Epidemiology and burden of multidrug-resistant bacterial infection in a developing country

Cherry Lim, Emi Takahashi, Maliwan Hongsuwan, Vanaporn Wuthiekanun, Visanu Thamlikitkul, Soawapak Hinjoy, Nicholas Pj Day, Sharon J Peacock, Direk Limmathurotsakul, Cherry Lim, Emi Takahashi, Maliwan Hongsuwan, Vanaporn Wuthiekanun, Visanu Thamlikitkul, Soawapak Hinjoy, Nicholas Pj Day, Sharon J Peacock, Direk Limmathurotsakul

Abstract

Little is known about the excess mortality caused by multidrug-resistant (MDR) bacterial infection in low- and middle-income countries (LMICs). We retrospectively obtained microbiology laboratory and hospital databases of nine public hospitals in northeast Thailand from 2004 to 2010, and linked these with the national death registry to obtain the 30-day mortality outcome. The 30-day mortality in those with MDR community-acquired bacteraemia, healthcare-associated bacteraemia, and hospital-acquired bacteraemia were 35% (549/1555), 49% (247/500), and 53% (640/1198), respectively. We estimate that 19,122 of 45,209 (43%) deaths in patients with hospital-acquired infection due to MDR bacteria in Thailand in 2010 represented excess mortality caused by MDR. We demonstrate that national statistics on the epidemiology and burden of MDR in LMICs could be improved by integrating information from readily available databases. The prevalence and mortality attributable to MDR in Thailand are high. This is likely to reflect the situation in other LMICs.

Keywords: Acinetobacter; E. coli; Enterococcus; K. pneumoniae; P. aeruginosa; Staphylococcus aureus; antimicrobial resistant; epidemiology; global health.

Conflict of interest statement

The authors declare that no competing interests exist.

Figures

Figure 1.. Location of participating hospitals.
Figure 1.. Location of participating hospitals.
These were situated in (1) Nong Khai, (2) Udon Thani, (3) Nakhon Phanom, (4) Chaiyaphum, (5) Mukdahan, (6) Yasothon, (7) Burirum, (8) Sisaket, and (9) Ubon Ratchathani provinces. DOI:http://dx.doi.org/10.7554/eLife.18082.003
Figure 2.. Trends in proportions of Staphylococcus…
Figure 2.. Trends in proportions of Staphylococcus aureus bacteraemia being caused by MRSA in Northeast Thailand.
(A) community-acquired, (B) healthcare-associated and (C) hospital-acquired Staphylococcus aureus bacteraemia. DOI:http://dx.doi.org/10.7554/eLife.18082.005
Figure 3.. Trends in proportions of Escherichia…
Figure 3.. Trends in proportions of Escherichia coli bacteraemia being caused by E. coli non-susceptible to extended-spectrum cephalosporins in Northeast Thailand.
(A) community-acquired, (B) healthcare-associated and (C) hospital-acquired E. coli bacteraemia. DOI:http://dx.doi.org/10.7554/eLife.18082.007
Figure 4.. Trends in proportions of Klebsiella…
Figure 4.. Trends in proportions of Klebsiella pneumoniae bacteraemia being caused by K. pneumoniae non-susceptible to extended-spectrum cephalosporins in Northeast Thailand.
(A) community-acquired, (B) healthcare-associated and (C) hospital-acquired K. pneumoniae bacteraemia. DOI:http://dx.doi.org/10.7554/eLife.18082.010
Figure 5.. Trends in proportions of Pseudomonas…
Figure 5.. Trends in proportions of Pseudomonas aeruginosa bacteraemia being caused by P. aeruginosa non-susceptible to carbapenem in Northeast Thailand.
(A) community-acquired, (B) healthcare-associated and (C) hospital-acquired Pseudomonas aeruginosa bacteraemia. DOI:http://dx.doi.org/10.7554/eLife.18082.012
Figure 6.. Trends in proportions of Acinetobacter…
Figure 6.. Trends in proportions of Acinetobacter spp bacteraemia being caused by Acinetobacter spp non-susceptible to carbapenem in Northeast Thailand.
(A) community-acquired, (B) healthcare-associated and (C) hospital-acquired Acinetobacter spp bacteraemia. DOI:http://dx.doi.org/10.7554/eLife.18082.014
Figure 7.. Forest plot of mortality in…
Figure 7.. Forest plot of mortality in patients with MDR bacteraemia compared with non-MDR bacteraemia in Northeast Thailand.
(A) Community-acquired bacteraemia. (B) Healthcare-associated bacteraemia. (C) Hospital-acquired bacteraemia. DOI:http://dx.doi.org/10.7554/eLife.18082.016

