Antimicrobial resistance of Klebsiella pneumoniae stool isolates circulating in Kenya

PLoS ONE

Volumn 12, Issue 6, 2017, Pages

  Taitt, Chris Rowe ^a   Leski, Tomasz A ^a   Erwin, Daniel P ^b   Odundo, Elizabeth A ^b   Kipkemoi, Nancy C ^b   Ndonye, Janet N ^b   Kirera, Ronald K ^b   Ombogo, Abigael N ^b   Walson, Judd L ^c   Pavlinac, Patricia B ^c   Hulseberg, Christine ^b   Vora, Gary J ^a  

^a NAVAL RESEARCH LABORATORY   (United States)

^b WALTER REED ARMY INSTITUTE OF RESEARCH   (United States)

^c UNIVERSITY OF WASHINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2,4 DIAMINOPYRIMIDINE DERIVATIVE; AMINE; AMINOGLYCOSIDE ANTIBIOTIC AGENT; ANSAMYCIN DERIVATIVE; ANTIBIOTIC AGENT; BETA LACTAM ANTIBIOTIC; BETA LACTAMASE AMPC; CHLORAMPHENICOL; MACROLIDE; QUINOLINE DERIVED ANTIINFECTIVE AGENT; STREPTOTHRICIN; SULFONAMIDE; TETRACYCLINE DERIVATIVE; ANTIINFECTIVE AGENT;

AMPC GENE; ANTIBIOTIC RESISTANCE; ARR GENE; ARTICLE; BACTERIAL GENE; BACTERIUM ISOLATE; CAT4 GENE; CATA1 GENE; CMLA GENE; CMR GENE; CONTROLLED STUDY; DFRA1 GENE; DFRA12 GENE; DFRA13 GENE; DFRA14 GENE; DFRA15 GENE; DFRA16 GENE; DFRA17 GENE; DFRA5 GENE; DFRA7 GENE; DFRA8 GENE; FECES ANALYSIS; FLOR GENE; GENE IDENTIFICATION; KENYA; KLEBSIELLA PNEUMONIAE; MICROARRAY ANALYSIS; MULTIDRUG RESISTANCE; NONHUMAN; PHENOTYPE; POLYMERASE CHAIN REACTION; QNRS GENE; RMTB GENE; SAT2 GENE; SUL1 GENE; SUL2 GENE; SUL3 GENE; ADOLESCENT; ADULT; CHILD; DRUG EFFECTS; FECES; FEMALE; GENETICS; HUMAN; INFANT; ISOLATION AND PURIFICATION; KLEBSIELLA INFECTIONS; MALE; MICROBIOLOGY; MIDDLE AGED; PRESCHOOL CHILD; YOUNG ADULT;

ADOLESCENT; ADULT; ANTI-BACTERIAL AGENTS; CHILD; CHILD, PRESCHOOL; DRUG RESISTANCE, BACTERIAL; FECES; FEMALE; GENES, BACTERIAL; HUMANS; INFANT; KENYA; KLEBSIELLA INFECTIONS; KLEBSIELLA PNEUMONIAE; MALE; MIDDLE AGED; YOUNG ADULT;

EID: 85020209906     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0178880     Document Type: Article

References (64)

