Skip to main content
NCBI home page
The BMJ logoLink to The BMJ
. 1996 Oct 19;313(7063):969–974. doi: 10.1136/bmj.313.7063.969

Cell mediated immunity after measles in Guinea-Bissau: historical cohort study.

S O Shaheen 1, P Aaby 1, A J Hall 1, D J Barker 1, C B Heyes 1, A W Shiell 1, A Goudiaby 1
PMCID: PMC2352342  PMID: 8892416

Abstract

OBJECTIVE: To investigate whether children who have had measles have reduced general cell mediated immunity three years later compared with vaccinated children who have not had measles. DESIGN: Historical cohort study. SETTING: Bissau, Guinea-Bissau. SUBJECTS: 391 children aged 3-13 years who were living in Bissau during a measles epidemic in 1991 and still lived there. These included 131 primary cases and 139 secondary cases from the epidemic and 121 vaccinated controls with no history of measles. MAIN OUTCOME MEASURES: General cell mediated immunity assessed by measurement of delayed type hypersensitivity skin responses to seven recall antigens. Anergy was defined as a lack of response to all antigens. RESULTS: 82 out of 268 cases of measles (31%) were anergic compared with 20 of the 121 vaccinated controls (17%) (odds ratio adjusted for potential confounding variables 2.2 (95% confidence interval 1.2 to 4.0); P 0.009). The prevalence of anergy was higher in secondary cases (33% (46/138)) than in primary cases (28% (36/130)), although this difference was not significant. Anergy was more common in the rainy season (unadjusted prevalence 31% (91/291) than in the dry season (11% (11/98)) (adjusted odds ratio 4.8 (2.2 to 10.3)). This seasonal increase occurred predominantly in the case of measles. CONCLUSION: Reduced general cell mediated immunity may contribute to the higher long term mortality in children who have had measles compared with recipients of standard measles vaccine and to the higher child mortality in the rainy season in west Africa.