References

    1. Ansari S, Nepal HP, Gautam R, Shrestha S, Neopane P, Gurung G, Chapagain ML. Community acquired multi-drug resistant clinical isolates of Escherichia coli in a tertiary care center of Nepal. Antimicrobial Resistance and Infection Control. 2015;4:15. doi: 10.1186/s13756-015-0059-2.
    1. Benichou J. A review of adjusted estimators of attributable risk. Statistical Methods in Medical Research. 2001;10:195–216. doi: 10.1191/096228001680195157.
    1. Bursac Z, Gauss CH, Williams DK, Hosmer DW. Purposeful selection of variables in logistic regression. Source Code for Biology and Medicine. 2008;3:17. doi: 10.1186/1751-0473-3-17.
    1. Center for Disease Controls and Prevention, U.S. Department of Health and Human Services Antibiotic resistance threats in the United States, 2013. 2013
    1. Cuellar LE, Fernandez-Maldonado E, Rosenthal VD, Castaneda-Sabogal A, Rosales R, Mayorga-Espichan MJ, Camacho-Cosavalente LA, Castillo-Bravo LI. Device-associated infection rates and mortality in intensive care units of Peruvian hospitals: findings of the International Nosocomial Infection Control Consortium. Revista Panamericana De Salud Pública. 2008;24:16–24. doi: 10.1590/S1020-49892008000700002.
    1. European Centre for Disease Prevention and Control and European Medicines Agency ECDC/EMEA joint technical report the bacterial challenge: Time to react 2009. 2009
    1. Falagas ME, Rafailidis PI. Attributable mortality of Acinetobacter baumannii: no longer a controversial issue. Critical Care. 2007;11:134. doi: 10.1186/cc5911.
    1. Fishbain J, Peleg AY. Treatment of Acinetobacter infections. Clinical Infectious Diseases. 2010;51:79–84. doi: 10.1086/653120.
    1. Greenland S, Robins JM. Conceptual problems in the definition and interpretation of attributable fractions. American Journal of Epidemiology. 1988;128:1185–1197.
    1. Hongsuwan M, Srisamang P, Kanoksil M, Luangasanatip N, Jatapai A, Day NP, Peacock SJ, Cooper BS, Limmathurotsakul D. Increasing incidence of hospital-acquired and healthcare-associated bacteremia in northeast Thailand: a multicenter surveillance study. PLoS ONE. 2014;9:e18082. doi: 10.1371/journal.pone.0109324.
    1. Kanoksil M, Jatapai A, Peacock SJ, Limmathurotsakul D. Epidemiology, microbiology and mortality associated with community-acquired bacteremia in northeast Thailand: a multicenter surveillance study. PLoS ONE. 2013;8:e18082. doi: 10.1371/annotation/e199ebcc-0bc1-4be1-ad91-ad2a8c0c9382.
    1. Kayange N, Kamugisha E, Mwizamholya DL, Jeremiah S, Mshana SE. Predictors of positive blood culture and deaths among neonates with suspected neonatal sepsis in a tertiary hospital, Mwanza-Tanzania. BMC Pediatrics. 2010;10:e18082. doi: 10.1186/1471-2431-10-39.
    1. Kwon KT, Oh WS, Song JH, Chang HH, Jung SI, Kim SW, Ryu SY, Heo ST, Jung DS, Rhee JY, Shin SY, Ko KS, Peck KR, Lee NY. Impact of imipenem resistance on mortality in patients with Acinetobacter bacteraemia. Journal of Antimicrobial Chemotherapy. 2007;59:525–530. doi: 10.1093/jac/dkl499.
    1. Laxminarayan R, Duse A, Wattal C, Zaidi AK, Wertheim HF, Sumpradit N, Vlieghe E, Hara GL, Gould IM, Goossens H, Greko C, So AD, Bigdeli M, Tomson G, Woodhouse W, Ombaka E, Peralta AQ, Qamar FN, Mir F, Kariuki S, Bhutta ZA, Coates A, Bergstrom R, Wright GD, Brown ED, Cars O. Antibiotic resistance-the need for global solutions. The Lancet Infectious Diseases. 2013;13:1057–1098. doi: 10.1016/S1473-3099(13)70318-9.
    1. Magiorakos AP, Srinivasan A, Carey RB, Carmeli Y, Falagas ME, Giske CG, Harbarth S, Hindler JF, Kahlmeter G, Olsson-Liljequist B, Paterson DL, Rice LB, Stelling J, Struelens MJ, Vatopoulos A, Weber JT, Monnet DL. Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. Clinical Microbiology and Infection. 2012;18:268–281. doi: 10.1111/j.1469-0691.2011.03570.x.
    1. Martone WJ, Jarvis WR, Edwards JR, Culver DH, Haley RW. Incidence and nature of endemic and epidemic nosocomial infections. In: Bennett J. V, Brachman P. S, editors. Hospital Infections. 4th ed. Philadelphia, PA, USA: Lippincott-Raven; 1998. pp. 461–476.
    1. Moine P, Timsit JF, De Lassence A, Troché G, Fosse JP, Alberti C, Cohen Y, OUTCOMEREA study group Mortality associated with late-onset pneumonia in the intensive care unit: results of a multi-center cohort study. Intensive Care Medicine. 2002;28:154–163. doi: 10.1007/s00134-001-1172-7.
