Skip to main content
PMC home page
Thorax logoLink to Thorax
. 2001 Apr;56(4):290–295. doi: 10.1136/thorax.56.4.290

Prenatal risk factors of wheezing at the age of four years in Tanzania

J Sunyer 1, C Mendendez 1, P Ventura 1, J Aponte 1, D Schellenberg 1, E Kahigwa 1, C Acosta 1, J Anto 1, P Alonso 1
PMCID: PMC1746018  PMID: 11254820

Abstract

BACKGROUND—A study was undertaken to assess the interactions between prenatal exposures, early life infections, atopic predisposition, and allergen exposures in the development of wheezing up to the age of 4 years in a tropical region of Africa.
METHODS—The study subjects comprised children born at the district hospital in Ifakara, Tanzania during a 1 year period who were participating in a trial of iron supplementation and malaria chemoprophylaxis during the first year of life and followed for up to 4 years. From this group of subjects, 658 (79%) participated in the interview at 18 months and 528 (64%) in a second interview at 4 years. Wheezing was measured with the ISAAC questionnaire. A hospital based inpatient and outpatient surveillance system was set up to document all attendance by study children for any cause, including episodes of clinical malaria and lower respiratory tract infections. Total IgE levels and malaria parasites were measured in maternal and cord blood. Total IgE was also measured at 18 months of age. Indoor environmental levels of Der p I and Fel d I were determined using an enzyme linked immunosorbent assay at the same time as the interview at the age of 18months.
RESULTS—The prevalence of wheezing at 4 years is common in Ifakara (14%, range 13-15%). The presence of malaria parasites in cord blood (odds ratio, OR = 6.84, 95% CI 1.84 to 24.0) and maternal asthma (OR = 8.47, 95% CI 2.72 to 26.2) were positively associated with wheezing at the age of 4 years, and cord blood total IgE was negatively associated (OR = 0.24, 95% CI 0.07 to 0.85) (all p<0.05). Parasitaemia at birth was not related to total IgE levels in cord blood (p=0.6). Clinical episodes of malaria during infancy were not associated with wheezing, and nor were levels of indoor aeroallergens.
CONCLUSION—These findings suggest that events occurring during pregnancy may play a role in the future appearance of wheezing, although the results must be interpreted with caution because of the small numbers studied.



