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Nosocomial Bloodstream Infections: Secular Trends in Rates, Mortality, and Contribution to Total Hospital Deaths

Nosocomial Bloodstream Infections: Secular Trends in Rates, Mortality, and Contribution to Total... Abstract Background: Nosocomial bloodstream infections occur at a rate of 1.3 to 14.5 per 1000 hospital admissions and are believed to lead directly to 62 500 deaths per year in the United States. Measures of the incidence and the proportion of all hospital deaths related to deaths from these infections provide estimates of their impact. The objectives of the study were to characterize the secular trends in nosocomial bloodstream infection at a single institution and to estimate the population-attributable risk for death among patients experiencing the infection. Methods: A 12-year retrospective study using prospectively collected data from a hospital-wide surveillance system for nosocomial infections in a 900-bed tertiary care institution. All patients (N=260 834) admitted to the institution between 1980 and 1992 were included in the study. Bloodstream infection rates were calculated for the 10 leading groups of pathogens, and trends were analyzed using simple linear regression. In-hospital mortality rates from patients who did or did not develop nosocomial bloodstream infections were compared. Results: Between 1980 and 1992, a total of 3077 patients developed 3464 episodes of nosocomial bloodstream infection. The crude infection rates increased linearly from 6.7 to 18.4 per 1000 discharges (0.83 to 1.72 episodes per 1000 patient-days) during the 12-year study period (r=.87). Increases in the infection rates were due to gram-positive cocci (r=.96) and yeasts (r=.95) and essentially explained by infections caused by coagulase-negative staphylococci, Staphylococcus aureus, enterococci, and Candida species, respectively. Although the crude mortality in patients with nosocomial bloodstream infections decreased from 51% in 1981 to 29% in 1992, the in-hospital population-attributable mortality among infected patients increased from 3.55 deaths per 1000 discharges in 1981 to 6.22 per 1000 discharges in 1992 (r=.67). The etiologic fraction or the proportion of deaths in patients with bloodstream infection to all deaths occurring in the hospital increased from 11.4% in 1981 to 20.4% in 1992 (r=.59). Conclusions: The incidence, the etiologic fraction, and the population-attributable risk for death among patients experiencing nosocomial bloodstream infections increased progressively during the last decade.(Arch Intern Med. 1995;155:1177-1184) References 1. Pittet D. Nosocomial bloodstream infections. In: Wenzel RP, ed. Prevention and Control of Nosocomial Infections . 2nd ed. Baltimore, Md: Williams & Wilkins; 1993:512-555. 2. Maki DG. Nosocomial bacteremia: an epidemiologic overview. Am J Med . 1981; 70:719-732.Crossref 3. Bryan CS, Hornung CA, Reynolds KL, Brenner ER. Endemic bacteremia in Columbia, South Carolina. Am J Epidemiol . 1986;123:113-127. 4. Morrison AJ Jr, Freer CV, Searcy MA, Landry SM, Wenzel RP. Nosocomial bloodstream infections: secular trends in a statewide surveillance program in Virginia. Infect Control . 1986;7:550-553. 5. Filice GA, Van Etta LL, Darby CP, Fraser DW. Bacteremia in Charleston County, South Carolina. Am J Epidemiol . 1986;123:128-136. 6. McLaws M, Gold J, King K, Irwig LM, Berry G. The prevalence of nosocomial and community-acquired infections in Australian hospitals. Med J Aust . 