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Environmental contamination across multiple hospital departments with multidrug-resistant bacteria pose an elevated risk of healthcare-associated infections in Kenyan hospitals

Environmental contamination across multiple hospital departments with multidrug-resistant... Background Healthcare-associated infections (HAIs) are often caused by multidrug-resistant (MDR) bacteria contaminating hospital environments which can cause outbreaks as well as sporadic transmission. Methods This study systematically sampled and utilized standard bacteriological culture methods to determine the numbers and types of MDR Enterococcus faecalis/faecium, Staphylococcus aureus, Klebsiella pneumoniae, Acinetobacter baumannii, Pseudomonas aeruginosa, Enterobacter species, and Escherichia coli (ESKAPEE) from high-touch environments of five Kenyan hospitals; level 6 and 5 hospitals (A, B, and C), and level 4 hospitals (D and E), in 2018. Six hundred and seventeen high-touch surfaces across six hospital departments; surgical, general, maternity, newborn, outpatient and pediatric were sampled. Results 78/617 (12.6%) of the sampled high-touch surfaces were contaminated with MDR ESKAPEE; A. baumannii, 23/617 (3.7%), K. pneumoniae, 22/617 (3.6%), Enterobacter species, 19/617 (3.1%), methicillin resistant S. aureus (MRSA), 5/617 (0.8%), E. coli, 5/617 (0.8%), P. aeruginosa, 2/617 (0.3%), and E. faecalis and faecium, 2/617 (0.3%). Items found in patient areas, such as beddings, newborn incubators, baby cots, and sinks were the most frequently contaminated. Level 6 and 5 hospitals, B, 21/122 (17.2%), A, 21/122 (17.2%), and C, 18/136 (13.2%), were more frequently contaminated with MDR ESKAPEE than level 4 hospitals; D, 6/101 (5.9%), and E, 8/131 (6.1%). All the sampled hospital departments were contaminated with MDR ESKAPEE, with high levels observed in newborn, surgical and maternity. All the A. baumannii, Enterobacter species, and K. pneumoniae isolates were non-susceptible to piperacillin, ceftriaxone and cefepime. 22/23 (95.6%) of the A. baumannii isolates were non-susceptible to meropenem. In addition, 5 K. pneumoniae isolates were resistant to all the antibiotics tested except for colistin. Conclusion The presence of MDR ESKAPEE across all the hospitals demonstrated gaps in infection prevention practices (IPCs) that should be addressed. Non-susceptibility to last-line antibiotics such as meropenem threatens the ability to treat infections. *Correspondence: Lillian Musila Lillian.musila@usamru-k.org Full list of author information is available at the end of the article © The Author(s) 2023. 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The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Odoyo et al. Antimicrobial Resistance & Infection Control (2023) 12:22 Page 2 of 9 Keywords Healthcare-associated infections, Hospital environment, Antibiotic resistance, Multi-drug resistance Background Briefly, one level six hospital (B), two level five hospitals Healthcare-associated infections (HAIs) are among the (A and C), and two level four hospitals (D and E) were leading threats to patient safety. Hospital patients are sampled. Hospital B is a 450-bed capacity national refer- often predisposed to infections because of exposure to ral and teaching hospital. Hospitals A and C, with 168 invasive devices during surgical procedures and possibly and 270-bed capacities, respectively, are county referral impaired or underdeveloped immunity [1]. In Kenya, the hospitals, while Hospitals D and E, with 158 and 54-bed prevalence of HAIs is estimated to be 4.4 per 100 patient capacities, respectively, are level four facilities. Three admissions, with the highest rates observed in medical, departments identified by the hospital administration as 5.1%, and pediatric, 4.9%, departments [2]. High rates of having high levels of HAIs were selected for sampling in surgical site infections of up to 9.3% have been reported each hospital. In addition, the outpatient departments of [3]. the five hospitals were sampled. In total, five outpatient Enterococcus faecalis/faecium, Staphylococcus aureus, departments (hospitals A, B, C, D, and E), five pediatric Klebsiella pneumoniae, Acinetobacter baumannii, Pseu- departments (hospitals A, B, C, D and E), four surgical domonas aeruginosa, Enterobacter species, and Esch- departments (hospitals B and E, and two surgical depart- erichia coli (ESKAPEE) pathogens are the leading causes ments in hospital A), three maternity departments (hos- of HAIs globally and in Kenya [4, 5]. Consequently, the pitals C, D and E), three newborn departments (hospitals World Health Organization lists antibiotic-resistant A, B, and D) and two general departments (hospitals D ESKAPEE pathogens as high to critical priority patho- and E) were sampled. gens for research and development of new antibiotics [6]. Infections caused by multi-drug resistant (MDR) Sampling strategy ESKAPEE pathogens are of particular concern as they are Sampling was carried out twice in each of the hospitals, associated with increased mortality and treatment costs between February and September. [7, 8]. 2018. Swabs in neutralizing buffer (NB) (Puritan ESK HAIs are frequently caused by bacterial pathogens that sampling kit, Guilford, ME, USA) were used to sample contaminate hospital environments[9]. These bacteria 617 selected high-touch areas. High-touch areas, as clas- persist in hospital environments through the formation sified in the guidelines for environmental infection con - of biofilms and can withstand desiccation and resist dis - trol in healthcare facilities [16], are surfaces or equipment infection [9, 10]. HAIs arising from contamination of fre- frequently handled by patients and clinicians, thus carry- quently handled hospital surfaces or equipment regarded ing a high risk for transmission of HAIs. For each surface, as high-touch surfaces[11], such as sinks, patients’ beds, one swab was used. The surfaces sampled included items and linens by bacterial pathogens, including; Acineto- and areas close to the patient, such as; intravenous pole bacter baumannii, Staphylococcus aureus, carbapenem- steering handles, intravenous tubing, patient bedding, resistant Enterobacterales, and vancomycin-resistant bed rails, newborn incubators, tray tabletops, baby cots, Enterococcus species, have been reported[12–14]. Micro- bedside tabletops, baby weighing scale, room light switch bial monitoring of these high-touch hospital environ- plates, room inner doorknobs and clinician gowns. Sur- ments can help determine the presence of contaminating faces in the bathroom, such as sinks, handrails, and toilet pathogens and thus aid in implementing targeted infec- flush handles, were also sampled. In addition, equipment, tion prevention practices (IPCs) that may reduce HAIs. including computer keyboards and mice, blood pressure Our previous study determined the overall bacteria levels cuffs, clinician cell phones, stethoscopes, and thermom - in Kenyan hospital environments and identified modifi - eters, were sampled. A sterile square frame measuring able risk factors for improved infection control [15]. This 500cm was used to define the swabbed area, while for study systematically sampled and characterized MDR smaller objects or surfaces, the surface area was approxi- ESKAPEE pathogens contaminating high-touch environ- mated, and the whole surface area was swabbed. Samples ments in five Kenyan hospitals and identified the highest- were collected from clinician uniforms by swabbing the risk departments to target to reduce the risk of HAIs to abdominal region and sleeve cuffs of the uniform. The patients in these hospitals. swabs were then shipped at 4℃ to the testing lab at the Kenya Medical Research Institute (KEMRI), Nairobi, Materials and methods where they were processed within 36 h. Study design This descriptive laboratory-based study was conducted in five hospitals in Kenya, as previously described [ 15]. Odoyo et al. Antimicrobial Resistance & Infection Control (2023) 12:22 Page 3 of 9 Isolation and detection of MDR ESKAPEE pathogens (CLSI) 2017 guidelines. AST-XN05 and AST-P580 cards The NB solution containing the swab was vortexed and were used for gram-negative and gram-positive antimi- 100  µl was inoculated on respective chromogenic agars crobial susceptibility testing, respectively. Staphylococ- (CHROMagar, Paris, France) for isolation and detec- cus aureus 25,923 and Escherichia coli 25,922 were used tion of ESKAPEE pathogens; CHROMagar ESBL for for quality control. Bacterial isolates were categorized as Enterobacterales, CHROMagar MRSA for methicillin MDR if they were non-susceptible to at least one anti- resistant Staphylococcus aureus (MRSA), CHROMagar microbial drug in three or more therapeutically relevant VRE for vancomycin-resistant Enterococcus species and antibacterial classes [17]. CHROMagar Acinetobacter for Acinetobacter bauman- nii. The inoculated plates were incubated aerobically at Statistical analysis 37 °C for 24 h. The target MDR ESKAPEE was identified Data were captured in excel sheets. All statistical analy- by observing the typical growth characteristics on the ses were performed on STATA (StataCorp. 