1. World Health Organization, http://www.who.int/drugresistance/documents/surveillancereport/en/; 27 May 2015.
2. Global Antibiotic Resistance Partnership-Kenya Working Group. Situational analysis and recommendations Antibiotic use and resistance in Kenya. Washington, DC Center for Disease Dynamics, Economics & Policy. 2011.
3. Thi PLN, Yassibanda S, Aidara A, Le Bouguenec C, Germani Y. Enteropathogenic Klebsiella pneumoniae HIV-Infected Adults, Africa. Emerg Infect Dis. 2003; 9: 135-137.
4. Fung C-P, Lin Y-T, Lin J-C, Chen T-L, Yeh K-M, Chang R-Y, et al. Klebsiella pneumoniae in gastrointestinal tract and pyogenic liver abscess Emerg Infect Dis. 2012; 18: 1322-1325. https://doi.org/10.3201/eid1808.111053
5. Selden R, Lee S, Wang W, Bennett JV, Eickhoff TC. Nosocomial klebsiella infections: intestinal colonization as a reservoir. Ann Intern Med. 1971; 74: 657-664.
6. Martin RM, Cao J, Brisse S, Passet V, Wu W, Zhao L, et al. Molecular epidemiology of colonizing and infecting isolates of Klebsiella pneumoniae. mSphere. 2016; 1: e00261-00216. https://doi.org/10.1128/mSphere.00261-16
7. Wanyiri JW, Kanyi H, Maina S, Wang DE, Ngugi P, O'Connor R, et al. Infectious diarrhoea in antiretroviral therapy-naïve HIV/AIDS patients in Kenya. Trans R Soc Trop Med Hyg. 2013; 107: 631-638. https://doi.org/10.1093/trstmh/trt078
8. Huddleston JR. Horizontal gene transfer in the human gastrointestinal tract: potential spread of antibiotic resistance genes. Infect Drug Resist. 2014; 7: 167-176. https://doi.org/10.2147/IDR.S48820
9. Schjørring S, Krogfelt KA. Assessment of bacterial antibiotic resistance transfer in the gut. Int J Microbiol. 2011; 2011: Article 312956.
10. Salyers AA, Gupta A, Wang Y. Human intestinal bacteria as reservoirs for antibiotic resistance genes. Trends Microbiol. 2004; 12: 412-416. https://doi.org/10.1016/j.tim.2004.07.004
11. Podschun R, Ullmann U. Klebsiella spp. as nosocomial pathogens: epidemiology, taxonomy, typing methods, and pathogenicity factors. Clin Microbiol Rev. 1998; 11: 589-603.
12. Schjorring S, Struve C, Krogfelt KA. Transfer of antimicrobial resistance plasmids from Klebsiella pneumoniae to Escherichia coli in the mouse intestine. J Antimicrob Chemother. 2008; 62: 1086-1093. https://doi.org/10.1093/jac/dkn323
13. Sidjabat HE, Silveira FP, Potoski BA, Abu-Elmagd KM, Adams-Haduch JM, Paterson DL, et al. Interspecies spread of Klebsiella pneumoniae carbapenemase gene in a single patient. Clin Infect Dis. 2009; 49: 1736-1738. https://doi.org/10.1086/648077
14. Gona F, Barbera F, Pasquariello AC, Grossi P, Gridelli B, Mezzatesta ML, et al. In vivo multiclonal transfer of blaKPC-3 from Klebsiella pneumoniae to Escherichia coli in surgery patients. Clin Microbiol Infect. 2014; 20: O633-O635. https://doi.org/10.1111/1469-0691.12577
15. Goren MG, Carmeli Y, Schwaber JM, Chmelnitsky I, Schechner V, Navon-Venezia S. Transfer of carbapenem-resistant plasmid from Klebsiella pneumoniae ST258 to Escherichia coli in patient. Emerg Infect Dis. 2010; 16: 1014-1017. https://doi.org/10.3201/eid1606.091671
16. Guan J, Liu S, Lin Z, Li W, Liu X, Chen D. Severe sepsis facilitates intestinal colonization by extendedspectrum-β-lactamase-producing Klebsiella pneumoniae and transfer of the SHV-18 resistance gene to Escherichia coli during antimicrobial treatment. Antimicrob Agents Chemother. 2014; 58: 1039-1046. https://doi.org/10.1128/AAC.01632-13
17. Pavlinac PB, John-Stewart GC, Naulikha JM, Onchiri FM, Denno DM, Odundo EA, et al. High-risk enteric pathogens associated with HIV-infection and HIV-exposure in Kenyan children with acute diarrhea. AIDS. 2014; 28: 2287-2296. https://doi.org/10.1097/QAD.0000000000000396