1988; 149:582-590. 7. Banerjee SN, Emori TG, Culver DH, et al. Secular trends in nosocomial primary bloodstream infections in the United States, 1980-1989: National Nosocomial Infections Surveillance System. Am J Med . 1991;91( (suppl 3B) ):86S-89S.Crossref 8. Gatell JM, Trilla A, Latorre X, et al. Nosocomial bacteremia in a large Spanish teaching hospital: analysis of factors influencing prognosis. Rev Infect Dis . 1988;10:203-210.Crossref 9. Centers for Disease Control. Increase in national hospital discharge survey rates for septicemia—United States. MMWR Morb Mortal Wkly Rep . 1990;39:31-34. 10. Centers for Disease Control and Prevention. Annual summary of births, marriages, divorces, and deaths: United States, 1993. Monthly Vital Stat Rep . 1994; 42:4-10. 11. Roberts FJ, Geere IW, Coldman A. A three-year study of positive blood cultures, with emphasis on prognosis. Rev Infect Dis . 1991;13:34-46.Crossref 12. Weinstein MP, Murphy JR, Reller LB, Lichtenstein KA. The clinical significance of positive blood cultures: a comprehensive analysis of 500 episodes of bacteremia and fungemia in adults, II: clinical observations, with special reference to factors influencing prognosis. Rev Infect Dis . 1983;5:54-70.Crossref 13. Bryan CS, Reynolds KL, Brenner ER. Analysis of 1186 episodes of gram-negative bacteremia in non-university hospitals: the effects of antimicrobial therapy. Rev Infect Dis . 1983;5:629-638.Crossref 14. Broderick A, Mori M, Nettleman MD, Streed SA, Wenzel RP. Nosocomial infections: validation of surveillance and computer modeling to identify patients at risk. Am J Epidemiol . 1990;131:734-742. 15. Garner JS, Jarvis WR, Emori TG. CDC definition for nosocomial infections. Am J Infect Control . 1988;16:128-140.Crossref 16. Weinstein MP, Reller LB, Murphy JR, Lichtenstein KA. The clinical significance of positive blood cultures: a comprehensive analysis of 500 episodes of bacteremia and fungemia in adults, I: laboratory and epidemiologic observations. Rev Infect Dis . 1983;5:35-53.Crossref 17. Roberts FJ. Definition of polymicrobial bacteremia. Rev Infect Dis . 1989;11: 1029-1030.Crossref 18. Miettinen OS. Proportions of disease caused or prevented by a given exposure, threat, or intervention. Am J Epidemiol . 1974;99:325-332. 19. Kesley JL, Thompson WD, Evans AS. Methods in Observational Epidemiology . New York, NY: Oxford University Press; 1986:3. 20. Bone RC. A critical evaluation of new agents for the treatment of sepsis. JAMA . 1991;266:1686-1691.Crossref 21. Bone RC. Toward an epidemiology and natural history of SIRS (systemic inflammatory response syndrome). JAMA . 1992;268:3452-3455.Crossref 22. Koontz FP, Flint KK, Reynolds JK, Allen SD. Multicenter comparison of the high volume (10 ml) NR BACTEC PLUS system and the standard (5 ml) NR BACTEC system. Diagn Microbiol Infect Dis . 1991;14:111-118.Crossref 23. Wenzel RP. The mortality of hospital-acquired bloodstream infections: need for a new vital statistic? Int J Epidemiol . 1988;17:225-227.Crossref 24. Mylotte JM, White D, McDermott C, Hodan C. Nosocomial bloodstream infection at a veterans hospital; 1979 to 1987. Infect Control Hosp Epidemiol . 1989; 10:455-464.Crossref 25. Erratum: Infect Control Hosp Epidemiol . 1990;11:62.Crossref 26. Winston DJ, Dudnick DV, Chapin M. Coagulase-negative staphycoccal bacteremia in patients receiving immunosuppressive therapy. Arch Intern Med . 1983; 143:32-36.Crossref 27. Stillman RI, Wenzel RP, Donowitz LC. Emergence of coagulase negative staphylococci as major nosocomial bloodstream pathogens. Infect Control . 