAS  Google Scholar 

  30. Hoppin JA, Jaramillo R, Salo P, Sandler DP, London SJ, Zeldin DC (2011) Questionnaire predictors of atopy in a US population sample: findings from the National Health and Nutrition Examination Survey, 2005–2006. Am J Epidemiol 173:544–552

    Article  PubMed  Google Scholar 

  31. Zhou M, Wiemels JL, Bracci PM, Wrensch MR, McCoy LS, Rice T, Sison JD, Patoka JS, Wiencke JK (2010) Circulating levels of the innate and humoral immune regulators CD14 and CD23 are associated with adult glioma. Cancer Res 70:7534–7542

    Article  PubMed  CAS  Google Scholar 

  32. Dobbins SE, Hosking FJ, Shete S, Armstrong G, Swerdlow A, Liu Y, Yu R, Lau C, Schoemaker MJ, Hepworth SJ, Miur K, Bondy M, Houlston RS (2011) Allergy and glioma risk: test of association by genotype. Int J Cancer 128:1736–1740

    Article  PubMed  CAS  Google Scholar 

  33. Lachance DH, Yang P, Johnson DR, Decker PA, Kollmeyer TM, McCoy LS, Rice T, Xiao Y, Ali-Osman F, Wang F, Stoddard SM, Sprau DJ, Kosel ML, Wiencke JK, Wiemels JL, Patoka JS, Davis F, McCarthy B, Rynearson AL, Worra JB, Fridley BL, O’Neill BP, Buckner JC, Il’yasova D, Jenkins RB, Wrensch MR (2011) Associations of high-grade glioma with glioma risk alleles and histories of allergy and smoking. Am J Epidemiol 174:574–581

    Article  PubMed  Google Scholar 

  34. Ruan Z, Zhao Y, Yan L, Chen H, Fan W, Chen J, Wu Q, Qian J, Zhang T, Zhou K, Mao Y, Zhou L, Huang Y, Lu D (2011) Single nucleotide polymorphisms in Il-4Ra, IL-13 and STAT6 genes occurs in brain glioma. Front Biosci (Elite Ed) 3:33–45

    Article  Google Scholar 

  35. Schoemaker MJ, Robertson L, Wigertz A, Jones ME, Hosking FJ, Feychting M, Lonn S, McKinney PA, Hepworth SJ, Muir KR, Auvinen A, Slaminen T, Kiuru A, Johansen C, Houlston RS, Swerdlow AJ (2010) Interaction between 5 genetic variants and allergy in glioma risk. Am J Epidemiol 171:1165–1173

    Article  PubMed  Google Scholar 

  36. Schwartzbaum J, Ahlbom A, Malmer B, Lonn S, Brookes AJ, Doss H, Debinski W, Henriksson R, Feychting M (2005) Polymorphisms associated with asthma are inversely related to glioblastoma multiforme. Cancer Res 65:6459–6465

    Article  PubMed  CAS  Google Scholar 

  37. Schwartzbaum JA, Ahlbom A, Lonn S, Malmer B, Wigertz A, Auvinen A, Brookes AJ, Collatz CH, Henriksson R, Johansen C, Salminen T, Schoemaker MJ, Swerdlow AJ, Debinski W, Feychting M (2007) An international case–control study of interleukin-4Ra, interleukin-13, and cyclooxygenase-2 polymorphisms and glioblastoma risk. Cancer Epidemiol Biomarkers Prev 16:2448–2454

    Article  PubMed  CAS  Google Scholar 

  38. Wiemels JL, Wiencke JK, Kelsey KT, Moghadassi M, Rice T, Urayama KY, Miike R, Wrensch M (2007) Allergy-related polymorphisms influence glioma status and serum IgE levels. Cancer Epidemiol Biomarkers Prev 16:1229–1235

    Article  PubMed  CAS  Google Scholar 

  39. Linabery AM, Jurek AM, Duval S, Ross JA (2010) The association between atopy and childhood/adolescent leukemia: a meta-analysis. Am J Epidemiol 171:749–764

    Article  PubMed  Google Scholar 

  40. Scheurer ME, El-Zein R, Thompson PA, Aldape KD, Levin VA, Gilbert MR, Weinberg JS, Bondy ML (2008) Long-term anti-inflammatory and antihistamine medication use and adult glioma risk. Cancer Epidemiol Biomarkers Prev 17:1277–1281