2013. College respective chromogenic agar. Three colonies of the tar - Station, TX, USA). Descriptive statistics were expressed get organisms were sub-cultured on Mueller Hinton agar as percentages. Chi-square Fisher’s exact test was used to (HIMEDIA, Mumbai, India) and incubated for 24  h to determine associations between the numbers and type of obtain pure bacterial isolates. Gram stain was performed contaminating MDR ESKAPEE and the study hospitals for each isolate. Bacterial identification and antimicro - and their departments. A P-value of ≤ 0.05 was consid- bial susceptibility testing were performed on the VITEK ered statistically significant. The hospitals were classified 2 system per Clinical and Laboratory Standards Institute as either higher level; level 6 hospitals (B), level 5 hospi- tals (A and C), or lower level; level 4 hospitals (D and E). Table 1 Distribution of MDR ESKAPEE pathogens on high-touch surfaces Results MDR ESKAPEE No. of isolated High-touch surfaces contami- Recovery of MDR ESKAPEE from the high-touch surfaces MDR ESKAPEE/ nated with the MDR ESKAPEE A total of 617 hospital high-touch surfaces were sampled No. of surfaces pathogens across the five study hospitals. Six hospital departments sampled (%) were sampled, including; surgical, general, maternity, Acinetobacter 23/617 (3.7%) Patient areas; bed rails, nursing newborn, outpatient and pediatric. 78/617 (12.6%) of baumannii chair, department sinks, patient beddings, door knob, tray table the sampled high-touch surfaces across the study hospi- top tals were contaminated with MDR ESKAPEE. The iso - Equipment; intravenous poles lated MDR ESKAPEE pathogens included; A. baumannii, steering handle, suction tube 23/617 (3.7%), K. pneumoniae, 22/617 (3.6%), Enterobac- Bathroom areas; saline bathtub ter species, 19/617 (3.1%), MRSA, 5/617 (0.8%), E. coli, Klebsiella 22/617 (3.6%) Patient areas; bed rails, patient 5/617 (0.8%), P. aeruginosa, 2/617 (0.3%), and Entero- pneumoniae beddings, newborn incubators, department sinks, baby cots, coccus faecalis and faecium, 2/617 (0.3%), (Table  1). A. patient chair baumannii, K. pneumoniae and Enterobacter species Equipment; an oxygen concen- contaminated the widest range of hospital surfaces. The trator dial pad, room light switch most frequently contaminated items were those found in plate patient areas, including patient beddings, newborn incu- Bathroom areas; bathroom sink Enterobacter 19/617 (3.1%) Patient areas; bed rails, baby bators and baby cots, department sinks, door knobs, and species cots, newborn incubators, surgi- tray table tops. MDR ESKAPEE pathogens were also iso- cal table, patient beddings, inner lated from equipment such as intravenous pole steering door knobs, department sinks handles, light switch plates, and a dial pad for a surgical Equipment; dial pad for a surgical table. Bathroom surfaces, bathroom sinks and a saline table bathtub were also contaminated with MDR ESKAPEE. MRSA 5/617 (0.8%) Patient areas; patient beddings, tray table top, bed rail Escherichia coli 5/617 (0.8%) Patient areas; bed rails, cupboard Distribution of MDR ESKAPEE pathogens across the handle, newborn incubator different hospital levels Equipment; light switch plate Higher-level hospitals were more frequently contami- Pseudomonas 2/617 (0.3%) Patient areas; newborn incubator nated with MDR ESKAPEE than lower-level hospitals; aeruginosa Bathroom areas; bathroom sink level 6 hospital B, 21/122 (17.2%), level 5 hospitals A and Enterococcus 2/617 (0.3%) Patient area; newborn incubator C, 21/122 (17.2%), and 18/136 (13.2%), respectively, and faecalis and level 4 hospitals, D, 6/101 (5.9%), and E, 8/131 (6.1%),. Enterococcus faecium There was no significant association between the rates Total 78/617 (12.6%) of contamination of each of the leading contaminants, Odoyo et al. Antimicrobial Resistance & Infection Control (2023) 12:22 Page 4 of 9 Table 2 Distribution of MDR ESKAPEE pathogens across the hospital departments MDR ESKAPEE Newborn Surgical Maternity Pediatric General Outpatient Total (n = 3) (n = 3) (n = 3) (n = 5) (n = 2) (n = 5) Acinetobacter baumannii 2 9 4 6 1 1 23 Klebsiella pneumoniae 8 6 5 1 0 2 22 Enterobacter species 4 3 5 2 2 3 19 Escherichia coli 1 2 0 2 0 0 5 Pseudomonas aeruginosa 1 0 0 0 0 1 2 MRSA 0 1 0 3 0 1 5 Enterococcus faecalis 1 0 0 0 0 0 1 Enterococcus faecium 1 0 0 0 0 0 1 Total 18/70 (25.0%) 21/110 (19.1%) 14/80 (17.5%) 14/119 (11.8%) 3/64 (4.7%) 8/174 78/617 (12.6%) (4.6%) Table 3 Antibiotic susceptibility profiles of the Gram-negative MDR ESKAPEE bacterial pathogens Antimicrobial agent Acinetobacter bauman- Klebsiella pneu- Enterobacter cloacae, Escherichia coli, Pseudomonas nii, n = 23 (%) moniae, n = 22 (%) n = 19 (%) n = 5, (%) aeruginosa, n = 2 (%) NS S NS S NS S NS S NS S Piperacillin 23 (100) 0 22 (100) 0 18 (94.7) 1 (5.3) 4 (80.0) 1 (20.0) 1 (50) 1 (50) Ticarcillin-Clavulanic Acid 23 (100) 0 18 (81.8) 4 (18.2) 18 (94.7) 1 (5.2) 5 (100) 0 2 (100) 0 Cefuroxime nd nd 22 (100) 0 19 (100) 0 4 (80.0) 1 (20.0) nd nd Cefixime nd nd 22 (100) 0 19 (100) 0 4 (80.0) 1 (20.0) nd nd Ceftriaxone 23 (100) 0 22 (100) 0 19 (100) 0 4 (80.0) 1 (20.0) nd nd Cefepime 23 (100) 0 22 (100) 0 19 (100) 0 3 (60.0) 2 (40.0) nd nd Aztreonam nd nd 22 (100) 0 19 (100) 0 3 (60.0) 2 (40.0) nd nd Meropenem 23 (100) 0 5 (22.7) 17 (77.3) 0 19 (100) 0 5 (100) 2 (100) 0 Moxifloxacin nd nd 11 (50.0) 11 (50.0) 3 (15.8) 16 (84.2) 2 (40.0) 3 (60.0) 0 2 (100) Levofloxacin 6 (26.1) 17 (73.9) 10 (45.5) 12 (54.5) 3 (15.8) 16 (84.2) 2 (40.0) 3 (60.0) nd nd Tetracycline 12 (52.2) 11 (47.8) 14 (63.6) 8 (36.4) 16 (84.2) 3 (15.8) 3 (60.0) 2 (40.0) 2 (100) 0 Minocycline 1 (4.3) 22 (95.7) 14 (63.6) 8 (36.4) 15 (78.9) 4 (21.1) 4 (80.0) 1 (20.0) 0 2 (100) Tigecycline 2 (8.7) 21 (91.3) nd nd 0 19 (100) 0 5 (100) 2 (100) 0 Chloramphenicol nd nd 13 (59.1) 9 (40.9) 13 (68.4) 6 (31.6) 2 (40.0) 3 (60.0) nd nd Colistin 0 23 (100) 0 22 (100) 1/ (5.3) 18 (94.7) 0 5 (100) 0 2 (100) Trimethoprim nd nd 21 (95.5) 1 (0.5) 15 (78.9) 4 (21.1) 5 (100) 0 nd nd Abbreviations: NS, non-susceptible (Resistant or Intermediate); S, Susceptible; nd, antimicrobial sensitivity testing not done MDR A. baumannii, MDR K. pneumoniae and MDR Antibiotic susceptibility profiles of the isolated MDR Enterobacter species, with the level of the hospital facil- ESKAPEE isolates ity, P = 0.097, P = 0.721 and P = 0.729, respectively. All the 23 A. baumannii isolates were non-susceptible to piperacillin, 23/23 (100.0%), cefepime, 23/23 (100.0%), Distribution of MDR ESKAPEE pathogens across the and ceftriaxone, 23/23 (100%) (Table  3). 