Full Text

The Full Text of this article is available as a PDF (112.4 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Anderson H. R. The epidemiological and allergic features of asthma in the New Guinea Highlands. Clin Allergy. 1974 Jun;4(2):171–183. doi: 10.1111/j.1365-2222.1974.tb01374.x. [DOI] [PubMed] [Google Scholar]
  2. Atkinson W., Harris J., Mills P., Moffat S., White C., Lynch O., Jones M., Cullinan P., Newman Taylor A. J. Domestic aeroallergen exposures among infants in an English town. Eur Respir J. 1999 Mar;13(3):583–589. doi: 10.1183/09031936.99.13358599. [DOI] [PubMed] [Google Scholar]
  3. Bodner C., Godden D., Seaton A. Family size, childhood infections and atopic diseases. The Aberdeen WHEASE Group. Thorax. 1998 Jan;53(1):28–32. doi: 10.1136/thx.53.1.28. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Burney P. G., Luczynska C., Chinn S., Jarvis D. The European Community Respiratory Health Survey. Eur Respir J. 1994 May;7(5):954–960. doi: 10.1183/09031936.94.07050954. [DOI] [PubMed] [Google Scholar]
  5. Carswell F., Meakins R. H., Harland P. S. Parasites and asthma in Tanzanian children. Lancet. 1976 Oct 2;2(7988):706–707. doi: 10.1016/s0140-6736(76)90004-0. [DOI] [PubMed] [Google Scholar]
  6. Everard M. L. What link between early respiratory viral infections and atopic asthma? Lancet. 1999 Aug 14;354(9178):527–528. doi: 10.1016/S0140-6736(99)00159-2. [DOI] [PubMed] [Google Scholar]
  7. Experimental and clinical-therapeutic features of asthma. Proceedings from the international meeting in Naples, Italy. June 7-8, 1999. Allergy. 2000;55 (Suppl 61):1–66. [PubMed] [Google Scholar]
  8. Farooqi I. S., Hopkin J. M. Early childhood infection and atopic disorder. Thorax. 1998 Nov;53(11):927–932. doi: 10.1136/thx.53.11.927. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Flynn M. G. Respiratory symptoms, bronchial responsiveness, and atopy in Fijian and Indian children. Am J Respir Crit Care Med. 1994 Aug;150(2):415–420. doi: 10.1164/ajrccm.150.2.8049824. [DOI] [PubMed] [Google Scholar]
  10. Godfrey R. C., Gradidge C. F. Allergic sensitisation of human lung fragments prevented by saturation of IgE binding sites. Nature. 1976 Feb 12;259(5543):484–486. doi: 10.1038/259484a0. [DOI] [PubMed] [Google Scholar]
  11. Kitua A. Y., Smith T., Alonso P. L., Masanja H., Urassa H., Menendez C., Kimario J., Tanner M. Plasmodium falciparum malaria in the first year of life in an area of intense and perennial transmission. Trop Med Int Health. 1996 Aug;1(4):475–484. doi: 10.1046/j.1365-3156.1996.d01-89.x. [DOI] [PubMed] [Google Scholar]
  12. Kuehr J., Frischer T., Meinert R., Barth R., Schraub S., Urbanek R., Karmaus W., Forster J. Sensitization to mite allergens is a risk factor for early and late onset of asthma and for persistence of asthmatic signs in children. J Allergy Clin Immunol. 1995 Mar;95(3):655–662. doi: 10.1016/s0091-6749(95)70168-0. [DOI] [PubMed] [Google Scholar]
  13. Lewis S. A. Infections in asthma and allergy. Thorax. 1998 Nov;53(11):911–912. doi: 10.1136/thx.53.11.911. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Lynch N. R., Hagel I. A., Palenque M. E., Di Prisco M. C., Escudero J. E., Corao L. A., Sandia J. A., Ferreira L. J., Botto C., Perez M. Relationship between helminthic infection and IgE response in atopic and nonatopic children in a tropical environment. J Allergy Clin Immunol. 1998 Feb;101(2 Pt 1):217–221. doi: 10.1016/S0091-6749(98)70386-0. [DOI] [PubMed] [Google Scholar]
  15. Martinez F. D., Stern D. A., Wright A. L., Taussig L. M., Halonen M. Association of non-wheezing lower respiratory tract illnesses in early life with persistently diminished serum IgE levels. Group Health Medical Associates. Thorax. 1995 Oct;50(10):1067–1072. doi: 10.1136/thx.50.10.1067. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Martinez F. D., Wright A. L., Taussig L. M., Holberg C. J., Halonen M., Morgan W. J. Asthma and wheezing in the first six years of life. The Group Health Medical Associates. N Engl J Med. 1995 Jan 19;332(3):133–138. doi: 10.1056/NEJM199501193320301. [DOI] [PubMed] [Google Scholar]
  17. Masters S., Barrett-Connor E. Parasites and asthma--predictive or protective? Epidemiol Rev. 1985;7:49–58. doi: 10.1093/oxfordjournals.epirev.a036285. [DOI] [PubMed] [Google Scholar]