1987;8: 108-112. 28. Scheckler WE, Scheibel W, Kresge D. Temporal trends in septicemia in a community hospital. Am J Med . 1991;91 ( (suppl 3B) ):90S-94S.Crossref 29. Freeman J, Platt R, Sidebottom DG, Leclair JM, Epstein MF, Goldmann DA. Coagulase-negative staphylococcal bacteremia in the changing neonatal intensive care unit population: is there an epidemic? JAMA . 1987;258:2548-2552.Crossref 30. Ponce de Leon S, Wenzel RP. Hospital-acquired bloodstream infections with Staphylococcus epidermidis. Am J Med . 1984;77:639-644.Crossref 31. Dominguez-de Villota E, Algora-Weber A, Millian I, Rubio JJ, Galdos P, Mosquera JM. Early evaluation of coagulase negative staphylococcus in blood samples of intensive care unit patients: a clinically uncertain judgement. Intensive Care Med . 1987;13:390-394.Crossref 32. Martin MA, Pfaller MA, Wenzel RP. Coagulase-negative staphylococcal bacteremia: mortality and hospital stay. Ann Intern Med . 1989;110:9-16.Crossref 33. Baumgart S, Hall SE, Campos JM. Sepsis with coagulase-negative staphylococci in critically ill newborns. AJDC . 1983;137:461-463. 34. Donowitz LG, Haley CE, Gregory WW, Wenzel RP. Neonatal intensive care unit bacteremia: emergence of gram-positive bacteria as major pathogens. Am J Infect Control . 1987;15:141-147.Crossref 35. Gaynes RP, Martone WJ, Culver DH, et al. Comparison of rates of nosocomial infections in neonatal intensive care units in the United States: National Nosocomial Infections Surveillance System. Am J Med . 1991;91 ( (suppl 3B) ):192S-196S.Crossref 36. Boo NY, Wong YH, Lim VK. Pattern of neonatal septicemia in a Malaysian maternity hospital. Med J Malaysia . 1989;44:189-193. 37. Pittet D, Herwaldt LA, Massanari RM, The Intensive Care Unit. In: Brachman PS, Bennett JV, eds. Hospital Infections . 3rd ed. Boston, Mass: Little Brown & Co Inc; 1992:405-439. 38. Sidebottom DG, Freeman J, Platt R, Epstein MF, Goldmann DA. Fifteen-year experience with bloodstream isolates of coagulase-negative staphylococci in neonatal intensive care. J Clin Microbiol . 1988;26:713-718. 39. Freeman J, Platt R, Epstein MF, Smith NE, Sidebottom DG, Goldmann DA. Birth weight and length of stay as determinants of nosocomial coagulase-negative staphylococcal bacteremia in neonatal intensive care unit populations: potential for confounding. Am J Epidemiol . 1990;132:1130-1140. 40. McGowan JE Jr. Changing etiology of nosocomial bacteremia and fungemia and other hospital-acquired infections. Rev Infect Dis . 1985;7( (suppl 3) ):S357-S370.Crossref 41. Landry SL, Kaiser DL, Wenzel RP. Hospital stay and mortality attributed to nosocomial enterococcal bacteremia: a controlled study. Am J Infect Control . 1989;17:323-329.Crossref 42. Maki DG, Agger WA. Enterococcal bacteremia: clinical features, the risk of endocarditis, and management. Medicine (Baltimore) . 1988;67:248-269.Crossref 43. Barrall DT, Kenney PR, Slotman GJ, Burchart KW. Enterococcal bacteremia in surgical patients. Arch Surg . 1985;120:57-63.Crossref 44. Maksymiuk AW, Thongprasert S, Hopfer R, Luna M, Fainstein V, Bodey GP. Systemic candidiasis in cancer patients. Am J Med . 1984;77:20-27. 45. Horn R, Wong B, Kiehn TE, Armstrong D. Fungemia in a cancer hospital: changing frequency, earlier onset, and results of therapy. Rev Infect Dis . 1985;7: 646-655.Crossref 46. Wey SB. Mori M, Pfaller MA, Woolson RF, Wenzel RP. Risk factors for hospital-acquired candidemia: a matched case-control study. Arch Intern Med . 