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Efficacy of Pneumococcal Vaccination in Adults: A Meta-analysis of Randomized Controlled Trials

Efficacy of Pneumococcal Vaccination in Adults: A Meta-analysis of Randomized Controlled Trials Abstract Background: Because of the prevalence of pneumococcal pneumonia, the substantial morbidity and mortality associated with many pneumococcal infections, and an increase in the incidence of antibiotic resistance among pneumococcal isolates, considerable efforts for disease prevention have been made using a polyvalent polysaccharide pneumococcal vaccine. Despite numerous clinical trials of the vaccine, its efficacy in the prevention of pneumococcal infections and other clinically relevant medical outcomes in adults remains uncertain. Methods: To assess quantitatively the efficacy of pneumococcal vaccination, a MEDLINE literature search, manual reviews of article bibliographies, and communications with pneumococcal vaccine investigators were used to identify randomized controlled trials of the pneumococcal vaccine. Independent review of 594 articles revealed nine randomized trials with 12 vaccine and control study groups that evaluated clinically relevant outcomes in adults. To estimate a summary effect size for all outcomes, Mantel-Haenszel odds ratios (ORs) and Dersimonian and Laird rate differences (RDs) and their associated 95% confidence intervals (CIs) were computed. Results: Summary ORs demonstrated a statistically significant protective effect of the vaccine for four pneumococcal infection—related outcomes: definitive pneumococcal pneumonia (OR=0.34; 95% CI=0.24 to 0.48), definitive pneumococcal pneumonia for vaccine-containing pneumococcal antigen types only (vaccine types only) (OR=0.17; 95% CI=0.09 to 0.33), presumptive pneumococcal pneumonia (OR=0.47; 95% CI=0.35 to 0.63), and presumptive pneumococcal pneumonia (vaccine types only) (OR=0.39; 95% CI=0.26 to 0.59). The summary RDs, which account for heterogeneity among studies, confirmed a statistically significant protective effect for two of these same outcomes: definitive pneumococcal pneumonia (RD=4/1000; 95% CI=0/1000 to 7/1000) and definitive pneumococcal pneumonia (vaccine types only) (RD=8/1000; 95% CI=1/1000 to 16/1000). Summary ORs and RDs failed to demonstrate a protective effect for pneumonia (all causes), bronchitis, and mortality (all causes) or mortality due to pneumonia or pneumococcal infection. Subgroup analyses showed that for all four pneumococcal infection—related outcomes, vaccine efficacy differed for high- and low-risk subjects, demonstrating efficacy for low-risk subjects and lack of efficacy for high-risk subjects. Conclusions: Pneumococcal vaccination appears efficacious in reducing bacteremic pneumococcal pneumonia in low-risk adults. However, evidence from randomized controlled trials fails to demonstrate vaccine efficacy for pneumococcal infection-related or other medical outcomes in the heterogeneous group of subjects currently labeled as high risk.(Arch Intern Med. 1994;154:2666-2677) References 1. Istre GR, Tarpay M, Anderson M, Pryor A, Welch D. Invasive disease due to Streptococcus pneumonia in an area with a high rate of relative penicillin resistance . J Infect Dis. 1987;156:732-735.Crossref 2. Breiman RF, Spika JS, Navarro VJ, Darden PM, Darby CP. Pneumococcal bacteremia in Charleston County, South Carolina: a decade later . Arch Intern Med. 1990;150:1401-1405.Crossref 3. Fedson DS, Musher DM. Pneumococcal vaccine . In: Plotkin SA, Mortimer EA, Jr, eds. Vaccines . Philadelphia, Pa: WB Saunders Co; 1994:517-564. 4. Mufson M. Streptococcus pneumoniae . In: Mandel GG, Douglas RB, Bennet JE, eds. Principles and Practice of Infectious Diseases . New York, NY: Churchill-Livingstone Inc; 1990:1539-1550. 5. Immunization Practices Advisory Committee. Pneumococcal polysaccharide vaccine . MMWR Morb Mortal Wkly Rep. 1989;38:64-68, 73-76. 