22/23 (95.6%) different hospital departments of the A. baumannii isolates were non-susceptible to Newborn and surgical departments were the most fre- meropenem. All the 22/22 (100.0%) K. pneumoniae iso- quently contaminated with MDR ESKAPEE, 18/70 lates were non-susceptible to; piperacillin, cefepime, (25.0%) and 21/110 (19.1%), respectively (Table  2). A. cefuroxime, cefuroxime-axetil, ceftriaxone, and aztreo- baumannii, K. pneumoniae, and Enterobacter spe- nam. Five of the twenty-two (22.7%) K. pneumoniae iso- cies accounted for 30/37 (81.1%) of MDR ESKAPEE lates were resistant to all the antibiotics tested except contamination in these two departments. Conversely, colistin. In addition, one of the twenty-three (4.4%) A. the outpatient departments, 8/174 (4.6%), and general baumannii isolates was also resistant to all antibiotics departments, 3/64 (4.7%), were the least frequently con- tested except colistin. All the 19/19 (100.0%) Enterobac- taminated with MDR ESKAPEE pathogens. ter species were non-susceptible to piperacillin, cefepime, Odoyo et al. Antimicrobial Resistance & Infection Control (2023) 12:22 Page 5 of 9 cefuroxime, cefuroxime-axetil, ceftriaxone, and aztreo- newborn having the highest rates of 25.0% and 19.1%, nam. 3/5 (60%) of the isolated E. coli were non-suscep- respectively. tible to antibiotics piperacillin, cefepime, cefuroxime, Surgical site infections comprise the largest propor- cefuroxime-axetil, ceftriaxone, aztreonam, minocycline, tion of HAIs in developing countries, with an estimated tetracycline and sulfamethoxazole. All five E. coli isolates incidence of 5.6 per 100 surgical procedures [18]. Cae- were susceptible to meropenem and tigecycline. Both sarian sections are the most common surgical proce- the P. aeruginosa isolates were non-susceptible to ticar- dure in Kenya[19]. Longer durations of labor have been cillin-clavulanic acid and meropenem. At least 3/5 (60%) associated with a higher incidence of surgical site infec- of the isolated MRSA were non-susceptible to cefoxitin, tions following caesarian-section in Kenyan hospitals benzylpenicillin, oxacillin, erythromycin, clindamycin, [20], suggesting a role of the hospital environments in the gentamycin, levofloxacin, moxifloxacin, tetracycline and acquisition of HAIs. The high contamination rate of the trimethoprim-sulfamethoxazole. Both the E. faecium and surgical and maternity departments by MDR ESKAPEE faecalis isolates were non-susceptible to erythromycin, in this study supports this hypothesis. Newborn popula- levofloxacin, tetracycline and nitrofurantoin (Table  4). tions are particularly vulnerable to HAIs because of their immature immunity [1] and the high rate of contamina- Discussion tion of newborn departments by the MDR ESKAPEE in This study sampled high-touch surfaces in five Kenyan this study may explain, in part, the high prevalence of hospitals and found that more than 12.0% were con- HAIs observed in Kenyan pediatric departments [2]. The taminated with MDR ESKAPEE pathogens. There higher levels of MDR ESKAPEE contamination in higher- was a risk of HAIs by MDR ESKAPEE pathogens in all level hospitals than in lower-level hospitals may be linked the hospital departments sampled. In particular, items to increased antibiotics selection pressure resulting from found in patient areas, such as newborn incubators and extensive use, particularly in critical care units or spe- patient beddings, were frequently contaminated, posing cialized departments such as the surgical departments. a high risk of HAIs. Four departments, newborn, surgi- Patients with severe infections, trauma and those referred cal, maternity, and pediatrics, had particularly worrying from lower-level hospitals often seek medical care in contamination rates of at least 10%, with the surgical and higher-level hospitals. These patients often require surgi - cal interventions and the administration of antibiotics for patient care. Table 4 Antibiotic susceptibility profiles of the Gram-positive MDR A. baumannii was the most frequently isolated MDR ESKAPEE bacterial pathogens Antimicrobial agent MRSA, n = 5 (%) E. faecium ESKAPEE pathogen, 23/617 (3.7%) and was found across and E. faeca- all departments. Its ability to form biofilms and with - lis, n = 2 (%) stand desiccation [21, 22] enables it to persist in the hos- NS S NS S pital environment for long periods. Furthermore, it can Cefoxitin 5 (100) 0 nd nd maintain virulence even after prolonged desiccation and Penicillin 5 (100) 0 nd nd starvation [23], which partly explains its ability to cause Oxacillin 5 (100) 0 nd nd frequent and prolonged hospital outbreaks [21]. As a Erythromycin 5 (100) 0 2 (100) 0 result, A. baumannii has been linked to a wide range of Gentamycin 5 (100) 0 nd nd HAIs, including ventilator-associated pneumoniae, skin Clindamycin 5 (100) 0 nd nd and soft tissue infections, urinary tract infections, sec- Linezolid 0 5/5 (100) 0 2 ondary meningitis and bloodstream infections that often (100) affect critically ill patients [ 24], all of which have been Levofloxacin 4 (80) 1/5 (20.0) 2 (100) 0 associated with high mortality rates [25]. Data on the Moxifloxacin 4 (80) 1/5 (20.0) ND nd burden of A. baumannii infections in Kenya is not readily Tetracycline 3 (60) 2/5 (40.0) 2 (100) 0 available. The available data is from facility-based studies, Tigecycline 0 5/5 (100) 0 2 (100) which show that A. baumannii is an important cause of Nitrofurantoin 0 5/5 (100) 2 (100) 0 infections in Kenya [26, 27]. A. baumannii has also been Trimethoprim-sulfamethoxazole 5 (100) 0 nd nd implicated in outbreaks in a teaching hospital in Kenya Teicoplanin 0 5/5 (100) 0 2 [28]. The high frequency of A. baumannii isolation in this (100) study suggests an impending threat of hospital acquired Vancomycin 0 5/5 (100) 0 2 A. baumannii infections. Typically, A. baumannii is (100) intrinsically resistant to commonly prescribed antibiot- Fusidic Acid 0 5/5 (100) nd nd ics, such as first and second-generation cephalosporins, Abbreviations: NS, non-susceptible (Resistant or Intermediate); S, Susceptible; chloramphenicol, and aminopenicillins [25]. Carbape- nd, antimicrobial sensitivity testing not done; MRSA Methicillin resistant S. aureus nem antibiotics are the main treatment option for MDR Odoyo et al. Antimicrobial Resistance & Infection Control (2023) 12:22 Page 6 of 9 A. baumannii infections [25], yet in this study, 22/23 reduce the risk of K. pneumoniae HAIs in the newborn isolates were carbapenem non-susceptible. The use of departments of the study hospitals. Additionally, safe dis- quaternary ammonium compounds-based disposable posal of diapers, cleaning of soiled articles with water and wipes by in-house staff and chlorine-based disinfection is appropriately diluted disinfectants and soap, adherence recommended to reduce contamination of hospital sur- to hand hygiene procedures, and limited staff rotations faces by carbapenem-resistant A. baumannii [29]. Ter- have been successfully employed to contain an outbreak minal cleaning and enhanced cleaning of the high-touch in a neonatal unit [44]. surfaces [30] can help reduce the risk of A. baumannii Enterobacter species are associated primarily with HAIs at the study hospitals. None of the contaminating HAIs [45] and were the third most frequently isolated A. baumannii isolates were resistant to colistin and 22/23 MDR ESKAPEE pathogen in this study, 19/617 (3.1%). were susceptible to minocycline, leaving these agents as It was isolated across all the departments. Third-gen - treatment options for carbapenem-resistant A. bauman- eration cephalosporins are known to induce variants of nii strains [31]. The high rate of carbapenem resistance AmpC beta-lactamases in Enterobacter species, resulting inA. baumanniiisolates reflects an overreliance on car - in resistance [46], and their widespread use in Kenyan bapenem, a last-line antibiotic, for treatingA. baumannii, hospitals [47, 48] could be providing a selective pres- while disregarding first- and second-line options such as sure that favors Enterobacter species and the emergence tetracyclines and fluoroquinolones at the study hospitals. of cephalosporin resistance. Because of innate resistance K. pneumoniae is a significant cause of opportunistic to first and second-generation cephalosporins, treat - HAIs, including; pneumoniae, urinary tract infections, ment of Enterobacter infections is often limited to car- skin and soft tissue infections, septicemia and endocar- bapenems, fluoroquinolones, and aminoglycosides [ 45]. ditis [32]. It is the most common cause of HAIs, includ- Fourth-generation cephalosporins have been used to ing hospital outbreaks, in Kenya and Africa [4, 33]. In treat Enterobacter infections due to their relative stabil- this study, MDR K. pnuemoniae was the second most ity to AmpC beta-lactamases in the absence of extended- frequently isolated MDR ESKAPEE pathogen, 22/617 spectrum beta-lactamases [45]. This study, however, (3.6%). It was isolated from newborn, surgical and mater- found all the Enterobacter isolates resistant to cefepime, nity departments from high-touch items in near-patient a fourth-generation cephalosporin, which further limits areas, bathroom areas, and hospital equipment, reflect - treatment options for Enterobacter infections in the study ing its ubiquitous nature [32] and ability to persist in hospitals. There was, however, a low rate of resistance to the hospital environment by forming biofilms [ 10, 34]. fluoroquinolones, moxifloxacin, and levofloxacin, while Equally important, K. pneumoniae has been implicated meropenem was active against all the Enterobacter