18. CLSI. Performance standards for antimicrobial susceptbility testing; twenty-fifth informational supplement. Wayne, PA: Clinical and Laboratory Standards Institute. 2015.
19. Taitt CR, Leski TA, Stockelman M, Craft DW, Zurawski DV, Kirkup BC Jr, et al. Antimicrobial resistance determinants in Acinetobacter baumannii isolates taken from military treatment facilities. Antimicrob Agents Chemother. 2014; 58: 767-781. https://doi.org/10.1128/AAC.01897-13
20. Taitt CR, Leski TA, Heang V, Ford GW, Prouty MG, Newell SW, et al. Antimicrobial resistance genotypes and phenotypes from multidrug-resistant bacterial wound infection isolates in Cambodia. J Glob Antimicrob Resist. 2015; 3: 198-204. https://doi.org/10.1016/j.jgar.2015.05.006
21. Leski TA, Vora GJ, Barrows BR, Pimentel G, House BL, Nicklasson M, et al. Molecular characterization of multidrug resistant hospital isolates using the Antimicrobial Resistance Determinant Microarray. PLOS ONE. 2013; 8: e69507. https://doi.org/10.1371/journal.pone.0069507
22. Magiorakos AP, Srinivasan A, Carey RB, Carmeli Y, Falagas ME, Giske CG, et al. Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: An international expert proposal for interim standard definitions for acquired resistance. Clin Microbiol Infect. 2012; 18: 268-281. https://doi.org/10. 1111/j.1469-0691.2011.03570.x
23. Ford PJ, Avison MB. Evolutionary mapping of the SHV b-lactamase and evidence for two separate IS26-dependent blaSHV mobilization events from the Klebsiella pneumoniae chromosome. J Antimicrob Chemother. 2004; 54: 69-75. https://doi.org/10.1093/jac/dkh251
24. French GL, Shannon KP, Simmons N. Hospital outbreak of Klebsiella pneumoniae resistant to broadspectrum cephalosporins and b-lactam-b-lactamase inhibitor combinations by hyperproduction of SHV-5 b-lactamase. J Clin Microbiol. 1996; 34: 358-363.
25. Shannon K, Williams H, King A, Philipps I. Hyperproduction of TEM-1 β-lactamase in clinical isolates of Escherichia coli serotype O15. FEMS Microbiol Lett. 1990; 67: 319-324.
26. Wu PJ, Shannon K, Phillips I. Mechanisms of hyperproduction of TEM-1 β-lactamase by clinical isolates of Escherichia coli. J Antimicrob Chemother. 1995; 36: 927-939.
27. Garrec H, Drieux-Rouzet L, Golmard JL, Jarlier V, Robert J. Comparison of nine phenotypic methods for detection of extended-spectrum β-lactamase production by Enterobacteriaceae. J Clin Microbiol. 2011; 49: 1048-1057. https://doi.org/10.1128/JCM.02130-10
28. Albrechtova K, Dolejska M, Cizek A, Tausova D, Klimes J, Bebora L, et al. Dogs of nomadic pastoralists in Northern Kenya are reservoirs of plasmid-mediated cepahlosporin-And quinolone-resistant Escherichi coli, including pandemic clone B2-O25-ST131. Antimicrob Agents Chemother. 2012; 56: 4013-4017. https://doi.org/10.1128/AAC.05859-11
29. Kiiru J, Kariuki S, Goddeeris B, Buraye P. Analysis of b-lactamase phenotypes and carriage of selected b-lactamase genes among Escherichia coli strains obtained from Kenyan patients during an 18-year period. BMC Microbiol. 2012; 12: 155. https://doi.org/10.1186/1471-2180-12-155
30. Nguyen MCP, Woerther P-L, Bouvet M, Andremont A, Leclercq R, Canu A. Escherichia coli as reservoir for macrolide resistance genes. Emerg Infect Dis. 2009; 15: 1648-1650. https://doi.org/10.3201/eid1510.090696
31. Kariuki S. Antimicrobial resistance in enteric pathogens in developing countries. In: Sosa AdJ, Byarugaba DK, Amabile-Cuevas CF, Hsueh PR, Kariuki S et al., editors. Antimicrobial Resistance in Developing Countries. New York: Springer; 2010. pp.