6. Kaufman P, Kaeffely A, O'Brien C, Burnstein C, Kling S, Dmitruk W. Studies on old age pneumonia: prophylactic effect of pneumococcus polysaccharide against pneumonia . Arch Intern Med. 1941;67:304-319.Crossref 7. MacLeod CM, Hodges RG, Heidelberger M, Bernhard WG. Prevention of pneumococcal pneumonia by immunization with specific capsular polysaccharides . J Exp Med. 1945;82:445-465.Crossref 8. Kaufman P, Kaeffely A, Klingst SK, O'Brien C, Stein H. Pneumonia in old age: active immunization against pneumonia with pneumococcus polysaccharide: results of a six-year study . Arch Intern Med. 1947;79:518-531.Crossref 9. Austrian R, Douglas RM, Schiffman G, Coetzee AM, Koornhof HJ, Hayden-Smith S, Reid RD. Prevention of pneumococcal pneumonia by vaccination . Trans Assoc Am Physician. 1976;89:184-194. 10. Smit P, Oberholzer D, Hayden-Smith S, Koornhof HJ, Hilleman MR. Protective efficacy of pneumococcal polysaccharide vaccines . JAMA . 1977;238:2613-2616.Crossref 11. Riley ID, Tarr PI, Andrews M, et al. Immunisation with a polyvalent pneumococcal vaccine: reduction of adult respiratory mortality in a New Guinea Highlands community . Lancet . 1977;1:1338-1341.Crossref 12. Austrian R. Surveillance of Pneumococcal Infection for Field Trials of Polyvalent Pneumococcal Vaccines . Bethesda, Md: National Institute of Allergy and Infectious Diseases; 1980:1-59. National Institutes of Health publication DAB-VDP-12-84; Contract N01 A13257. 13. Gaillat J, Zmirou D, Mallaret MR, et al. Clinical trial of an antipneumococcal vaccine in elderly subjects living in institutions . Rev Epidemiol Sante Publique. 1985;33:437-444. 14. Klastersky J, Mommen P, Cantraine F, Safary A. Placebo controlled pneumococcal immunization in patients with bronchogenic carcinoma . Eur J Cancer Clin Oncol. 1986;22:807-813.Crossref 15. Simberkoff MS, Cross AP, Al-lbrahim M, et al. Efficacy of pneumococcal vaccine in high-risk patients: results of a Veterans Administration Cooperative Study . N Engl J Med. 1986;315:1318-1327.Crossref 16. Davis AL, Aranda CP, Schiffman G, Christianson LC. Pneumococcal infection and immunologic response to pneumococcal vaccine in chronic obstructive pulmonary disease: a pilot study . Chest. 1987;92:204-212.Crossref 17. Leech JA, Gervais A, Ruben FL. Efficacy of pneumococcal vaccine in severe chronic obstructive pulmonary disease . Can Med Assoc J. 1987;136:361-365. 18. Shapiro ED, Clemens JD. A controlled evaluation of the protective efficacy of pneumococcal vaccine for patients at high risk of serious pneumococcal infections . Ann Intern Med. 1984;101:325-330.Crossref 19. Forrester HL, Jahnigen DW, LaForce FM. Inefficacy of pneumococcal vaccine in a high-risk population . Am J Med. 1987;83:425-430.Crossref 20. Sims RV, Steinmann WC, McConville JH, King LR, Zwick WC, Schwartz JS. The clinical effectiveness of pneumococcal vaccine in the elderly . Ann Intern Med. 1988;108:653-657.Crossref 21. Shapiro ED, Berg AT, Austrian R, et al. The protective efficacy of polyvalent pneumococcal polysaccharide vaccine . N Engl J Med. 1991;325:1453-1460.Crossref 22. Frame PS. A critical review of adult health maintenance, II: prevention of infectious diseases . J Fam Pract. 1986;22:341-346. 23. Fedson D, Jenrichsen J, Makela PH, Austrian R. WHO recommendations on pneumococcal vaccination . Infection. 1986;6:437-441. 24. US Preventive Services Task Force. Guide to Clinical Preventive Services: An Assessment of the Effectiveness of 169 Interventions . Baltimore, Md; Williams & Wilkins; 1989. 25. American College of Physicians Task Force on Adult Immunization. Guide for Adult Immunization . 2nd ed. Philadelphia, Pa: American College of Physicians; 1990. 26. Canadian Task Force on the Periodic Health Examination. Periodic Health Examination, 1991: update 2: administration of pneumococcal vaccine . Can Med Assoc J. 1991;144:665-671. 27. L'Abbe KA, Detsky AS, O'Rourke K. Meta-analysis in clinical research . Ann Intern Med. 1987;107-224-233. 