iso- in several outbreaks and HAIs in neonatal units [35–38]. lates from the study hospitals. Interestingly, one isolate In Kenya, multi-drug resistant K. pneumoniae has been was resistant to colistin while retaining susceptibility to implicated in an outbreak in a neonatal critical care unit other drug classes, which may be attributed to chromo- of a referral hospital in which six of the thirteen patients somal mutations or acquired resistance genes. However, succumbed, a 46% case fatality rate [39]. Multi-drug- a more reliable colistin test will be necessary to rule out resistant K. pneumoniae was also identified as the com - any false resistance often observed with colistin testing in mon cause of blood-borne infections in newborn units automated platforms. of another referral hospital in Kenya [40]. Indeed, these This study isolated two isolates of P. aeruginosa from reports highlight multi-drug-resistant K. pneumoniae as high-touch surfaces. P. aeruginosa is a common contami- an important cause of HAIs in Kenyan hospitals. There - nant in hospital environments, particularly moist sur- fore, the high contamination rate of surfaces and equip- faces such as sinks and taps [49, 50], which were sampled ment in newborn departments in this study is of grave in this study. The media used to detect P. aeruginosa was concern. All the K. pneumoniae isolates were resistant not the optimal selective media which could have limited to aztreonam and third and fourth-generation cephalo- the ability to detect it from the hospital environment. sporins, ceftriaxone and cefepime, respectively, which Similar to A. baumannii, the two isolates of P. aeruginosa infers the production of extended-spectrum beta-lacta- in this study were resistant to meropenem but retained mases and/or AmpC β-lactamases in addition to other susceptibility to the fluoroquinolone moxifloxacin fur - resistance mechanisms [41]. Additionally, 22.7% of the ther highlighting an overreliance on carbapenem for K. pneumoniae isolates were also resistant to merope- treatment at the study hospitals. Putting carbapenems on nem which infers the production of carbapenemases [42] watch lists and limiting access without approval can help [43]. Resistance to last-line antibiotics such as merope- limit increasing levels of carbapenem resistance in the nem threatens the ability to treat K. pneumoniae HAIs. study hospitals. Enforcing effective terminal cleaning of newborn incuba - At least 3/5 E. coli isolates were non-susceptible to tors and enhanced cleaning of high-touch areas can help third-generation cephalosporins, which may infer the Odoyo et al. Antimicrobial Resistance & Infection Control (2023) 12:22 Page 7 of 9 production of extended-spectrum beta-lactamases. How- practices. In addition, enforcing terminal cleaning of ever, all five isolates of E. coli were susceptible to last-line patients’ beds and newborn incubators, hospital environ- antibiotics such as meropenem and tigecycline. ment biomonitoring around high-touch areas, antibiotic The Gram-positive MDR ESKAPEE pathogens, MRSA stewardship programs, enforced hand hygiene, and ade- and Enterococcus faecalis/faecium, had high levels of quate and frequent cleaning of high-touch areas, as pre- resistance to first-line antibiotics, including erythro - viously described [15] can help reduce the risk of HAIs at mycin, levofloxacin, and tetracycline, while they were the study hospitals. susceptible to last line antibiotics; vancomycin, teico- List of abbreviations planin, and tigecycline. This study isolated MRSA and HAIs Healthcare-associated infections Enterococcus faecalis/faecium mainly from the newborn MDR Multidrug-resistant ESKAPEE Enterococcus faecalis/faecium, Staphylococcus aureus, Klebsiella and pediatric departments, which signifies a high risk pneumoniae, Acinetobacter baumannii, Pseudomonas aeruginosa, of HAIs to these younger patient populations. CHRO- Enterobacter species, and Escherichia coli Magar VRE should ideally limit the growth of contami- IPCs Infection prevention control practices NB Neutralizing buffer nating bacteria and vancomycin-susceptible Enterococcus KEMRI Kenya Medical Research Institute species. Despite this, in this study, the detected isolates CLSI Clinical and Laboratory Standards Institute of the Enterococcus faecalis/faecium were susceptible to WRAIR Walter Reed Army Institute of Research R Resistant vancomycin, indicating that the media may be permis- NS Non-susceptible (Resistant or Intermediate) sive to their growth and antimicrobial sensitivity testing S Susceptible is necessary to confirm whether the recovered isolates nd Antimicrobial sensitivity testing not done are indeed vancomycin-resistant. Gram-negative MDR Acknowledgements ESKAPEE pathogens were isolated in greater num- The authors appreciate the collaboration and support of the study hospital bers than Gram-positive MDR ESKAPEE, which may administration. The authors also appreciate Cliff Momanyi, Ruth Kiage, Mitsanze Thoya, Ruth Mupa, Charles Adega, Gladys Biwott, Alfred Odindo and be linked to IPC practices such as using contaminated Catherine Muriuki for sample collection. cleaning materials, which has been found to mainly replaceram-positive cocci with Gram-negative bacilli Author contributions Funding acquisition: L.M. Conceptualization: L.M., E.O. Investigation: E. O., D.M., [51]. In a previous study conducted in the same hospitals F.T., M.G., C. K., W. M. Data Analysis: E. O. and S.W. Writing – original draft: E. O. [15], storing wet mops was predictive of increased bacte- Writing – review and editing: E. O., L. M. All authors read and approved the rial loads, reflecting that this poor cleaning practice con - final manuscript. tributes to the spread of bacterial contamination. Funding This work was funded by the Armed Forces Health Surveillance Division Study limitations (AFHSD), Global Emerging Infections Surveillance (GEIS) Branch [PROMIS ID 17_KY_1.3.1]. The funders had no role in study design, data collection and Molecular characterization of the isolates from this study analysis, decision to publish, or preparation of the manuscript. would provide more information on the MDR ESKAPEE strain types found within these hospitals. Further, a com- Data Availability All data generated or analyzed during this study are included in this published parison with clinical strains could confirm the trans - article. mission patterns and ascertain that these pathogens are causes of HAIs in the study hospitals. The low rate of Declarations detection of Pseudomonas aeruginosa, a common cause of HAIs [52, 53], may be due to the failure to use a suit- Competing Interests The authors declared that they have no competing interests. able culture media for its detection in the study. Ethical statement Conclusion This study was approved by the KEMRI Scientific and Ethical Review Board, protocol #3482, and the Walter Reed Army Institute of Research ( WRAIR), The widespread presence of MDR ESKAPEE contami - protocol #2416, institutional review boards. Written approval was also nation in the study hospital environments suggests low obtained from the county and hospital administration. No human subjects compliance to IPC practices in Kenyan hospitals, which or animals were involved in this study. Permission has been granted for publication of this manuscript by the Director KEMRI. Material has been are already outstretched by challenges such as poor water reviewed by WRAIR. There is no objection to its publication. The opinions or supply, frequent electricity outages, sporadic supply of assertions contained herein are the private views of the author and are not to critical cleaning reagents and personnel, among others. be construed as official or as reflecting the true views of the Department of Defense. There was a high risk of HAIs by MDR ESKAPEE patho - gens across all the sampled hospitals. Non-susceptibility Author details to last-line antibiotics such as meropenem threatens the United States Army Medical Research Directorate-Africa, P.O. Box 606- 00621, Nairobi, Kenya ability to treat HAIs. The study hospitals could benefit Kenya Medical Research Institute, P.O. Box 54840-00200, Nairobi, Kenya from strengthening diagnostic capacity for antimicrobial 3 Independent researcher, Nairobi, Kenya sensitivity testing for judicious antibiotics prescription Odoyo et al. 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Environmental contamination across multiple hospital departments with multidrug-resistant bacteria pose an elevated risk of healthcare-associated infections in Kenyan hospitals