1989; 149:2349-2353.Crossref 47. Bross J, Talbot GH, Maislin G, Hurwits S, Strom BL. Risk factors for nosocomial candidemia: a case-control study in adults without leukemia. Am J Med . 1989;87:614-620.Crossref 48. Richet HM, Andremont A, Tancrede C, Pico JL, Jarvis WR. Risk factors for candidemia in patients with acute lymphocytic leukemia. Rev Infect Dis . 1991; 13:211-215.Crossref 49. Pittet D, Monod M, Suter PM, Frenk E, Auckenthaler R. Candida colonization and subsequent infections in critically ill surgical patients. Ann Surg . 1994; 220:751-758.Crossref 50. Bodey GP, Nies BA, Freireich EJ. Multiple organism septicemia in acute leukemia. Arch Intern Med . 1985;116:266-272.Crossref 51. Whimbey E, Kiehn TE, Brannon P, Blevins A, Armstrong D. Bacteremia and fungemia in patients with neoplastic disease. Am J Med . 1987;82:723-730.Crossref 52. Eltlng LS, Bodey GP, Fainstein V. Polymicrobial septicemia in cancer patient. Medicine (Baltimore) . 1990;69:296-306. 53. Terpenning MS. Anaerobic bacteremia in the elderly. Gerontology . 1989;35: 130-136.Crossref 54. Muder RR, Brennen C, Wagener MM, Goetz AM. Bacteremia in long-term-care facility: a five-year prospective study of 163 consecutive episodes. Clin Infect Dis . 1992;14:647-654.Crossref 55. Faix RG, Kovarik SM. Polymicrobial sepsis among intensive care nursery infants. J Perinatol . 1989;9:131-136. 56. Bryant RE, Hood AF, Hood CE, Koenig MG. Factors affecting mortality of gram-negative bacteremia. Arch Intern Med . 1971;127:120-128.Crossref 57. Weinstein MP, Reller LB, Murphy JR. Clinical importance of polymicrobial bacteremia. Diagn Microbiol Infect Dis . 1986;5:185-196.Crossref 58. Pittet D, Li N, Wenzel RP. Association of secondary and polymicrobial nosocomial bloodstream infections with higher mortality. Eur J Clin Microbiol Infect Dis . 1993;12:813-819.Crossref 59. Saviteer SM, Samsa GP, Rutala WA. Nosocomial infections in the elderly: increased risk per hospital day. Am J Med . 1988;4:661-666.Crossref 60. Pittet D, Omahen J, Tarara D, Wenzel RP. Current risk factors for nosocomial bloodstream infection in a tertiary health care center. In: Programs and abstracts of the 31st Interscience Conference on Antimicrobial Agents and Chemotherapy ; September 29 to October 2, 1991; Chicago, Ill. Abstract 800. 61. Donowitz LG, Wenzel RP, Hoyt JW. High risk of hospital-acquired infection in the ICU patient. Crit Care Med . 1982;10:355-357.Crossref 62. Daschner FD, Frey P, Wolff G, Baumann PC, Suter P. Nosocomial infections in intensive care wards: a multicenter prospective study. Intensive Care Med . 1982; 8:5-9.Crossref 63. Pittet D, Tarara D, Wenzel RP. Nosocomial bloodstream infection in critically ill patients: excess length of stay, extra costs, and attributable mortality. JAMA . 1994;271:1598-1601.Crossref 64. Centers for Disease Control. Advance report of final mortality statistics, 1989. Monthly Vital Stat Rep . 1992;40:1-13. 65. McGowan JE Jr, Barnes MW, Finland M. Bacteremia at Boston City Hospital: occurrence and mortality during 12 selected years (1935-1972) with special reference to hospital-acquired cases. J Infect Dis . 1975;132:316-335.Crossref http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Archives of Internal Medicine American Medical Association

Nosocomial Bloodstream Infections: Secular Trends in Rates, Mortality, and Contribution to Total Hospital Deaths

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References (71)

Publisher
American Medical Association
Copyright
Copyright © 1995 American Medical Association. All Rights Reserved.