28. Chalmers TC, Smith H Jr, Blackburn B, et al. A method for assessing the quality of a randomized control trial . Control Clin Trials. 1981;2:31-49.Crossref 29. Fleiss JA. The Mantel-Haenszel method . In: Statistical Methods for Rates and Proportions . 2nd ed. New York, NY: John Wiley & Sons Inc; 1981:173-175. 30. Dersimonian R, Laird N. Meta-analysis in clinical trials . Control Clin Trials. 1986; 7:177-188.Crossref 31. Hedges LV, Olkin I. Statistical Methods for Meta-analysis . Orlando, Fla: Academic Press Inc; 1985:305-306. 32. Sacks HS, Berrier J, Reitman D, Ancona-Berk VA, Chalmers TC. Meta-analysis of randomized controlled trials . N Engl J Med. 1987;316:450-455.Crossref 33. Hirschmann JF, Lipsky BA. Pneumococcal vaccine in the United States . JAMA . 1981;246:1428-1431.Crossref 34. Schwartz JS. Pneumococcal vaccine: clinical efficacy and effectiveness . Ann Intern Med. 1982;96:208-220.Crossref 35. LaForce FM. Immunizations, immunoprophylaxis, and chemoprophylaxis to prevent selected infections . JAMA . 1987;257:2464-2470.Crossref 36. Bolan G, Broome CV, Facklam RR, Plikaytis BD, Fraser DW, Schlech WF III. Pneumococcal vaccine efficacy in selected populations in the United States . Ann Intern Med. 1986;104:1-6.Crossref 37. Butler JC, Breiman RF, Cambell JF, Lipman HB, Broome CV, Facklam RR. Pneumococcal polysaccharide vaccine efficacy: an evaluation of current recommendations . JAMA . 1993;270:1826-1831.Crossref 38. Stein KE. Thymus-independent and thymus-dependent responses to polysaccharide antigens . J Infect Dis. 1992;165( (suppl 1) ):S49-S52.Crossref 39. Simberkoff MS. Pneumococcal vaccination in the prevention of communityacquired pneumonia: a skeptical view of cost-effectiveness . Semin Respir Infect. 1994;8:294-299. 40. Glaser JB, Volpe S, Aguirre A, Simkins H, Schiffman G. Zidovudine improves response to pneumococcal vaccine among persons with AIDS and AIDS-related complex . J Infect Dis. 1991;164:761-764.Crossref 41. Rodriguez-Barradas MC, Musher DM, Lahart C, et al. Antibody to capsular polysaccharides of Streptococcus pneumoniae after vaccination of human immunodeficiency virus—infected subjects with 23-valent pneumococcal vaccine . J Infect Dis. 1992;165:553-556.Crossref 42. Simberkoff MS, Schiffman G, Katz LA, Spicehandler JR, Moldover NH, Rahal JJ. Pneumococcal capsular polysaccharide vaccination in adult chronic hemodialysis patients . J Lab Clin Med. 1980;96:363-370. 43. Linneman CC, First R, Schiffman G. Revaccination of renal transplant and hemodialysis recipients with pneumococcal vaccine . Arch Intern Med. 1986;146: 1554-1556.Crossref 44. Minor DR, Schiffman G, McIntosh LS. Response of patients with Hodgkin's disease to pneumococcal vaccine . Ann Intern Med. 1979;90:887-892.Crossref 45. Lazarus HM, Lederman M, Lubin A, et al. Pneumococcal vaccination: the response of patients with multiple myeloma . Am J Med. 1980;69:419-423.Crossref 46. Douglas RM, Hansman D, McDonald B, Paton J, Kirke K. Pneumococcal vaccine in aboriginal children: a randomized controlled trial involving 60 children . Comm Health Studies . 1986;10:189-196.Crossref 47. Lehmann D. Pneumococcal polysaccharide vaccine prevents death from pneumonia in Papua New Guinean children . Papua New Guinea Med J. 1986;29: 281-283. 48. Gray BM, Dillon HC. Clinical and epidemiologic studies of pneumococcal infection in children . Pediatr Infect Dis. 1986;5:201-207.Crossref 49. Jacobs NM, Lerdkachornsuk S, Metsger WI. Pneumococcal bacteremia in infants and children: a ten-year experience at the Cook County Hospital with special reference to the pneumococcal serotypes isolated . Pediatrics. 1979; 64:296-300. http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Archives of Internal Medicine American Medical Association

Efficacy of Pneumococcal Vaccination in Adults: A Meta-analysis of Randomized Controlled Trials

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Publisher
American Medical Association
Copyright
Copyright © 1994 American Medical Association. All Rights Reserved.