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Abstract

Background Healthcare-associated infections (HAIs) are often caused by multidrug-resistant (MDR) bacteria contaminating hospital environments which can cause outbreaks as well as sporadic transmission. Methods This study systematically sampled and utilized standard bacteriological culture methods to determine the numbers and types of MDR Enterococcus faecalis/faecium, Staphylococcus aureus, Klebsiella pneumoniae, Acinetobacter baumannii, Pseudomonas aeruginosa, Enterobacter species, and Escherichia coli (ESKAPEE) from high-touch environments of five Kenyan hospitals; level 6 and 5 hospitals (A, B, and C), and level 4 hospitals (D and E), in 2018. Six hundred and seventeen high-touch surfaces across six hospital departments; surgical, general, maternity, newborn, outpatient and pediatric were sampled. Results 78/617 (12.6%) of the sampled high-touch surfaces were contaminated with MDR ESKAPEE; A. baumannii, 23/617 (3.7%), K. pneumoniae, 22/617 (3.6%), Enterobacter species, 19/617 (3.1%), methicillin resistant S. aureus (MRSA), 5/617 (0.8%), E. coli, 5/617 (0.8%), P. aeruginosa, 2/617 (0.3%), and E. faecalis and faecium, 2/617 (0.3%). Items found in patient areas, such as beddings, newborn incubators, baby cots, and sinks were the most frequently contaminated. Level 6 and 5 hospitals, B, 21/122 (17.2%), A, 21/122 (17.2%), and C, 18/136 (13.2%), were more frequently contaminated with MDR ESKAPEE than level 4 hospitals; D, 6/101 (5.9%), and E, 8/131 (6.1%). All the sampled hospital departments were contaminated with MDR ESKAPEE, with high levels observed in newborn, surgical and maternity. All the A. baumannii, Enterobacter species, and K. pneumoniae isolates were non-susceptible to piperacillin, ceftriaxone and cefepime. 22/23 (95.6%) of the A. baumannii isolates were non-susceptible to meropenem. In addition, 5 K. pneumoniae isolates were resistant to all the antibiotics tested except for colistin. Conclusion The presence of MDR ESKAPEE across all the hospitals demonstrated gaps in infection prevention practices (IPCs) that should be addressed. Non-susceptibility to last-line antibiotics such as meropenem threatens the ability to treat infections. *Correspondence: Lillian Musila Lillian.musila@usamru-k.org Full list of author information is available at the end of the article © The Author(s) 2023. Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Odoyo et al. Antimicrobial Resistance & Infection Control (2023) 12:22 Page 2 of 9 Keywords Healthcare-associated infections, Hospital environment, Antibiotic resistance, Multi-drug resistance Background Briefly, one level six hospital (B), two level five hospitals Healthcare-associated infections (HAIs) are among the (A and C), and two level four hospitals (D and E) were leading threats to patient safety. Hospital patients are sampled. Hospital B is a 450-bed capacity national refer- often predisposed to infections because of exposure to ral and teaching hospital. Hospitals A and C, with 168 invasive devices during surgical procedures and possibly and 270-bed capacities, respectively, are county referral impaired or underdeveloped immunity [1]. In Kenya, the hospitals, while Hospitals D and E, with 158 and 54-bed prevalence of HAIs is estimated to be 4.4 per 100 patient capacities, respectively, are level four facilities. Three admissions, with the highest rates observed in medical, departments identified by the hospital administration as 5.1%, and pediatric, 4.9%, departments [2]. High rates of having high levels of HAIs were selected for sampling in surgical site infections of up to 9.3% have been reported each hospital. In addition, the outpatient departments of [3]. the five hospitals were sampled. In total, five outpatient Enterococcus faecalis/faecium, Staphylococcus aureus, departments (hospitals A, B, C, D, and E), five pediatric Klebsiella pneumoniae, Acinetobacter baumannii, Pseu- departments (hospitals A, B, C, D and E), four surgical domonas aeruginosa, Enterobacter species, and Esch- departments (hospitals B and E, and two surgical depart- erichia coli (ESKAPEE) pathogens are the leading causes ments in hospital A), three maternity departments (hos- of HAIs globally and in Kenya [4, 5]. Consequently, the pitals C, D and E), three newborn departments (hospitals World Health Organization lists antibiotic-resistant A, B, and D) and two general departments (hospitals D ESKAPEE pathogens as high to critical priority patho- and E) were sampled. gens for research and development of new antibiotics [6]. Infections caused by multi-drug resistant (MDR) Sampling strategy ESKAPEE pathogens are of particular concern as they are Sampling was carried out twice in each of the hospitals, associated with increased mortality and treatment costs between February and September. [7, 8]. 2018. Swabs in neutralizing buffer (NB) (Puritan ESK HAIs are frequently caused by bacterial pathogens that sampling kit, Guilford, ME, USA) were used to sample contaminate hospital environments[9]. These bacteria 617 selected high-touch areas. High-touch areas, as clas- persist in hospital environments through the formation sified in the guidelines for environmental infection con - of biofilms and can withstand desiccation and resist dis - trol in healthcare facilities [16], are surfaces or equipment infection [9, 10]. HAIs arising from contamination of fre- frequently handled by patients and clinicians, thus carry- quently handled hospital surfaces or equipment regarded ing a high risk for transmission of HAIs. For each surface, as high-touch surfaces[11], such as sinks, patients’ beds, one swab was used. The surfaces sampled included items and linens by bacterial pathogens, including; Acineto- and areas close to the patient, such as; intravenous pole bacter baumannii, Staphylococcus aureus, carbapenem- steering handles, intravenous tubing, patient bedding, resistant Enterobacterales, and vancomycin-resistant bed rails, newborn incubators, tray tabletops, baby cots, Enterococcus species, have been reported[12–14]. Micro- bedside tabletops, baby weighing scale, room light switch bial monitoring of these high-touch hospital environ- plates, room inner doorknobs and clinician gowns. Sur- ments can help determine the presence of contaminating faces in the bathroom, such as sinks, handrails, and toilet pathogens and thus aid in implementing targeted infec- flush handles, were also sampled. In addition, equipment, tion prevention practices (IPCs) that may reduce HAIs. including computer keyboards and mice, blood pressure Our previous study determined the overall bacteria levels cuffs, clinician cell phones, stethoscopes, and thermom - in Kenyan hospital environments and identified modifi - eters, were sampled. A sterile square frame measuring able risk factors for improved infection control [15]. This 500cm was used to define the swabbed area, while for study systematically sampled and characterized MDR smaller objects or surfaces, the surface area was approxi- ESKAPEE pathogens contaminating high-touch environ- mated, and the whole surface area was swabbed. Samples ments in five Kenyan hospitals and identified the highest- were collected from clinician uniforms by swabbing the risk departments to target to reduce the risk of HAIs to abdominal region and sleeve cuffs of the uniform. The patients in these hospitals. swabs were then shipped at 4℃ to the testing lab at the Kenya Medical Research Institute (KEMRI), Nairobi, Materials and methods where they were processed within 36 h. Study design This descriptive laboratory-based study was conducted in five hospitals in Kenya, as previously described [ 15]. Odoyo et al. Antimicrobial Resistance & Infection Control (2023) 12:22 Page 3 of 9 Isolation and detection of MDR ESKAPEE pathogens (CLSI) 2017 guidelines. AST-XN05 and AST-P580 cards The NB solution containing the swab was vortexed and were used for gram-negative and gram-positive antimi- 100  µl was inoculated on respective chromogenic agars crobial susceptibility testing, respectively. Staphylococ- (CHROMagar, Paris, France) for isolation and detec- cus aureus 25,923 and Escherichia coli 25,922 were used tion of ESKAPEE pathogens; CHROMagar ESBL for for quality control. Bacterial isolates were categorized as Enterobacterales, CHROMagar MRSA for methicillin MDR if they were non-susceptible to at least one anti- resistant Staphylococcus aureus (MRSA), CHROMagar microbial drug in three or more therapeutically relevant VRE for vancomycin-resistant Enterococcus species and antibacterial classes [17]. CHROMagar Acinetobacter for Acinetobacter bauman- nii. The inoculated plates were incubated aerobically at Statistical analysis 37 °C for 24 h. The target MDR ESKAPEE was identified Data were captured in excel sheets. All statistical analy- by observing the typical growth characteristics on the ses were performed on STATA (StataCorp. 