    1. Moreno CA, Rosenthal VD, Olarte N, Gomez WV, Sussmann O, Agudelo JG, Rojas C, Osorio L, Linares C, Valderrama A, Mercado PG, Bernate PH, Vergara GR, Pertuz AM, Mojica BE, Navarrete MP, Romero AS, Henriquez D. Device-associated infection rate and mortality in intensive care units of 9 Colombian hospitals: findings of the International Nosocomial Infection Control Consortium. Infection Control and Hospital Epidemiology. 2006;27:349–356. doi: 10.1086/503341.
    1. Munoz-Price LS, Weinstein RA. Acinetobacter infection. New England Journal of Medicine. 2008;358:1271–1281. doi: 10.1056/NEJMra070741.
    1. National Committee for Clinical Laboratory Standards . NCCLS Document M100-514. Wayne Pa: National Committee for Clinical Laboratory Standards; 2004. Performance Standards for Antimicrobial Disk Susceptibility Tests.
    1. Nguile-Makao M, Zahar JR, Français A, Tabah A, Garrouste-Orgeas M, Allaouchiche B, Goldgran-Toledano D, Azoulay E, Adrie C, Jamali S, Clec'h C, Souweine B, Timsit JF. Attributable mortality of ventilator-associated pneumonia: respective impact of main characteristics at ICU admission and VAP onset using conditional logistic regression and multi-state models. Intensive Care Medicine. 2010;36:781–789. doi: 10.1007/s00134-010-1824-6.
    1. Nhu NT, Lan NP, Campbell JI, Parry CM, Thompson C, Tuyen HT, Hoang NV, Tam PT, Le VM, Nga TV, Nhu TH, Van Minh P, Nga NT, Thuy CT, Dung le T, Yen NT, Van Hao N, Loan HT, Yen LM, Nghia HD, Hien TT, Thwaites L, Thwaites G, Chau NV, Baker S. Emergence of carbapenem-resistant Acinetobacter baumannii as the major cause of ventilator-associated pneumonia in intensive care unit patients at an infectious disease hospital in southern Vietnam. Journal of Medical Microbiology. 2014;63:1386–1394. doi: 10.1099/jmm.0.076646-0.
    1. Opartkiattikul N, Bejrachandra S. The external quality assessment schemes in Thailand. Rinsho Byori. the Japanese Journal of Clinical Pathology. 2002;50:121–125.
    1. Peleg AY, Hooper DC. Hospital-acquired infections due to gram-negative bacteria. New England Journal of Medicine. 2010;362:1804–1813. doi: 10.1056/NEJMra0904124.
    1. Pumart P, Phodha T, Thamlikitkul V, Riewpaiboon A, Prakongsai P, Limwattananon S. Health and economic impacts of antimicrobial resistance in Thailand. Journal Health Services Research Policy. 2012;9:352–360.
    1. Roberts RR, Hota B, Ahmad I, Scott RD, Foster SD, Abbasi F, Schabowski S, Kampe LM, Ciavarella GG, Supino M, Naples J, Cordell R, Levy SB, Weinstein RA. Hospital and societal costs of antimicrobial-resistant infections in a Chicago teaching hospital: implications for antibiotic stewardship. Clinical Infectious Diseases. 2009;49:1175–1184. doi: 10.1086/605630.
    1. Rosenthal VD, Guzman S, Orellano PW. Nosocomial infections in medical-surgical intensive care units in Argentina: attributable mortality and length of stay. American Journal of Infection Control. 2003;31:291–295. doi: 10.1067/mic.2003.1.
    1. Rosenthal VD, Maki DG, Mehta Y, Leblebicioglu H, Memish ZA, Al-Mousa HH, Balkhy H, Hu B, Alvarez-Moreno C, Medeiros EA, Apisarnthanarak A, Raka L, Cuellar LE, Ahmed A, Navoa-Ng JA, El-Kholy AA, Kanj SS, Bat-Erdene I, Duszynska W, Van Truong N, Pazmino LN, See-Lum LC, Fernández-Hidalgo R, Di-Silvestre G, Zand F, Hlinkova S, Belskiy V, Al-Rahma H, Luque-Torres MT, Bayraktar N, Mitrev Z, Gurskis V, Fisher D, Abu-Khader IB, Berechid K, Rodríguez-Sánchez A, Horhat FG, Requejo-Pino O, Hadjieva N, Ben-Jaballah N, García-Mayorca E, Kushner-Dávalos L, Pasic S, Pedrozo-Ortiz LE, Apostolopoulou E, Mejía N, Gamar-Elanbya MO, Jayatilleke K, de Lourdes-Dueñas M, Aguirre-Avalos G, International Nosocomial Infection Control Consortium International Nosocomial Infection Control Consortium (INICC) report, data summary of 43 countries for 2007-2012. Device-associated module. American Journal of Infection Control. 2014;42:942–956. doi: 10.1016/j.ajic.2014.05.029.
    1. World Health Organization Antimicrobial resistance: global report on surveillance. 2014
    1. WorldBank Thailand Overview. 2015

Source: PubMed

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