ISSN
0003-9926
eISSN
1538-3679
DOI
10.1001/archinte.1994.00420230051007
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Abstract

Abstract Background: Because of the prevalence of pneumococcal pneumonia, the substantial morbidity and mortality associated with many pneumococcal infections, and an increase in the incidence of antibiotic resistance among pneumococcal isolates, considerable efforts for disease prevention have been made using a polyvalent polysaccharide pneumococcal vaccine. Despite numerous clinical trials of the vaccine, its efficacy in the prevention of pneumococcal infections and other clinically relevant medical outcomes in adults remains uncertain. Methods: To assess quantitatively the efficacy of pneumococcal vaccination, a MEDLINE literature search, manual reviews of article bibliographies, and communications with pneumococcal vaccine investigators were used to identify randomized controlled trials of the pneumococcal vaccine. Independent review of 594 articles revealed nine randomized trials with 12 vaccine and control study groups that evaluated clinically relevant outcomes in adults. To estimate a summary effect size for all outcomes, Mantel-Haenszel odds ratios (ORs) and Dersimonian and Laird rate differences (RDs) and their associated 95% confidence intervals (CIs) were computed. Results: Summary ORs demonstrated a statistically significant protective effect of the vaccine for four pneumococcal infection—related outcomes: definitive pneumococcal pneumonia (OR=0.34; 95% CI=0.24 to 0.48), definitive pneumococcal pneumonia for vaccine-containing pneumococcal antigen types only (vaccine types only) (OR=0.17; 95% CI=0.09 to 0.33), presumptive pneumococcal pneumonia (OR=0.47; 95% CI=0.35 to 0.63), and presumptive pneumococcal pneumonia (vaccine types only) (OR=0.39; 95% CI=0.26 to 0.59). The summary RDs, which account for heterogeneity among studies, confirmed a statistically significant protective effect for two of these same outcomes: definitive pneumococcal pneumonia (RD=4/1000; 95% CI=0/1000 to 7/1000) and definitive pneumococcal pneumonia (vaccine types only) (RD=8/1000; 95% CI=1/1000 to 16/1000). Summary ORs and RDs failed to demonstrate a protective effect for pneumonia (all causes), bronchitis, and mortality (all causes) or mortality due to pneumonia or pneumococcal infection. Subgroup analyses showed that for all four pneumococcal infection—related outcomes, vaccine efficacy differed for high- and low-risk subjects, demonstrating efficacy for low-risk subjects and lack of efficacy for high-risk subjects. Conclusions: Pneumococcal vaccination appears efficacious in reducing bacteremic pneumococcal pneumonia in low-risk adults. However, evidence from randomized controlled trials fails to demonstrate vaccine efficacy for pneumococcal infection-related or other medical outcomes in the heterogeneous group of subjects currently labeled as high risk.(Arch Intern Med. 1994;154:2666-2677) References 1. Istre GR, Tarpay M, Anderson M, Pryor A, Welch D. Invasive disease due to Streptococcus pneumonia in an area with a high rate of relative penicillin resistance . J Infect Dis. 1987;156:732-735.Crossref 2. Breiman RF, Spika JS, Navarro VJ, Darden PM, Darby CP. Pneumococcal bacteremia in Charleston County, South Carolina: a decade later . Arch Intern Med. 1990;150:1401-1405.Crossref 3. Fedson DS, Musher DM. Pneumococcal vaccine . In: Plotkin SA, Mortimer EA, Jr, eds. Vaccines . Philadelphia, Pa: WB Saunders Co; 1994:517-564. 4. Mufson M. Streptococcus pneumoniae . In: Mandel GG, Douglas RB, Bennet JE, eds. Principles and Practice of Infectious Diseases . New York, NY: Churchill-Livingstone Inc; 1990:1539-1550. 5. Immunization Practices Advisory Committee. Pneumococcal polysaccharide vaccine . MMWR Morb Mortal Wkly Rep. 1989;38:64-68, 73-76. 