2013. College respective chromogenic agar. Three colonies of the tar - Station, TX, USA). Descriptive statistics were expressed get organisms were sub-cultured on Mueller Hinton agar as percentages. Chi-square Fisher’s exact test was used to (HIMEDIA, Mumbai, India) and incubated for 24  h to determine associations between the numbers and type of obtain pure bacterial isolates. Gram stain was performed contaminating MDR ESKAPEE and the study hospitals for each isolate. Bacterial identification and antimicro - and their departments. A P-value of ≤ 0.05 was consid- bial susceptibility testing were performed on the VITEK ered statistically significant. The hospitals were classified 2 system per Clinical and Laboratory Standards Institute as either higher level; level 6 hospitals (B), level 5 hospi- tals (A and C), or lower level; level 4 hospitals (D and E). Table 1 Distribution of MDR ESKAPEE pathogens on high-touch surfaces Results MDR ESKAPEE No. of isolated High-touch surfaces contami- Recovery of MDR ESKAPEE from the high-touch surfaces MDR ESKAPEE/ nated with the MDR ESKAPEE A total of 617 hospital high-touch surfaces were sampled No. of surfaces pathogens across the five study hospitals. Six hospital departments sampled (%) were sampled, including; surgical, general, maternity, Acinetobacter 23/617 (3.7%) Patient areas; bed rails, nursing newborn, outpatient and pediatric. 78/617 (12.6%) of baumannii chair, department sinks, patient beddings, door knob, tray table the sampled high-touch surfaces across the study hospi- top tals were contaminated with MDR ESKAPEE. The iso - Equipment; intravenous poles lated MDR ESKAPEE pathogens included; A. baumannii, steering handle, suction tube 23/617 (3.7%), K. pneumoniae, 22/617 (3.6%), Enterobac- Bathroom areas; saline bathtub ter species, 19/617 (3.1%), MRSA, 5/617 (0.8%), E. coli, Klebsiella 22/617 (3.6%) Patient areas; bed rails, patient 5/617 (0.8%), P. aeruginosa, 2/617 (0.3%), and Entero- pneumoniae beddings, newborn incubators, department sinks, baby cots, coccus faecalis and faecium, 2/617 (0.3%), (Table  1). A. patient chair baumannii, K. pneumoniae and Enterobacter species Equipment; an oxygen concen- contaminated the widest range of hospital surfaces. The trator dial pad, room light switch most frequently contaminated items were those found in plate patient areas, including patient beddings, newborn incu- Bathroom areas; bathroom sink Enterobacter 19/617 (3.1%) Patient areas; bed rails, baby bators and baby cots, department sinks, door knobs, and species cots, newborn incubators, surgi- tray table tops. MDR ESKAPEE pathogens were also iso- cal table, patient beddings, inner lated from equipment such as intravenous pole steering door knobs, department sinks handles, light switch plates, and a dial pad for a surgical Equipment; dial pad for a surgical table. Bathroom surfaces, bathroom sinks and a saline table bathtub were also contaminated with MDR ESKAPEE. MRSA 5/617 (0.8%) Patient areas; patient beddings, tray table top, bed rail Escherichia coli 5/617 (0.8%) Patient areas; bed rails, cupboard Distribution of MDR ESKAPEE pathogens across the handle, newborn incubator different hospital levels Equipment; light switch plate Higher-level hospitals were more frequently contami- Pseudomonas 2/617 (0.3%) Patient areas; newborn incubator nated with MDR ESKAPEE than lower-level hospitals; aeruginosa Bathroom areas; bathroom sink level 6 hospital B, 21/122 (17.2%), level 5 hospitals A and Enterococcus 2/617 (0.3%) Patient area; newborn incubator C, 21/122 (17.2%), and 18/136 (13.2%), respectively, and faecalis and level 4 hospitals, D, 6/101 (5.9%), and E, 8/131 (6.1%),. Enterococcus faecium There was no significant association between the rates Total 78/617 (12.6%) of contamination of each of the leading contaminants, Odoyo et al. Antimicrobial Resistance & Infection Control (2023) 12:22 Page 4 of 9 Table 2 Distribution of MDR ESKAPEE pathogens across the hospital departments MDR ESKAPEE Newborn Surgical Maternity Pediatric General Outpatient Total (n = 3) (n = 3) (n = 3) (n = 5) (n = 2) (n = 5) Acinetobacter baumannii 2 9 4 6 1 1 23 Klebsiella pneumoniae 8 6 5 1 0 2 22 Enterobacter species 4 3 5 2 2 3 19 Escherichia coli 1 2 0 2 0 0 5 Pseudomonas aeruginosa 1 0 0 0 0 1 2 MRSA 0 1 0 3 0 1 5 Enterococcus faecalis 1 0 0 0 0 0 1 Enterococcus faecium 1 0 0 0 0 0 1 Total 18/70 (25.0%) 21/110 (19.1%) 14/80 (17.5%) 14/119 (11.8%) 3/64 (4.7%) 8/174 78/617 (12.6%) (4.6%) Table 3 Antibiotic susceptibility profiles of the Gram-negative MDR ESKAPEE bacterial pathogens Antimicrobial agent Acinetobacter bauman- Klebsiella pneu- Enterobacter cloacae, Escherichia coli, Pseudomonas nii, n = 23 (%) moniae, n = 22 (%) n = 19 (%) n = 5, (%) aeruginosa, n = 2 (%) NS S NS S NS S NS S NS S Piperacillin 23 (100) 0 22 (100) 0 18 (94.7) 1 (5.3) 4 (80.0) 1 (20.0) 1 (50) 1 (50) Ticarcillin-Clavulanic Acid 23 (100) 0 18 (81.8) 4 (18.2) 18 (94.7) 1 (5.2) 5 (100) 0 2 (100) 0 Cefuroxime nd nd 22 (100) 0 19 (100) 0 4 (80.0) 1 (20.0) nd nd Cefixime nd nd 22 (100) 0 19 (100) 0 4 (80.0) 1 (20.0) nd nd Ceftriaxone 23 (100) 0 22 (100) 0 19 (100) 0 4 (80.0) 1 (20.0) nd nd Cefepime 23 (100) 0 22 (100) 0 19 (100) 0 3 (60.0) 2 (40.0) nd nd Aztreonam nd nd 22 (100) 0 19 (100) 0 3 (60.0) 2 (40.0) nd nd Meropenem 23 (100) 0 5 (22.7) 17 (77.3) 0 19 (100) 0 5 (100) 2 (100) 0 Moxifloxacin nd nd 11 (50.0) 11 (50.0) 3 (15.8) 16 (84.2) 2 (40.0) 3 (60.0) 0 2 (100) Levofloxacin 6 (26.1) 17 (73.9) 10 (45.5) 12 (54.5) 3 (15.8) 16 (84.2) 2 (40.0) 3 (60.0) nd nd Tetracycline 12 (52.2) 11 (47.8) 14 (63.6) 8 (36.4) 16 (84.2) 3 (15.8) 3 (60.0) 2 (40.0) 2 (100) 0 Minocycline 1 (4.3) 22 (95.7) 14 (63.6) 8 (36.4) 15 (78.9) 4 (21.1) 4 (80.0) 1 (20.0) 0 2 (100) Tigecycline 2 (8.7) 21 (91.3) nd nd 0 19 (100) 0 5 (100) 2 (100) 0 Chloramphenicol nd nd 13 (59.1) 9 (40.9) 13 (68.4) 6 (31.6) 2 (40.0) 3 (60.0) nd nd Colistin 0 23 (100) 0 22 (100) 1/ (5.3) 18 (94.7) 0 5 (100) 0 2 (100) Trimethoprim nd nd 21 (95.5) 1 (0.5) 15 (78.9) 4 (21.1) 5 (100) 0 nd nd Abbreviations: NS, non-susceptible (Resistant or Intermediate); S, Susceptible; nd, antimicrobial sensitivity testing not done MDR A. baumannii, MDR K. pneumoniae and MDR Antibiotic susceptibility profiles of the isolated MDR Enterobacter species, with the level of the hospital facil- ESKAPEE isolates ity, P = 0.097, P = 0.721 and P = 0.729, respectively. All the 23 A. baumannii isolates were non-susceptible to piperacillin, 23/23 (100.0%), cefepime, 23/23 (100.0%), Distribution of MDR ESKAPEE pathogens across the and ceftriaxone, 23/23 (100%) (Table  3). 22/23 (95.6%) different hospital departments of the A. baumannii isolates were non-susceptible to Newborn and surgical departments were the most fre- meropenem. All the 22/22 (100.0%) K. pneumoniae iso- quently contaminated with MDR ESKAPEE, 18/70 lates were non-susceptible to; piperacillin, cefepime, (25.0%) and 21/110 (19.1%), respectively (Table  2). A. cefuroxime, cefuroxime-axetil, ceftriaxone, and aztreo- baumannii, K. pneumoniae, and Enterobacter spe- nam. Five of the twenty-two (22.7%) K. pneumoniae iso- cies accounted for 30/37 (81.1%) of MDR ESKAPEE lates were resistant to all the antibiotics tested except contamination in these two departments. Conversely, colistin. In addition, one of the twenty-three (4.4%) A. the outpatient departments, 8/174 (4.6%), and general baumannii isolates was also resistant to all antibiotics departments, 3/64 (4.7%), were the least frequently con- tested except colistin. All the 19/19 (100.0%) Enterobac- taminated with MDR ESKAPEE pathogens. ter species were non-susceptible to piperacillin, cefepime, Odoyo et al. Antimicrobial Resistance & Infection Control (2023) 12:22 Page 5 of 9 cefuroxime, cefuroxime-axetil, ceftriaxone, and aztreo- newborn having the highest rates of 25.0% and 19.1%, nam. 3/5 (60%) of the isolated E. coli were non-suscep- respectively. tible to antibiotics