Full text

PDF
969

Selected References

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

  1. Aaby P., Andersen M., Sodemann M., Jakobsen M., Gomes J., Fernandes M. Reduced childhood mortality after standard measles vaccination at 4-8 months compared with 9-11 months of age. BMJ. 1993 Nov 20;307(6915):1308–1311. doi: 10.1136/bmj.307.6915.1308. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Aaby P., Bukh J., Lisse I. M., Smits A. J. Measles vaccination and reduction in child mortality: a community study from Guinea-Bissau. J Infect. 1984 Jan;8(1):13–21. doi: 10.1016/s0163-4453(84)93192-x. [DOI] [PubMed] [Google Scholar]
  3. Aaby P., Bukh J., Lisse I. M., da Silva M. C. Further community studies on the role of overcrowding and intensive exposure on measles mortality. Rev Infect Dis. 1988 Mar-Apr;10(2):474–477. doi: 10.1093/clinids/10.2.474. [DOI] [PubMed] [Google Scholar]
  4. Aaby P., Coovadia H. Severe measles: a reappraisal of the role of nutrition, overcrowding and virus dose. Med Hypotheses. 1985 Oct;18(2):93–112. doi: 10.1016/0306-9877(85)90042-8. [DOI] [PubMed] [Google Scholar]
  5. Aaby P., Knudsen K., Jensen T. G., Thårup J., Poulsen A., Sodemann M., da Silva M. C., Whittle H. Measles incidence, vaccine efficacy, and mortality in two urban African areas with high vaccination coverage. J Infect Dis. 1990 Nov;162(5):1043–1048. doi: 10.1093/infdis/162.5.1043. [DOI] [PubMed] [Google Scholar]
  6. Aaby P., Knudsen K., Whittle H., Lisse I. M., Thaarup J., Poulsen A., Sodemann M., Jakobsen M., Brink L., Gansted U. Long-term survival after Edmonston-Zagreb measles vaccination in Guinea-Bissau: increased female mortality rate. J Pediatr. 1993 Jun;122(6):904–908. doi: 10.1016/s0022-3476(09)90015-4. [DOI] [PubMed] [Google Scholar]
  7. Aaby P., Lisse I. M., Mølbak K., Knudsen K., Whittle H. No persistent T lymphocyte immunosuppression or increased mortality after measles infection: a community study from Guinea-Bissau. Pediatr Infect Dis J. 1996 Jan;15(1):39–44. doi: 10.1097/00006454-199601000-00009. [DOI] [PubMed] [Google Scholar]
  8. Aaby P., Pedersen I. R., Knudsen K., da Silva M. C., Mordhorst C. H., Helm-Petersen N. C., Hansen B. S., Thårup J., Poulsen A., Sodemann M. Child mortality related to seroconversion or lack of seroconversion after measles vaccination. Pediatr Infect Dis J. 1989 Apr;8(4):197–200. [PubMed] [Google Scholar]
  9. Aaby P., Samb B., Andersen M., Simondon F. No long-term excess mortality after measles infection: a community study from Senegal. Am J Epidemiol. 1996 May 15;143(10):1035–1041. doi: 10.1093/oxfordjournals.aje.a008667. [DOI] [PubMed] [Google Scholar]
  10. Aaby P., Samb B., Simondon F., Seck A. M., Knudsen K., Whittle H. Non-specific beneficial effect of measles immunisation: analysis of mortality studies from developing countries. BMJ. 1995 Aug 19;311(7003):481–485. doi: 10.1136/bmj.311.7003.481. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Akinwolere O. A., Williams A. I., Akinkugbe F. M., Laditan A. A. Immunity in malaria: depression of delayed hypersensitivity reaction in acute Plasmodium falciparum infection. Afr J Med Med Sci. 1988 Mar;17(1):47–52. [PubMed] [Google Scholar]
  12. Baqui A. H., Black R. E., Sack R. B., Chowdhury H. R., Yunus M., Siddique A. K. Malnutrition, cell-mediated immune deficiency, and diarrhea: a community-based longitudinal study in rural Bangladeshi children. Am J Epidemiol. 1993 Feb 1;137(3):355–365. doi: 10.1093/oxfordjournals.aje.a116682. [DOI] [PubMed] [Google Scholar]
  13. Black R. E., Lanata C. F., Lazo F. Delayed cutaneous hypersensitivity: epidemiologic factors affecting and usefulness in predicting diarrheal incidence in young Peruvian children. Pediatr Infect Dis J. 1989 Apr;8(4):210–215. [PubMed] [Google Scholar]
  14. Chandra R. K., Ali S. K., Kutty K. M., Chandra S. Thymus-dependent lymphocytes and delayed hypersensitivity in low birth weight infants. Biol Neonate. 1977;31(1-2):15–18. doi: 10.1159/000240937. [DOI] [PubMed] [Google Scholar]
  15. Corriel R. N., Kniker W. T., McBryde J. L., Lesourd B. M. Cell-mediated immunity in schoolchildren assessed by multitest skin testing. Normal values and proposed scoring system for healthy children. Am J Dis Child. 1985 Feb;139(2):141–146. doi: 10.1001/archpedi.1985.02140040039022. [DOI] [PubMed] [Google Scholar]
  16. Ferguson A. C. Prolonged impairment of cellular immunity in children with intrauterine growth retardation. J Pediatr. 1978 Jul;93(1):52–56. doi: 10.1016/s0022-3476(78)80599-x. [DOI] [PubMed] [Google Scholar]
  17. Garenne M., Aaby P. Pattern of exposure and measles mortality in Senegal. J Infect Dis. 1990 Jun;161(6):1088–1094. doi: 10.1093/infdis/161.6.1088. [DOI] [PubMed] [Google Scholar]
  18. Gordin F. M., Hartigan P. M., Klimas N. G., Zolla-Pazner S. B., Simberkoff M. S., Hamilton J. D. Delayed-type hypersensitivity skin tests are an independent predictor of human immunodeficiency virus disease progression. Department of Veterans Affairs Cooperative Study Group. J Infect Dis. 1994 Apr;169(4):893–897. doi: 10.1093/infdis/169.4.893. [DOI] [PubMed] [Google Scholar]
  19. Greenwood B. M., Bradley-Moore A. M., Bryceson A. D., Palit A. Immunosuppression in children with malaria. Lancet. 1972 Jan 22;1(7743):169–172. doi: 10.1016/s0140-6736(72)90569-7. [DOI] [PubMed] [Google Scholar]