6. Kaufman P, Kaeffely A, O'Brien C, Burnstein C, Kling S, Dmitruk W. Studies on old age pneumonia: prophylactic effect of pneumococcus polysaccharide against pneumonia . Arch Intern Med. 1941;67:304-319.Crossref 7. MacLeod CM, Hodges RG, Heidelberger M, Bernhard WG. Prevention of pneumococcal pneumonia by immunization with specific capsular polysaccharides . J Exp Med. 1945;82:445-465.Crossref 8. Kaufman P, Kaeffely A, Klingst SK, O'Brien C, Stein H. Pneumonia in old age: active immunization against pneumonia with pneumococcus polysaccharide: results of a six-year study . Arch Intern Med. 1947;79:518-531.Crossref 9. Austrian R, Douglas RM, Schiffman G, Coetzee AM, Koornhof HJ, Hayden-Smith S, Reid RD. Prevention of pneumococcal pneumonia by vaccination . Trans Assoc Am Physician. 1976;89:184-194. 10. Smit P, Oberholzer D, Hayden-Smith S, Koornhof HJ, Hilleman MR. Protective efficacy of pneumococcal polysaccharide vaccines . JAMA . 1977;238:2613-2616.Crossref 11. Riley ID, Tarr PI, Andrews M, et al. Immunisation with a polyvalent pneumococcal vaccine: reduction of adult respiratory mortality in a New Guinea Highlands community . Lancet . 1977;1:1338-1341.Crossref 12. Austrian R. Surveillance of Pneumococcal Infection for Field Trials of Polyvalent Pneumococcal Vaccines . Bethesda, Md: National Institute of Allergy and Infectious Diseases; 1980:1-59. National Institutes of Health publication DAB-VDP-12-84; Contract N01 A13257. 13. Gaillat J, Zmirou D, Mallaret MR, et al. Clinical trial of an antipneumococcal vaccine in elderly subjects living in institutions . Rev Epidemiol Sante Publique. 1985;33:437-444. 14. Klastersky J, Mommen P, Cantraine F, Safary A. Placebo controlled pneumococcal immunization in patients with bronchogenic carcinoma . Eur J Cancer Clin Oncol. 1986;22:807-813.Crossref 15. Simberkoff MS, Cross AP, Al-lbrahim M, et al. Efficacy of pneumococcal vaccine in high-risk patients: results of a Veterans Administration Cooperative Study . N Engl J Med. 1986;315:1318-1327.Crossref 16. Davis AL, Aranda CP, Schiffman G, Christianson LC. Pneumococcal infection and immunologic response to pneumococcal vaccine in chronic obstructive pulmonary disease: a pilot study . Chest. 1987;92:204-212.Crossref 17. Leech JA, Gervais A, Ruben FL. Efficacy of pneumococcal vaccine in severe chronic obstructive pulmonary disease . Can Med Assoc J. 1987;136:361-365. 18. Shapiro ED, Clemens JD. A controlled evaluation of the protective efficacy of pneumococcal vaccine for patients at high risk of serious pneumococcal infections . Ann Intern Med. 1984;101:325-330.Crossref 19. Forrester HL, Jahnigen DW, LaForce FM. Inefficacy of pneumococcal vaccine in a high-risk population . Am J Med. 1987;83:425-430.Crossref 20. Sims RV, Steinmann WC, McConville JH, King LR, Zwick WC, Schwartz JS. The clinical effectiveness of pneumococcal vaccine in the elderly . Ann Intern Med. 1988;108:653-657.Crossref 21. Shapiro ED, Berg AT, Austrian R, et al. The protective efficacy of polyvalent pneumococcal polysaccharide vaccine . N Engl J Med. 1991;325:1453-1460.Crossref 22. Frame PS. A critical review of adult health maintenance, II: prevention of infectious diseases . J Fam Pract. 1986;22:341-346. 23. Fedson D, Jenrichsen J, Makela PH, Austrian R. WHO recommendations on pneumococcal vaccination . Infection. 1986;6:437-441. 24. US Preventive Services Task Force. Guide to Clinical Preventive Services: An Assessment of the Effectiveness of 169 Interventions . Baltimore, Md; Williams & Wilkins; 1989. 25. American College of Physicians Task Force on Adult Immunization. Guide for Adult Immunization . 2nd ed. Philadelphia, Pa: American College of Physicians; 1990. 26. Canadian Task Force on the Periodic Health Examination. Periodic Health Examination, 1991: update 2: administration of pneumococcal vaccine . Can Med Assoc J. 1991;144:665-671. 