32. Nys S, Okeke IN, Kariuki S, Dinant GJ, Driessen C, Stobberingh EE. Antibiotic resistance of faecal Escherichia coli from healthy volunteers from eight developing countries. J Antimicrob Chemother. 2004; 54: 952-955. https://doi.org/10.1093/jac/dkh448
33. Okeke IN, Aboderin OA, Byarugaba DK, Ojo KK, Opintan JA. Growing problem of multidrug-resistant enteric pathogens in Africa. Emerg Infect Dis. 2007; 13: 1640-1646. https://doi.org/10.3201/eid1311. 070674
34. DuPont HL. For the record: A history of the definition & management of travelers' diarrhea. In: Brunette GW, Kozarsky PE, Gershman MD, Magill AJ, Ostroff SM et al., editors. CDC Health Information for International Travel. Atlanta, GA: CDC; 2016. pp.
35. Steffen R, Sack DA, Riopel L, Jiang ZD, Sturchler M, Ericsoon CD, et al. Therapy of travelers' diarrhea with rifaximin on various continents. Am J Gastroenterol. 2003; 98: 1073-1078. https://doi.org/10.1111/j.1572-0241.2003.07283.x
36. Vila J, Vargas M, Casals C, Urassa H, Mshinda H, Schellemberg D, et al. Antimicrobial resistance of diarrheagenic Escherichia coli isolated from children under the age of 5 years from Ifakara, Tanzania. Antimicrob Agents Chemother. 1999; 43: 3022-3024.
37. Frank T, Gautier V, Talarmin A, Bercion R, Arlet G. Characterization of sulphonamide resistance genes and class 1 integron gene cassettes in Enterobacteriaceae, Central African Republic (CAR). J Antimicrob Chemother. 2007; 59: 742-745. https://doi.org/10.1093/jac/dkl538
38. Labar AS, Millman JS, Ruebush E, Opintan JA, Bishar RA, Aboderin AO, et al. Regional dissemination of a trimethoprim-resistance gene cassette via a successful transposable element. PLOS ONE. 2012; 7: e38142. https://doi.org/10.1371/journal.pone.0038142
39. Kiiru J, Butaye P, Goddeeris B, Kariuki S. Analysis for prevalence and physical linkages amongst integrons, ISEcp1, ISCR1, Tn21 and Tn7 encountered in Escherichia coli strains from hospitalized and non-hospitalized patients in Kenya during a 19-year period (1992-2011). BMC Microbiol. 2013; 13: 109. https://doi.org/10.1186/1471-2180-13-109
40. Jaglic Z, Cervinkova D. Genetic basis of resistance to quaternary ammonium compoundsthe qac genes and their role: A review. Vet Med (Praha). 2012; 57: 275-281.
41. Conlan S, Park M, Deming C, Thomas PJ, Young AC, Coleman H, et al. Plasmid dynamics in KPC-positive Klebsiella pneumoniae during long-Term patient colonization. mBio. 2016; 7: e00742-00716. https://doi.org/10.1128/mBio.00742-16
42. van Schaik W. The human gut resistome. Philos Trans R Soc London, Ser B. 2015; 370: 20140087.
43. Mitema ES, Kikuvi GM, Wegener HC, Stohr K. An assessment of antimicrobial consumption in food producing animals in Kenya. J Vet Pharmacol Ther. 2001; 24: 385-390.
44. Ministry of Medical Services and Ministry of Public Health and Sanitation. Kenya essential medicines list. Nairobi: Government of Kenya with the World Health Organization. 2010.
45. Bwakura-Dangarembizi M, Kendall L, Bakeera-Kitaka S, Nahirya-Ntege P, Keishanyu R, Nathoo K, et al. A randomized trial of prolonged co-Trimoxazole in HIV-infected children in Africa. N Engl J Med. 2014; 370: 41-53. https://doi.org/10.1056/NEJMoa1214901
46. Hamel MJ, Greene C, Chiller T, Ouma P, Polyak C, Otieno K, et al. Does cotrimoxazole prophylaxis for the prevention of HIV-Associated opportunistic infections select for resistant pathogens in Kenyan adults? Am J Trop Med Hyg. 2008; 79: 320-330.
47. Nelson N, Joshi M, Kirika R. Antimicrobial resistance: The need for action in the East, Central, and Southern Africa region. Arlington, VA: USAID. 2009.
48. Mwambete KD, Kamuhabwa AAR. Resistance of commensal intestinal Escherichia coli and other enterics to co-Trimoxazole and commonly used antibiotics in HIV/AIDS patients. Clin Microbiol Rev. 2013; 3: 1000134.