ISSN
0003-9926
eISSN
1538-3679
DOI
10.1001/archinte.1995.00430110089009
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Abstract

Abstract Background: Nosocomial bloodstream infections occur at a rate of 1.3 to 14.5 per 1000 hospital admissions and are believed to lead directly to 62 500 deaths per year in the United States. Measures of the incidence and the proportion of all hospital deaths related to deaths from these infections provide estimates of their impact. The objectives of the study were to characterize the secular trends in nosocomial bloodstream infection at a single institution and to estimate the population-attributable risk for death among patients experiencing the infection. Methods: A 12-year retrospective study using prospectively collected data from a hospital-wide surveillance system for nosocomial infections in a 900-bed tertiary care institution. All patients (N=260 834) admitted to the institution between 1980 and 1992 were included in the study. Bloodstream infection rates were calculated for the 10 leading groups of pathogens, and trends were analyzed using simple linear regression. In-hospital mortality rates from patients who did or did not develop nosocomial bloodstream infections were compared. Results: Between 1980 and 1992, a total of 3077 patients developed 3464 episodes of nosocomial bloodstream infection. The crude infection rates increased linearly from 6.7 to 18.4 per 1000 discharges (0.83 to 1.72 episodes per 1000 patient-days) during the 12-year study period (r=.87). Increases in the infection rates were due to gram-positive cocci (r=.96) and yeasts (r=.95) and essentially explained by infections caused by coagulase-negative staphylococci, Staphylococcus aureus, enterococci, and Candida species, respectively. Although the crude mortality in patients with nosocomial bloodstream infections decreased from 51% in 1981 to 29% in 1992, the in-hospital population-attributable mortality among infected patients increased from 3.55 deaths per 1000 discharges in 1981 to 6.22 per 1000 discharges in 1992 (r=.67). The etiologic fraction or the proportion of deaths in patients with bloodstream infection to all deaths occurring in the hospital increased from 11.4% in 1981 to 20.4% in 1992 (r=.59). Conclusions: The incidence, the etiologic fraction, and the population-attributable risk for death among patients experiencing nosocomial bloodstream infections increased progressively during the last decade.(Arch Intern Med. 1995;155:1177-1184) References 1. Pittet D. Nosocomial bloodstream infections. In: Wenzel RP, ed. Prevention and Control of Nosocomial Infections . 2nd ed. Baltimore, Md: Williams & Wilkins; 1993:512-555. 2. Maki DG. Nosocomial bacteremia: an epidemiologic overview. Am J Med . 1981; 70:719-732.Crossref 3. Bryan CS, Hornung CA, Reynolds KL, Brenner ER. Endemic bacteremia in Columbia, South Carolina. Am J Epidemiol . 1986;123:113-127. 4. Morrison AJ Jr, Freer CV, Searcy MA, Landry SM, Wenzel RP. Nosocomial bloodstream infections: secular trends in a statewide surveillance program in Virginia. Infect Control . 1986;7:550-553. 5. Filice GA, Van Etta LL, Darby CP, Fraser DW. Bacteremia in Charleston County, South Carolina. Am J Epidemiol . 1986;123:128-136. 6. McLaws M, Gold J, King K, Irwig LM, Berry G. The prevalence of nosocomial and community-acquired infections in Australian hospitals. Med J Aust . 1988; 149:582-590. 