  18. Menendez C., Kahigwa E., Hirt R., Vounatsou P., Aponte J. J., Font F., Acosta C. J., Schellenberg D. M., Galindo C. M., Kimario J. Randomised placebo-controlled trial of iron supplementation and malaria chemoprophylaxis for prevention of severe anaemia and malaria in Tanzanian infants. Lancet. 1997 Sep 20;350(9081):844–850. doi: 10.1016/S0140-6736(97)04229-3. [DOI] [PubMed] [Google Scholar]
  19. Openshaw P. J., O'Donnell D. R. Asthma and the common cold: can viruses imitate worms? Thorax. 1994 Feb;49(2):101–103. doi: 10.1136/thx.49.2.101. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Pearce N., Pekkanen J., Beasley R. How much asthma is really attributable to atopy? Thorax. 1999 Mar;54(3):268–272. doi: 10.1136/thx.54.3.268. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Pearce N., Weiland S., Keil U., Langridge P., Anderson H. R., Strachan D., Bauman A., Young L., Gluyas P., Ruffin D. Self-reported prevalence of asthma symptoms in children in Australia, England, Germany and New Zealand: an international comparison using the ISAAC protocol. Eur Respir J. 1993 Nov;6(10):1455–1461. [PubMed] [Google Scholar]
  22. Ponsonby A. L., Couper D., Dwyer T., Carmichael A., Kemp A. Relationship between early life respiratory illness, family size over time, and the development of asthma and hay fever: a seven year follow up study. Thorax. 1999 Aug;54(8):664–669. doi: 10.1136/thx.54.8.664. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Reid T. M. Striking a balance in maternal immune response to infection. Lancet. 1998 Jun 6;351(9117):1670–1672. doi: 10.1016/S0140-6736(98)22023-X. [DOI] [PubMed] [Google Scholar]
  24. Rusconi F., Galassi C., Corbo G. M., Forastiere F., Biggeri A., Ciccone G., Renzoni E. Risk factors for early, persistent, and late-onset wheezing in young children. SIDRIA Collaborative Group. Am J Respir Crit Care Med. 1999 Nov;160(5 Pt 1):1617–1622. doi: 10.1164/ajrccm.160.5.9811002. [DOI] [PubMed] [Google Scholar]
  25. Schellenberg D., Menendez C., Kahigwa E., Font F., Galindo C., Acosta C., Schellenberg J. A., Aponte J. J., Kimario J., Urassa H. African children with malaria in an area of intense Plasmodium falciparum transmission: features on admission to the hospital and risk factors for death. Am J Trop Med Hyg. 1999 Sep;61(3):431–438. doi: 10.4269/ajtmh.1999.61.431. [DOI] [PubMed] [Google Scholar]
  26. Shirakawa T., Enomoto T., Shimazu S., Hopkin J. M. The inverse association between tuberculin responses and atopic disorder. Science. 1997 Jan 3;275(5296):77–79. doi: 10.1126/science.275.5296.77. [DOI] [PubMed] [Google Scholar]
  27. Stein R. T., Sherrill D., Morgan W. J., Holberg C. J., Halonen M., Taussig L. M., Wright A. L., Martinez F. D. Respiratory syncytial virus in early life and risk of wheeze and allergy by age 13 years. Lancet. 1999 Aug 14;354(9178):541–545. doi: 10.1016/S0140-6736(98)10321-5. [DOI] [PubMed] [Google Scholar]
  28. Strachan D. P. Hay fever, hygiene, and household size. BMJ. 1989 Nov 18;299(6710):1259–1260. doi: 10.1136/bmj.299.6710.1259. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Tager I. B., Hanrahan J. P., Tosteson T. D., Castile R. G., Brown R. W., Weiss S. T., Speizer F. E. Lung function, pre- and post-natal smoke exposure, and wheezing in the first year of life. Am Rev Respir Dis. 1993 Apr;147(4):811–817. doi: 10.1164/ajrccm/147.4.811. [DOI] [PubMed] [Google Scholar]
  30. Warner A. M., Björkstén B., Munir A. K., Möller C., Schou C., Kjellman N. I. Childhood asthma and exposure to indoor allergens: low mite levels are associated with sensitivity. Pediatr Allergy Immunol. 1996 May;7(2):61–67. doi: 10.1111/j.1399-3038.1996.tb00108.x. [DOI] [PubMed] [Google Scholar]
  31. Watier H., Auriault C., Capron A. Does Epstein-Barr virus infection confer selective advantage to malaria-infected children? Lancet. 1993 Mar 6;341(8845):612–613. doi: 10.1016/0140-6736(93)90364-m. [DOI] [PubMed] [Google Scholar]
  32. Yemaneberhan H., Bekele Z., Venn A., Lewis S., Parry E., Britton J. Prevalence of wheeze and asthma and relation to atopy in urban and rural Ethiopia. Lancet. 1997 Jul 12;350(9071):85–90. doi: 10.1016/S0140-6736(97)01151-3. [DOI] [PubMed] [Google Scholar]
  33. von Mutius E., Martinez F. D., Fritzsch C., Nicolai T., Reitmeir P., Thiemann H. H. Skin test reactivity and number of siblings. BMJ. 1994 Mar 12;308(6930):692–695. doi: 10.1136/bmj.308.6930.692. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Thorax are provided here courtesy of BMJ Publishing Group

RESOURCES