49. Kohli R, Omuse G, Revathi G. Antibacterial susceptibility patterns of blood stram isolates in patients investigated at the Aga Khan University Hospital, Nairobi. East Afr Med J. 2010; 87: 74-80.
50. Blomberg S, Jureen R, Manji KP, Tamim BS, Mwakagile DS, Urassa WK, et al. High rate of fatal cases of pediatric septicemia caused by Gram-negative bacteria with extended-spectrum β-lactamases in Dar es Salaam, Tanzania. J Clin Microbiol. 2005;43.
51. Maina D, Revathi G, Kariuki S, Ozwara H. Genotypes and cephalosporin susceptibility in extendedspectrum beta-lactamase producing Enterobacteriacea in the community. J Infect Dev Ctries. 2012; 6: 470-477.
52. Muvunyi CM, Masaisa F, Bayingana C, Mutesa L, Musemakweri A, Muhirwa G, et al. Decreased susceptibility to commonly used antimicrobial agents in bacterial pathogens isolated from urinary tract infections in Rwanda: Need for new antimicrobial guidelines. Am J Trop Med Hyg. 2011; 84: 923-928. https://doi.org/10.4269/ajtmh.2011.11-0057
53. Rogawski ET, Platts-Mills JA, Seidman JC, John S, Mahfuz M, Ulak M, et al. Use of antibiotics in children younger than two years in eight countries: A prospective cohort study. Bull World Health Organ. 2017; 95: 49-61. https://doi.org/10.2471/BLT.16.176123
54. Cameron A, Ewen M, Ross-Degnan D, Ball D, Laing R. Medicine prices, availability, and affordability in 36 developing and middle-income countries: A secondary analysis. The Lancet. 2009; 373: 240-249.
55. Ministry of Medical Services and Ministry of Public Health and Sanitation. Kenya: Service provision assessment survey 2010. Nairobi, Kenya: Ministry of Medical Services and Ministry of Public Health and Sanitation. 2010.
56. World Health Organization. Medicine prices in Kenya. Geneva: World Health Organization. 2004.
57. Okoche D, Asiimwe BB, Katabazi FA, Kato L, Najjuka CF. Prevalence and characterization of carbapenem-resistant Enterobacteriaceae isolated from Mulago National Referral Hospital, Uganda. PLOS ONE. 2015; 10: e0135745. https://doi.org/10.1371/journal.pone.0135745
58. Mushi MF, Mshana SE, Imirzalioglu C, Bwanga F. Carbapenemase genes among multidrug resistant Gram negative clinical isolates from a tertiary hospital in Mwanza, Tanzania. Biomed Res Int. 2014; 2014: 303104. https://doi.org/10.1155/2014/303104
59. Poirel L, Revathi G, Bernabeu S, Nordmann P. Detection of NDM-1-producing Klebsiella pneumoniae in Kenya. Antimicrob Agents Chemother. 2011; 55: 934-936. https://doi.org/10.1128/AAC.01247-10
60. Musembi KP (2016) Drug consumption patterns with clinical and financial implications at Kenyatta National Hospital. Nairobi, Kenya: University of Nairobi.
61. Kariuki S, Okoro C, Kiiru J, Njoroge S, Omuse G, Langridge G, et al. Ceftriaxone-resistant Salmonella enterica serotype Typhimurium sequence type 313 from Kenyan patients is associated with the blaCTXM-15 gene on a novel IncHI2 plasmid. Antimicrob Agents Chemother. 2015; 59: 3133-3139. https://doi. org/10.1128/AAC.00078-15
62. Ruiz J. Mechanisms of resistance to quinolones: Target alterations, decreased accumulation, and DNA gyrase protection. J Antimicrob Chemother. 2003; 51: 1109-1117. https://doi.org/10.1093/jac/dkg222
63. Weigel LM, Steward CD, Tenover FC. gyrA mutations associated with fluoroquinolone resistance in eight species of Enterobacteriaceae. Antimicrob Agents Chemother. 1998; 42: 2661-2667.
64. Sims D, Sudbery I, Ilott NE, Heger A, Ponting CP. Sequencing depth and coverage: key considerations in genomic analyses. Nat Rev Genet. 2014; 15: 121-132. https://doi.org/10.1038/nrg3642