7. Banerjee SN, Emori TG, Culver DH, et al. Secular trends in nosocomial primary bloodstream infections in the United States, 1980-1989: National Nosocomial Infections Surveillance System. Am J Med . 1991;91( (suppl 3B) ):86S-89S.Crossref 8. Gatell JM, Trilla A, Latorre X, et al. Nosocomial bacteremia in a large Spanish teaching hospital: analysis of factors influencing prognosis. Rev Infect Dis . 1988;10:203-210.Crossref 9. Centers for Disease Control. Increase in national hospital discharge survey rates for septicemia—United States. MMWR Morb Mortal Wkly Rep . 1990;39:31-34. 10. Centers for Disease Control and Prevention. Annual summary of births, marriages, divorces, and deaths: United States, 1993. Monthly Vital Stat Rep . 1994; 42:4-10. 11. Roberts FJ, Geere IW, Coldman A. A three-year study of positive blood cultures, with emphasis on prognosis. Rev Infect Dis . 1991;13:34-46.Crossref 12. Weinstein MP, Murphy JR, Reller LB, Lichtenstein KA. The clinical significance of positive blood cultures: a comprehensive analysis of 500 episodes of bacteremia and fungemia in adults, II: clinical observations, with special reference to factors influencing prognosis. Rev Infect Dis . 1983;5:54-70.Crossref 13. Bryan CS, Reynolds KL, Brenner ER. Analysis of 1186 episodes of gram-negative bacteremia in non-university hospitals: the effects of antimicrobial therapy. Rev Infect Dis . 1983;5:629-638.Crossref 14. Broderick A, Mori M, Nettleman MD, Streed SA, Wenzel RP. Nosocomial infections: validation of surveillance and computer modeling to identify patients at risk. Am J Epidemiol . 1990;131:734-742. 15. Garner JS, Jarvis WR, Emori TG. CDC definition for nosocomial infections. Am J Infect Control . 1988;16:128-140.Crossref 16. Weinstein MP, Reller LB, Murphy JR, Lichtenstein KA. The clinical significance of positive blood cultures: a comprehensive analysis of 500 episodes of bacteremia and fungemia in adults, I: laboratory and epidemiologic observations. Rev Infect Dis . 1983;5:35-53.Crossref 17. Roberts FJ. Definition of polymicrobial bacteremia. Rev Infect Dis . 1989;11: 1029-1030.Crossref 18. Miettinen OS. Proportions of disease caused or prevented by a given exposure, threat, or intervention. Am J Epidemiol . 1974;99:325-332. 19. Kesley JL, Thompson WD, Evans AS. Methods in Observational Epidemiology . New York, NY: Oxford University Press; 1986:3. 20. Bone RC. A critical evaluation of new agents for the treatment of sepsis. JAMA . 1991;266:1686-1691.Crossref 21. Bone RC. Toward an epidemiology and natural history of SIRS (systemic inflammatory response syndrome). JAMA . 1992;268:3452-3455.Crossref 22. Koontz FP, Flint KK, Reynolds JK, Allen SD. Multicenter comparison of the high volume (10 ml) NR BACTEC PLUS system and the standard (5 ml) NR BACTEC system. Diagn Microbiol Infect Dis . 1991;14:111-118.Crossref 23. Wenzel RP. The mortality of hospital-acquired bloodstream infections: need for a new vital statistic? Int J Epidemiol . 1988;17:225-227.Crossref 24. Mylotte JM, White D, McDermott C, Hodan C. Nosocomial bloodstream infection at a veterans hospital; 1979 to 1987. Infect Control Hosp Epidemiol . 1989; 10:455-464.Crossref 25. Erratum: Infect Control Hosp Epidemiol . 1990;11:62.Crossref 26. Winston DJ, Dudnick DV, Chapin M. Coagulase-negative staphycoccal bacteremia in patients receiving immunosuppressive therapy. Arch Intern Med . 