27. L'Abbe KA, Detsky AS, O'Rourke K. Meta-analysis in clinical research . Ann Intern Med. 1987;107-224-233. 28. Chalmers TC, Smith H Jr, Blackburn B, et al. A method for assessing the quality of a randomized control trial . Control Clin Trials. 1981;2:31-49.Crossref 29. Fleiss JA. The Mantel-Haenszel method . In: Statistical Methods for Rates and Proportions . 2nd ed. New York, NY: John Wiley & Sons Inc; 1981:173-175. 30. Dersimonian R, Laird N. Meta-analysis in clinical trials . Control Clin Trials. 1986; 7:177-188.Crossref 31. Hedges LV, Olkin I. Statistical Methods for Meta-analysis . Orlando, Fla: Academic Press Inc; 1985:305-306. 32. Sacks HS, Berrier J, Reitman D, Ancona-Berk VA, Chalmers TC. Meta-analysis of randomized controlled trials . N Engl J Med. 1987;316:450-455.Crossref 33. Hirschmann JF, Lipsky BA. Pneumococcal vaccine in the United States . JAMA . 1981;246:1428-1431.Crossref 34. Schwartz JS. Pneumococcal vaccine: clinical efficacy and effectiveness . Ann Intern Med. 1982;96:208-220.Crossref 35. LaForce FM. Immunizations, immunoprophylaxis, and chemoprophylaxis to prevent selected infections . JAMA . 1987;257:2464-2470.Crossref 36. Bolan G, Broome CV, Facklam RR, Plikaytis BD, Fraser DW, Schlech WF III. Pneumococcal vaccine efficacy in selected populations in the United States . Ann Intern Med. 1986;104:1-6.Crossref 37. Butler JC, Breiman RF, Cambell JF, Lipman HB, Broome CV, Facklam RR. Pneumococcal polysaccharide vaccine efficacy: an evaluation of current recommendations . JAMA . 1993;270:1826-1831.Crossref 38. Stein KE. Thymus-independent and thymus-dependent responses to polysaccharide antigens . J Infect Dis. 1992;165( (suppl 1) ):S49-S52.Crossref 39. Simberkoff MS. Pneumococcal vaccination in the prevention of communityacquired pneumonia: a skeptical view of cost-effectiveness . Semin Respir Infect. 1994;8:294-299. 40. Glaser JB, Volpe S, Aguirre A, Simkins H, Schiffman G. Zidovudine improves response to pneumococcal vaccine among persons with AIDS and AIDS-related complex . J Infect Dis. 1991;164:761-764.Crossref 41. Rodriguez-Barradas MC, Musher DM, Lahart C, et al. Antibody to capsular polysaccharides of Streptococcus pneumoniae after vaccination of human immunodeficiency virus—infected subjects with 23-valent pneumococcal vaccine . J Infect Dis. 1992;165:553-556.Crossref 42. Simberkoff MS, Schiffman G, Katz LA, Spicehandler JR, Moldover NH, Rahal JJ. Pneumococcal capsular polysaccharide vaccination in adult chronic hemodialysis patients . J Lab Clin Med. 1980;96:363-370. 43. Linneman CC, First R, Schiffman G. Revaccination of renal transplant and hemodialysis recipients with pneumococcal vaccine . Arch Intern Med. 1986;146: 1554-1556.Crossref 44. Minor DR, Schiffman G, McIntosh LS. Response of patients with Hodgkin's disease to pneumococcal vaccine . Ann Intern Med. 1979;90:887-892.Crossref 45. Lazarus HM, Lederman M, Lubin A, et al. Pneumococcal vaccination: the response of patients with multiple myeloma . Am J Med. 1980;69:419-423.Crossref 46. Douglas RM, Hansman D, McDonald B, Paton J, Kirke K. Pneumococcal vaccine in aboriginal children: a randomized controlled trial involving 60 children . Comm Health Studies . 1986;10:189-196.Crossref 47. Lehmann D. Pneumococcal polysaccharide vaccine prevents death from pneumonia in Papua New Guinean children . Papua New Guinea Med J. 1986;29: 281-283. 48. Gray BM, Dillon HC. Clinical and epidemiologic studies of pneumococcal infection in children . Pediatr Infect Dis. 1986;5:201-207.Crossref 49. Jacobs NM, Lerdkachornsuk S, Metsger WI. Pneumococcal bacteremia in infants and children: a ten-year experience at the Cook County Hospital with special reference to the pneumococcal serotypes isolated . Pediatrics. 1979; 64:296-300.

Journal

Archives of Internal MedicineAmerican Medical Association

Published: Dec 12, 1994

References