  20. Harland P. S. Tuberculin reactions in malnourished children. Lancet. 1965 Oct 9;2(7415):719–721. doi: 10.1016/s0140-6736(65)90457-5. [DOI] [PubMed] [Google Scholar]
  21. Hull H. F., Williams P. J., Oldfield F. Measles mortality and vaccine efficacy in rural West Africa. Lancet. 1983 Apr 30;1(8331):972–975. doi: 10.1016/s0140-6736(83)92091-3. [DOI] [PubMed] [Google Scholar]
  22. Kauffman C. A., Linnemann C. C., Jr, Schiff G. M., Phair J. P. Effect of viral and bacterial pneumonias on cell-mediated immunity in humans. Infect Immun. 1976 Jan;13(1):78–83. doi: 10.1128/iai.13.1.78-83.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Kniker W. T., Anderson C. T., Roumiantzeff M. The multi-test system: a standardized approach to evaluation of delayed hypersensitivity and cell-mediated immunity. Ann Allergy. 1979 Aug;43(2):73–79. [PubMed] [Google Scholar]
  24. Kniker W. T., Lesourd B. M., McBryde J. L., Corriel R. N. Cell-mediated immunity assessed by Multitest CMI skin testing in infants and preschool children. Am J Dis Child. 1985 Aug;139(8):840–845. doi: 10.1001/archpedi.1985.02140100102044. [DOI] [PubMed] [Google Scholar]
  25. Koster F. T., Palmer D. L., Chakraborty J., Jackson T., Curlin G. C. Cellular immune competence and diarrheal morbidity in malnourished Bangladeshi children: a prospective field study. Am J Clin Nutr. 1987 Jul;46(1):115–120. doi: 10.1093/ajcn/46.1.115. [DOI] [PubMed] [Google Scholar]
  26. León M. E., Ward B., Kanashiro R., Hernández H., Berry S., Vaisberg A., Escamilla J., Campos M., Bellomo S., Azabache V. Immunologic parameters 2 years after high-titer measles immunization in Peruvian children. J Infect Dis. 1993 Nov;168(5):1097–1104. doi: 10.1093/infdis/168.5.1097. [DOI] [PubMed] [Google Scholar]
  27. Lisse I. M., Aaby P., Knudsen K., Whittle H., Andersen H. Long term impact of high titer Edmonston-Zagreb measles vaccine on T lymphocyte subsets. Pediatr Infect Dis J. 1994 Feb;13(2):109–112. doi: 10.1097/00006454-199402000-00006. [DOI] [PubMed] [Google Scholar]
  28. Mølbak K., Aaby P., Ingholt L., Højlyng N., Gottschau A., Andersen H., Brink L., Gansted U., Permin A., Vollmer A. Persistent and acute diarrhoea as the leading causes of child mortality in urban Guinea Bissau. Trans R Soc Trop Med Hyg. 1992 Mar-Apr;86(2):216–220. doi: 10.1016/0035-9203(92)90580-6. [DOI] [PubMed] [Google Scholar]
  29. Pabst H. F., Godel J., Grace M., Cho H., Spady D. W. Effect of breast-feeding on immune response to BCG vaccination. Lancet. 1989 Feb 11;1(8633):295–297. doi: 10.1016/s0140-6736(89)91307-x. [DOI] [PubMed] [Google Scholar]
  30. Poulsen A. G., Aaby P., Gottschau A., Kvinesdal B. B., Dias F., Mølbak K., Lauritzen E. HIV-2 infection in Bissau, West Africa, 1987-1989: incidence, prevalences, and routes of transmission. J Acquir Immune Defic Syndr. 1993 Aug;6(8):941–948. [PubMed] [Google Scholar]
  31. Poulsen A. G., Kvinesdal B. B., Aaby P., Lisse I. M., Gottschau A., Mølbak K., Dias F., Lauritzen E. Lack of evidence of vertical transmission of human immunodeficiency virus type 2 in a sample of the general population in Bissau. J Acquir Immune Defic Syndr. 1992;5(1):25–30. [PubMed] [Google Scholar]
  32. Poulsen A. G., Kvinesdal B., Aaby P., Mølbak K., Frederiksen K., Dias F., Lauritzen E. Prevalence of and mortality from human immunodeficiency virus type 2 in Bissau, West Africa. Lancet. 1989 Apr 15;1(8642):827–831. doi: 10.1016/s0140-6736(89)92281-2. [DOI] [PubMed] [Google Scholar]
  33. Salmeron G., Lipsky P. E. Immunosuppressive potential of antimalarials. Am J Med. 1983 Jul 18;75(1A):19–24. doi: 10.1016/0002-9343(83)91266-4. [DOI] [PubMed] [Google Scholar]
  34. Schlesinger J. J., Covelli H. D. Evidence for transmission of lymphocyte responses to tuberculin by breast-feeding. Lancet. 1977 Sep 10;2(8037):529–532. doi: 10.1016/s0140-6736(77)90665-1. [DOI] [PubMed] [Google Scholar]
  35. Shaheen S. O., Aaby P., Hall A. J., Barker D. J., Heyes C. B., Shiell A. W., Goudiaby A. Measles and atopy in Guinea-Bissau. Lancet. 1996 Jun 29;347(9018):1792–1796. doi: 10.1016/s0140-6736(96)91617-7. [DOI] [PubMed] [Google Scholar]
  36. Smedman L., Lindeberg A., Jeppsson O., Zetterstrom R. Nutritional status and measles: a community study in Guinea-Bissau. Ann Trop Paediatr. 1983 Dec;3(4):169–176. doi: 10.1080/02724936.1983.11748290. [DOI] [PubMed] [Google Scholar]
  37. Smith S. M., Levy N. S., Hayes C. E. Impaired immunity in vitamin A-deficient mice. J Nutr. 1987 May;117(5):857–865. doi: 10.1093/jn/117.5.857. [DOI] [PubMed] [Google Scholar]
  38. Sokal J. E. Editorial: Measurement of delayed skin-test responses. N Engl J Med. 1975 Sep 4;293(10):501–502. doi: 10.1056/NEJM197509042931013. [DOI] [PubMed] [Google Scholar]
  39. Tamashiro V. G., Perez H. H., Griffin D. E. Prospective study of the magnitude and duration of changes in tuberculin reactivity during uncomplicated and complicated measles. Pediatr Infect Dis J. 1987 May;6(5):451–454. doi: 10.1097/00006454-198705000-00007. [DOI] [PubMed] [Google Scholar]
  40. Whittle H. C., Bradley-Moore A., Fleming A., Greenwood B. M. Effects of measles on the immune response of Nigerian children. Arch Dis Child. 1973 Oct;48(10):753–756. doi: 10.1136/adc.48.10.753. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from BMJ : British Medical Journal are provided here courtesy of BMJ Publishing Group

RESOURCES