1983; 143:32-36.Crossref 27. Stillman RI, Wenzel RP, Donowitz LC. Emergence of coagulase negative staphylococci as major nosocomial bloodstream pathogens. Infect Control . 1987;8: 108-112. 28. Scheckler WE, Scheibel W, Kresge D. Temporal trends in septicemia in a community hospital. Am J Med . 1991;91 ( (suppl 3B) ):90S-94S.Crossref 29. Freeman J, Platt R, Sidebottom DG, Leclair JM, Epstein MF, Goldmann DA. Coagulase-negative staphylococcal bacteremia in the changing neonatal intensive care unit population: is there an epidemic? JAMA . 1987;258:2548-2552.Crossref 30. Ponce de Leon S, Wenzel RP. Hospital-acquired bloodstream infections with Staphylococcus epidermidis. Am J Med . 1984;77:639-644.Crossref 31. Dominguez-de Villota E, Algora-Weber A, Millian I, Rubio JJ, Galdos P, Mosquera JM. Early evaluation of coagulase negative staphylococcus in blood samples of intensive care unit patients: a clinically uncertain judgement. Intensive Care Med . 1987;13:390-394.Crossref 32. Martin MA, Pfaller MA, Wenzel RP. Coagulase-negative staphylococcal bacteremia: mortality and hospital stay. Ann Intern Med . 1989;110:9-16.Crossref 33. Baumgart S, Hall SE, Campos JM. Sepsis with coagulase-negative staphylococci in critically ill newborns. AJDC . 1983;137:461-463. 34. Donowitz LG, Haley CE, Gregory WW, Wenzel RP. Neonatal intensive care unit bacteremia: emergence of gram-positive bacteria as major pathogens. Am J Infect Control . 1987;15:141-147.Crossref 35. Gaynes RP, Martone WJ, Culver DH, et al. Comparison of rates of nosocomial infections in neonatal intensive care units in the United States: National Nosocomial Infections Surveillance System. Am J Med . 1991;91 ( (suppl 3B) ):192S-196S.Crossref 36. Boo NY, Wong YH, Lim VK. Pattern of neonatal septicemia in a Malaysian maternity hospital. Med J Malaysia . 1989;44:189-193. 37. Pittet D, Herwaldt LA, Massanari RM, The Intensive Care Unit. In: Brachman PS, Bennett JV, eds. Hospital Infections . 3rd ed. Boston, Mass: Little Brown & Co Inc; 1992:405-439. 38. Sidebottom DG, Freeman J, Platt R, Epstein MF, Goldmann DA. Fifteen-year experience with bloodstream isolates of coagulase-negative staphylococci in neonatal intensive care. J Clin Microbiol . 1988;26:713-718. 39. Freeman J, Platt R, Epstein MF, Smith NE, Sidebottom DG, Goldmann DA. Birth weight and length of stay as determinants of nosocomial coagulase-negative staphylococcal bacteremia in neonatal intensive care unit populations: potential for confounding. Am J Epidemiol . 1990;132:1130-1140. 40. McGowan JE Jr. Changing etiology of nosocomial bacteremia and fungemia and other hospital-acquired infections. Rev Infect Dis . 1985;7( (suppl 3) ):S357-S370.Crossref 41. Landry SL, Kaiser DL, Wenzel RP. Hospital stay and mortality attributed to nosocomial enterococcal bacteremia: a controlled study. Am J Infect Control . 1989;17:323-329.Crossref 42. Maki DG, Agger WA. Enterococcal bacteremia: clinical features, the risk of endocarditis, and management. Medicine (Baltimore) . 1988;67:248-269.Crossref 43. Barrall DT, Kenney PR, Slotman GJ, Burchart KW. Enterococcal bacteremia in surgical patients. Arch Surg . 1985;120:57-63.Crossref 44. Maksymiuk AW, Thongprasert S, Hopfer R, Luna M, Fainstein V, Bodey GP. Systemic candidiasis in cancer patients. Am J Med . 1984;77:20-27. 45. Horn R, Wong B, Kiehn TE, Armstrong D. Fungemia in a cancer hospital: changing frequency, earlier onset, and results of therapy. Rev Infect Dis . 