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

Funding for the INTERPHONE Study was provided by the European Fifth Framework Program, ‘Quality of Life and Management of Living Resources’ (contract QLK4-CT-1999901563), the International Union against Cancer (UICC). The UICC received funds for this purpose from the Mobile Manufacturers’ Forum and GSM Association. Provision of funds to the INTERPHONE Study investigators via the UICC was governed by agreements that guaranteed INTERPHONE’s complete scientific independence. The terms of these agreements are publicly available at http://www.iarc.fr/en/research-groups/RAD/RCAd.html. The Australian center was supported by the National Health and Medical Research Council (EME grant 219129); BKA was supported by a University of Sydney Medical Foundation Program Grant. The Cancer Council NSW and the Cancer Council Victoria provided most of the infrastructure for the project in Australia. The Canada-Montreal data collection was funded by a grant from the Canadian Institutes of Health Research (CIHR) (project MOP-42525). Additionally, JS’s research team was partly funded by the Canada Research Chair programme and by the Guzzo-CRS Chair in Environment and Cancer. The other Canadian centers were supported by a university-industry partnership grant from the CIHR, the latter including partial support from the Canadian Wireless Telecommunications Association. The CIHR university-industry partnerships program also includes provisions that ensure complete scientific independence of the investigators. DK is the Natural Sciences and Engineering Research Council (NSERC) Chair in Risk Science at the University of Ottawa. Additional funding for the study in France was provided by l’Association pour la Recherche sur le Cancer (ARC) (contract 5142) and three network operators (Orange, SFR, Bouygues Telecom). The funds provided by the operators represented 5 % of the total cost of the French study and were governed by contracts guaranteeing the complete scientific independence of the investigators. In New Zealand, funding was provided by the Health Research Council, Hawkes Bay Medical Research Foundation and the Cancer Society of New Zealand. The authors would like to acknowledge Jordi Figuerola (CREAL) for programming and database management support. The Australian team would like to acknowledge the overall support given to study design and implementation by Michael Besser and Andrew Kaye; and to thank fieldwork staff in Melbourne—Monique Kilkenny, Georgina Marr, Tracey McPhail, Fiona Phillips, Hayley Shaw, Yvonne Torn-Broers; and Sydney—Matthew Carroll, Sally Dunlop, Virginia MacDonald and Elizabeth Willows—the many interviewers for their hard work, and the NSW and Victorian Cancer Registries for aiding case identification. We also thank Angus Cook (University of Western Australia) and Neil Pearce (London School of Hygiene and Tropical Medicine) who, together with Alistair Woodward, were responsible for the conduct of the INTERPHONE Study in New Zealand. The Canada-Ottawa center gratefully acknowledges the work of Lynn Pratt and Daniel Bedard for their leading roles in study coordination. The Canada-Montreal team acknowledges Louise Nadon and the diligent work of fieldwork staff including Marie-Claire Goulet, Sylvie Plante, Sally Campbell, and the interviewer team. The following hospitals and physicians in Montreal permitted access to their patients: CHUM Hopital Notre-Dame (Dr Wieslaw Michel Bojanowski, Dr Jean Jacques Dufour, Dr Francois Lavigne, Dr Robert A Moumdjian); Neurological Institute of Montreal (Dr Rolando Del Maestro, Dr Richard Leblanc); Hopital du Sacre-Coeur de Montreal (Dr Marc F Giroux); The Jewish General Hospital (Dr Gerard Mohr, Dr Jamie Miles Rappaport). The Canada-Vancouver center wishes to acknowledge the work carried out by Dr Alison Pope, Patricia Nelson, Nelson Ha, Dr Kaushik Bhagat and the interviewer team. The French team to thank the French fieldwork team, Mary-Pierre Herrscher, Fatima Lamri, Agnes Boidart, Helene Gire, Juliette Krassilchik, Judith Lenti, Delphine Maillac, Frederique Sonnet, Flore Taguiev, Julie Frantz, France Castay, Florian Gay, for their excellent work. The Israeli team acknowledges the diligent work of the fieldwork and office staff including Etti Aviezer, Tehila Ben-Tal, Meirav Dolev, Yonit Deutch, Tamara Rodkin, Ahuva Zultan and the interviewer team.

Conflict of interest

The authors have no conflict of interest to declare.

Author information

Authors and Affiliations

  1. McLaughlin Centre for Population Health Risk Assessment, Institute of Population Health, University of Ottawa, One Stewart Street, Room 313, Ottawa, ON, K1N 6N5, Canada

    Michelle C. Turner & Daniel Krewski

  2. Centre for Research in Environmental Epidemiology (CREAL), Barcelona, Spain

    Michelle C. Turner & Elisabeth Cardis

  3. CIBER Epidemiología y Salud Pública (CIBERESP), Barcelona, Spain

    Michelle C. Turner & Elisabeth Cardis

  4. Department of Epidemiology and Community Medicine, Faculty of Medicine, University of Ottawa, Ottawa, Canada

    Daniel Krewski

  5. Risk Sciences International, Ottawa, Canada

    Daniel Krewski

  6. Sydney School of Public Health, The University of Sydney, Sydney, Australia

    Bruce K. Armstrong

  7. Cancer and Radiation Epidemiology Unit, The Gertner Institute for Epidemiology and Health Policy Research, Chaim Sheba Medical Centre, Tel-Hashomer, Israel

    Angela Chetrit & Siegal Sadetzki

  8. Cancer Epidemiology Centre, Cancer Council Victoria, Melbourne, Australia

    Graham G. Giles

  9. Centre for MEGA Epidemiology, School of Population Health, The University of Melbourne, Melbourne, Australia

    Graham G. Giles

  10. Unité Mixte de Recherche Epidémiologique Transport Travail Environnement IFSTTAR, UCBL, Université Lyon 1 IFSTTAR, 69373, Lyon, France

    Martine Hours

  11. Cancer Control Research, British Columbia Cancer Agency, Vancouver, Canada

    Mary L. McBride

  12. INRS-Institut Armand-Frappier, Université du Québec, Laval, Canada

    Marie-Élise Parent

  13. Sackler School of Medicine, Tel-Aviv University, Tel-Aviv, Israel

    Siegal Sadetzki

  14. CRCHUM, University of Montreal, Montreal, Canada

    Jack Siemiatycki

  15. School of Population Health, University of Auckland, Auckland, New Zealand

    Alistair Woodward

Authors
  1. Michelle C. Turner
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Daniel Krewski
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Bruce K. Armstrong
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Angela Chetrit
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Graham G. Giles
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Martine Hours
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Mary L. McBride
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Marie-Élise Parent
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Siegal Sadetzki
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Jack Siemiatycki
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Alistair Woodward
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Elisabeth Cardis
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Michelle C. Turner.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Turner, M.C., Krewski, D., Armstrong, B.K. et al. Allergy and brain tumors in the INTERPHONE study: pooled results from Australia, Canada, France, Israel, and New Zealand. Cancer Causes Control 24, 949–960 (2013). https://doi.org/10.1007/s10552-013-0171-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10552-013-0171-7

Keywords

Search

Navigation