piperacillin, cefepime, cefuroxime, Surgical site infections comprise the largest propor- cefuroxime-axetil, ceftriaxone, aztreonam, minocycline, tion of HAIs in developing countries, with an estimated tetracycline and sulfamethoxazole. All five E. coli isolates incidence of 5.6 per 100 surgical procedures [18]. Cae- were susceptible to meropenem and tigecycline. Both sarian sections are the most common surgical proce- the P. aeruginosa isolates were non-susceptible to ticar- dure in Kenya[19]. Longer durations of labor have been cillin-clavulanic acid and meropenem. At least 3/5 (60%) associated with a higher incidence of surgical site infec- of the isolated MRSA were non-susceptible to cefoxitin, tions following caesarian-section in Kenyan hospitals benzylpenicillin, oxacillin, erythromycin, clindamycin, [20], suggesting a role of the hospital environments in the gentamycin, levofloxacin, moxifloxacin, tetracycline and acquisition of HAIs. The high contamination rate of the trimethoprim-sulfamethoxazole. Both the E. faecium and surgical and maternity departments by MDR ESKAPEE faecalis isolates were non-susceptible to erythromycin, in this study supports this hypothesis. Newborn popula- levofloxacin, tetracycline and nitrofurantoin (Table  4). tions are particularly vulnerable to HAIs because of their immature immunity [1] and the high rate of contamina- Discussion tion of newborn departments by the MDR ESKAPEE in This study sampled high-touch surfaces in five Kenyan this study may explain, in part, the high prevalence of hospitals and found that more than 12.0% were con- HAIs observed in Kenyan pediatric departments [2]. The taminated with MDR ESKAPEE pathogens. There higher levels of MDR ESKAPEE contamination in higher- was a risk of HAIs by MDR ESKAPEE pathogens in all level hospitals than in lower-level hospitals may be linked the hospital departments sampled. In particular, items to increased antibiotics selection pressure resulting from found in patient areas, such as newborn incubators and extensive use, particularly in critical care units or spe- patient beddings, were frequently contaminated, posing cialized departments such as the surgical departments. a high risk of HAIs. Four departments, newborn, surgi- Patients with severe infections, trauma and those referred cal, maternity, and pediatrics, had particularly worrying from lower-level hospitals often seek medical care in contamination rates of at least 10%, with the surgical and higher-level hospitals. These patients often require surgi - cal interventions and the administration of antibiotics for patient care. Table 4 Antibiotic susceptibility profiles of the Gram-positive MDR A. baumannii was the most frequently isolated MDR ESKAPEE bacterial pathogens Antimicrobial agent MRSA, n = 5 (%) E. faecium ESKAPEE pathogen, 23/617 (3.7%) and was found across and E. faeca- all departments. Its ability to form biofilms and with - lis, n = 2 (%) stand desiccation [21, 22] enables it to persist in the hos- NS S NS S pital environment for long periods. Furthermore, it can Cefoxitin 5 (100) 0 nd nd maintain virulence even after prolonged desiccation and Penicillin 5 (100) 0 nd nd starvation [23], which partly explains its ability to cause Oxacillin 5 (100) 0 nd nd frequent and prolonged hospital outbreaks [21]. As a Erythromycin 5 (100) 0 2 (100) 0 result, A. baumannii has been linked to a wide range of Gentamycin 5 (100) 0 nd nd HAIs, including ventilator-associated pneumoniae, skin Clindamycin 5 (100) 0 nd nd and soft tissue infections, urinary tract infections, sec- Linezolid 0 5/5 (100) 0 2 ondary meningitis and bloodstream infections that often (100) affect critically ill patients [ 24], all of which have been Levofloxacin 4 (80) 1/5 (20.0) 2 (100) 0 associated with high mortality rates [25]. Data on the Moxifloxacin 4 (80) 1/5 (20.0) ND nd burden of A. baumannii infections in Kenya is not readily Tetracycline 3 (60) 2/5 (40.0) 2 (100) 0 available. The available data is from facility-based studies, Tigecycline 0 5/5 (100) 0 2 (100) which show that A. baumannii is an important cause of Nitrofurantoin 0 5/5 (100) 2 (100) 0 infections in Kenya [26, 27]. A. baumannii has also been Trimethoprim-sulfamethoxazole 5 (100) 0 nd nd implicated in outbreaks in a teaching hospital in Kenya Teicoplanin 0 5/5 (100) 0 2 [28]. The high frequency of A. baumannii isolation in this (100) study suggests an impending threat of hospital acquired Vancomycin 0 5/5 (100) 0 2 A. baumannii infections. Typically, A. baumannii is (100) intrinsically resistant to commonly prescribed antibiot- Fusidic Acid 0 5/5 (100) nd nd ics, such as first and second-generation cephalosporins, Abbreviations: NS, non-susceptible (Resistant or Intermediate); S, Susceptible; chloramphenicol, and aminopenicillins [25]. Carbape- nd, antimicrobial sensitivity testing not done; MRSA Methicillin resistant S. aureus nem antibiotics are the main treatment option for MDR Odoyo et al. Antimicrobial Resistance & Infection Control (2023) 12:22 Page 6 of 9 A. baumannii infections [25], yet in this study, 22/23 reduce the risk of K. pneumoniae HAIs in the newborn isolates were carbapenem non-susceptible. The use of departments of the study hospitals. Additionally, safe dis- quaternary ammonium compounds-based disposable posal of diapers, cleaning of soiled articles with water and wipes by in-house staff and chlorine-based disinfection is appropriately diluted disinfectants and soap, adherence recommended to reduce contamination of hospital sur- to hand hygiene procedures, and limited staff rotations faces by carbapenem-resistant A. baumannii [29]. Ter- have been successfully employed to contain an outbreak minal cleaning and enhanced cleaning of the high-touch in a neonatal unit [44]. surfaces [30] can help reduce the risk of A. baumannii Enterobacter species are associated primarily with HAIs at the study hospitals. None of the contaminating HAIs [45] and were the third most frequently isolated A. baumannii isolates were resistant to colistin and 22/23 MDR ESKAPEE pathogen in this study, 19/617 (3.1%). were susceptible to minocycline, leaving these agents as It was isolated across all the departments. Third-gen - treatment options for carbapenem-resistant A. bauman- eration cephalosporins are known to induce variants of nii strains [31]. The high rate of carbapenem resistance AmpC beta-lactamases in Enterobacter species, resulting inA. baumanniiisolates reflects an overreliance on car - in resistance [46], and their widespread use in Kenyan bapenem, a last-line antibiotic, for treatingA. baumannii, hospitals [47, 48] could be providing a selective pres- while disregarding first- and second-line options such as sure that favors Enterobacter species and the emergence tetracyclines and fluoroquinolones at the study hospitals. of cephalosporin resistance. Because of innate resistance K. pneumoniae is a significant cause of opportunistic to first and second-generation cephalosporins, treat - HAIs, including; pneumoniae, urinary tract infections, ment of Enterobacter infections is often limited to car- skin and soft tissue infections, septicemia and endocar- bapenems, fluoroquinolones, and aminoglycosides [ 45]. ditis [32]. It is the most common cause of HAIs, includ- Fourth-generation cephalosporins have been used to ing hospital outbreaks, in Kenya and Africa [4, 33]. In treat Enterobacter infections due to their relative stabil- this study, MDR K. pnuemoniae was the second most ity to AmpC beta-lactamases in the absence of extended- frequently isolated MDR ESKAPEE pathogen, 22/617 spectrum beta-lactamases [45]. This study, however, (3.6%). It was isolated from newborn, surgical and mater- found all the Enterobacter isolates resistant to cefepime, nity departments from high-touch items in near-patient a fourth-generation cephalosporin, which further limits areas, bathroom areas, and hospital equipment, reflect - treatment options for Enterobacter infections in the study ing its ubiquitous nature [32] and ability to persist in hospitals. There was, however, a low rate of resistance to the hospital environment by forming biofilms [ 10, 34]. fluoroquinolones, moxifloxacin, and levofloxacin, while Equally important, K. pneumoniae has been implicated meropenem was active against all the Enterobacter iso- in several outbreaks and HAIs in neonatal units [35–38]. lates from the study hospitals. Interestingly, one isolate In Kenya, multi-drug resistant K. pneumoniae has been was resistant to colistin