1985;7: 646-655.Crossref 46. Wey SB. Mori M, Pfaller MA, Woolson RF, Wenzel RP. Risk factors for hospital-acquired candidemia: a matched case-control study. Arch Intern Med . 1989; 149:2349-2353.Crossref 47. Bross J, Talbot GH, Maislin G, Hurwits S, Strom BL. Risk factors for nosocomial candidemia: a case-control study in adults without leukemia. Am J Med . 1989;87:614-620.Crossref 48. Richet HM, Andremont A, Tancrede C, Pico JL, Jarvis WR. Risk factors for candidemia in patients with acute lymphocytic leukemia. Rev Infect Dis . 1991; 13:211-215.Crossref 49. Pittet D, Monod M, Suter PM, Frenk E, Auckenthaler R. Candida colonization and subsequent infections in critically ill surgical patients. Ann Surg . 1994; 220:751-758.Crossref 50. Bodey GP, Nies BA, Freireich EJ. Multiple organism septicemia in acute leukemia. Arch Intern Med . 1985;116:266-272.Crossref 51. Whimbey E, Kiehn TE, Brannon P, Blevins A, Armstrong D. Bacteremia and fungemia in patients with neoplastic disease. Am J Med . 1987;82:723-730.Crossref 52. Eltlng LS, Bodey GP, Fainstein V. Polymicrobial septicemia in cancer patient. Medicine (Baltimore) . 1990;69:296-306. 53. Terpenning MS. Anaerobic bacteremia in the elderly. Gerontology . 1989;35: 130-136.Crossref 54. Muder RR, Brennen C, Wagener MM, Goetz AM. Bacteremia in long-term-care facility: a five-year prospective study of 163 consecutive episodes. Clin Infect Dis . 1992;14:647-654.Crossref 55. Faix RG, Kovarik SM. Polymicrobial sepsis among intensive care nursery infants. J Perinatol . 1989;9:131-136. 56. Bryant RE, Hood AF, Hood CE, Koenig MG. Factors affecting mortality of gram-negative bacteremia. Arch Intern Med . 1971;127:120-128.Crossref 57. Weinstein MP, Reller LB, Murphy JR. Clinical importance of polymicrobial bacteremia. Diagn Microbiol Infect Dis . 1986;5:185-196.Crossref 58. Pittet D, Li N, Wenzel RP. Association of secondary and polymicrobial nosocomial bloodstream infections with higher mortality. Eur J Clin Microbiol Infect Dis . 1993;12:813-819.Crossref 59. Saviteer SM, Samsa GP, Rutala WA. Nosocomial infections in the elderly: increased risk per hospital day. Am J Med . 1988;4:661-666.Crossref 60. Pittet D, Omahen J, Tarara D, Wenzel RP. Current risk factors for nosocomial bloodstream infection in a tertiary health care center. In: Programs and abstracts of the 31st Interscience Conference on Antimicrobial Agents and Chemotherapy ; September 29 to October 2, 1991; Chicago, Ill. Abstract 800. 61. Donowitz LG, Wenzel RP, Hoyt JW. High risk of hospital-acquired infection in the ICU patient. Crit Care Med . 1982;10:355-357.Crossref 62. Daschner FD, Frey P, Wolff G, Baumann PC, Suter P. Nosocomial infections in intensive care wards: a multicenter prospective study. Intensive Care Med . 1982; 8:5-9.Crossref 63. Pittet D, Tarara D, Wenzel RP. Nosocomial bloodstream infection in critically ill patients: excess length of stay, extra costs, and attributable mortality. JAMA . 1994;271:1598-1601.Crossref 64. Centers for Disease Control. Advance report of final mortality statistics, 1989. Monthly Vital Stat Rep . 1992;40:1-13. 65. McGowan JE Jr, Barnes MW, Finland M. Bacteremia at Boston City Hospital: occurrence and mortality during 12 selected years (1935-1972) with special reference to hospital-acquired cases. J Infect Dis . 1975;132:316-335.Crossref

Journal

Archives of Internal Medicine – American Medical Association

Published: Jun 12, 1995

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