while retaining susceptibility to implicated in an outbreak in a neonatal critical care unit other drug classes, which may be attributed to chromo- of a referral hospital in which six of the thirteen patients somal mutations or acquired resistance genes. However, succumbed, a 46% case fatality rate [39]. Multi-drug- a more reliable colistin test will be necessary to rule out resistant K. pneumoniae was also identified as the com - any false resistance often observed with colistin testing in mon cause of blood-borne infections in newborn units automated platforms. of another referral hospital in Kenya [40]. Indeed, these This study isolated two isolates of P. aeruginosa from reports highlight multi-drug-resistant K. pneumoniae as high-touch surfaces. P. aeruginosa is a common contami- an important cause of HAIs in Kenyan hospitals. There - nant in hospital environments, particularly moist sur- fore, the high contamination rate of surfaces and equip- faces such as sinks and taps [49, 50], which were sampled ment in newborn departments in this study is of grave in this study. The media used to detect P. aeruginosa was concern. All the K. pneumoniae isolates were resistant not the optimal selective media which could have limited to aztreonam and third and fourth-generation cephalo- the ability to detect it from the hospital environment. sporins, ceftriaxone and cefepime, respectively, which Similar to A. baumannii, the two isolates of P. aeruginosa infers the production of extended-spectrum beta-lacta- in this study were resistant to meropenem but retained mases and/or AmpC β-lactamases in addition to other susceptibility to the fluoroquinolone moxifloxacin fur - resistance mechanisms [41]. Additionally, 22.7% of the ther highlighting an overreliance on carbapenem for K. pneumoniae isolates were also resistant to merope- treatment at the study hospitals. Putting carbapenems on nem which infers the production of carbapenemases [42] watch lists and limiting access without approval can help [43]. Resistance to last-line antibiotics such as merope- limit increasing levels of carbapenem resistance in the nem threatens the ability to treat K. pneumoniae HAIs. study hospitals. Enforcing effective terminal cleaning of newborn incuba - At least 3/5 E. coli isolates were non-susceptible to tors and enhanced cleaning of high-touch areas can help third-generation cephalosporins, which may infer the Odoyo et al. Antimicrobial Resistance & Infection Control (2023) 12:22 Page 7 of 9 production of extended-spectrum beta-lactamases. How- practices. In addition, enforcing terminal cleaning of ever, all five isolates of E. coli were susceptible to last-line patients’ beds and newborn incubators, hospital environ- antibiotics such as meropenem and tigecycline. ment biomonitoring around high-touch areas, antibiotic The Gram-positive MDR ESKAPEE pathogens, MRSA stewardship programs, enforced hand hygiene, and ade- and Enterococcus faecalis/faecium, had high levels of quate and frequent cleaning of high-touch areas, as pre- resistance to first-line antibiotics, including erythro - viously described [15] can help reduce the risk of HAIs at mycin, levofloxacin, and tetracycline, while they were the study hospitals. susceptible to last line antibiotics; vancomycin, teico- List of abbreviations planin, and tigecycline. This study isolated MRSA and HAIs Healthcare-associated infections Enterococcus faecalis/faecium mainly from the newborn MDR Multidrug-resistant ESKAPEE Enterococcus faecalis/faecium, Staphylococcus aureus, Klebsiella and pediatric departments, which signifies a high risk pneumoniae, Acinetobacter baumannii, Pseudomonas aeruginosa, of HAIs to these younger patient populations. CHRO- Enterobacter species, and Escherichia coli Magar VRE should ideally limit the growth of contami- IPCs Infection prevention control practices NB Neutralizing buffer nating bacteria and vancomycin-susceptible Enterococcus KEMRI Kenya Medical Research Institute species. Despite this, in this study, the detected isolates CLSI Clinical and Laboratory Standards Institute of the Enterococcus faecalis/faecium were susceptible to WRAIR Walter Reed Army Institute of Research R Resistant vancomycin, indicating that the media may be permis- NS Non-susceptible (Resistant or Intermediate) sive to their growth and antimicrobial sensitivity testing S Susceptible is necessary to confirm whether the recovered isolates nd Antimicrobial sensitivity testing not done are indeed vancomycin-resistant. Gram-negative MDR Acknowledgements ESKAPEE pathogens were isolated in greater num- The authors appreciate the collaboration and support of the study hospital bers than Gram-positive MDR ESKAPEE, which may administration. The authors also appreciate Cliff Momanyi, Ruth Kiage, Mitsanze Thoya, Ruth Mupa, Charles Adega, Gladys Biwott, Alfred Odindo and be linked to IPC practices such as using contaminated Catherine Muriuki for sample collection. cleaning materials, which has been found to mainly replaceram-positive cocci with Gram-negative bacilli Author contributions Funding acquisition: L.M. Conceptualization: L.M., E.O. Investigation: E. O., D.M., [51]. In a previous study conducted in the same hospitals F.T., M.G., C. K., W. M. Data Analysis: E. O. and S.W. Writing – original draft: E. O. [15], storing wet mops was predictive of increased bacte- Writing – review and editing: E. O., L. M. All authors read and approved the rial loads, reflecting that this poor cleaning practice con - final manuscript. tributes to the spread of bacterial contamination. Funding This work was funded by the Armed Forces Health Surveillance Division Study limitations (AFHSD), Global Emerging Infections Surveillance (GEIS) Branch [PROMIS ID 17_KY_1.3.1]. The funders had no role in study design, data collection and Molecular characterization of the isolates from this study analysis, decision to publish, or preparation of the manuscript. would provide more information on the MDR ESKAPEE strain types found within these hospitals. Further, a com- Data Availability All data generated or analyzed during this study are included in this published parison with clinical strains could confirm the trans - article. mission patterns and ascertain that these pathogens are causes of HAIs in the study hospitals. The low rate of Declarations detection of Pseudomonas aeruginosa, a common cause of HAIs [52, 53], may be due to the failure to use a suit- Competing Interests The authors declared that they have no competing interests. able culture media for its detection in the study. Ethical statement Conclusion This study was approved by the KEMRI Scientific and Ethical Review Board, protocol #3482, and the Walter Reed Army Institute of Research ( WRAIR), The widespread presence of MDR ESKAPEE contami - protocol #2416, institutional review boards. Written approval was also nation in the study hospital environments suggests low obtained from the county and hospital administration. No human subjects compliance to IPC practices in Kenyan hospitals, which or animals were involved in this study. Permission has been granted for publication of this manuscript by the Director KEMRI. Material has been are already outstretched by challenges such as poor water reviewed by WRAIR. There is no objection to its publication. The opinions or supply, frequent electricity outages, sporadic supply of assertions contained herein are the private views of the author and are not to critical cleaning reagents and personnel, among others. be construed as official or as reflecting the true views of the Department of Defense. There was a high risk of HAIs by MDR ESKAPEE patho - gens across all the sampled hospitals. Non-susceptibility Author details to last-line antibiotics such as meropenem threatens the United States Army Medical Research Directorate-Africa, P.O. Box 606- 00621, Nairobi, Kenya ability to treat HAIs. The study hospitals could benefit Kenya Medical Research Institute, P.O. Box 54840-00200, Nairobi, Kenya from strengthening diagnostic capacity for antimicrobial 3 Independent researcher, Nairobi, Kenya sensitivity testing for judicious antibiotics prescription Odoyo et al. 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Journal

Antimicrobial Resistance and Infection Control – Springer Journals

Published: Mar 29, 2023

Keywords: Healthcare-associated infections; Hospital environment; Antibiotic resistance; Multi-drug resistance

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