Antibiotics, Vol. 11, Pages 1718: Multidrug-Resistant Uropathogens Causing Community Acquired Urinary Tract Infections among Patients Attending Health Facilities in Mwanza and Dar es Salaam, Tanzania

1. IntroductionUrinary tract infections (UTIs) are among the most common bacterial infections encountered in healthcare community settings and are associated with increased treatment cost, morbidity, and mortality [1,2]. UTIs can be categorized based on how the infection was acquired, which includes hospital-acquired and community acquired urinary tract infections [1,3,4]. Community acquired urinary tract infections occur when a patient develops a UTI before admission to the healthcare facility and not within 10 days after the patient has been discharged from the healthcare facility [1,5]. Escherichia coli is the most common bacterium reported to cause urinary tract infections, while other common uropathogens isolated from urinary tract infections include Klebsiella spp., Staphylococcus spp., Enterococcus spp., Enterobacter spp., and Citrobacter spp. [1,3]. Community acquired UTIs are usually uncomplicated, as opposed to hospital-acquired UTIs, which, in most cases, are complicated and associated with risk factors such as catheterization and recent antibiotic use [6]. In most resource-limited health facilities, community acquired urinary tract infections are the predominant type of UTI and are inappropriately treated with antibiotics due to a lack of laboratory services, as well as sufficiently trained medical personnel [7,8]. Inadvertently, this leads to the emergence and spreading of multidrug-resistant (MDR) bacteria strains in the community [8], leading to recurrences [2,6,7,8] and complications such pyelonephritis with sepsis and pre-term birth in pregnancy [9,10]. In Tanzania, most of the antibiotics’ profile data on UTIs are from patients attending referral hospitals where microbiological services are available [11]. Unfortunately, limited data on UTIs in communities, coupled with a lack of antibiotic stewardship and an absence of laboratory services, leads to irrational uses of antibiotics, especially the widely available cheap medicines, which are often of variable quality [12,13].

We designed this cross-sectional health centre-based study to determine the antibiotic susceptibility profiles of multidrug resistant (MDR) bacteria causing community acquired urinary tract infections in Tanzania, where such information is essentially non-existent. Data emanating from this study may be used in drafting evidence-based empirical treatment guidelines among outpatients attending healthcare facilities where urine culture is currently not feasible.

3. Discussion

This study aimed to determine the antibiotic resistance profiles of uropathogens causing community acquired urinary tract infections among outpatients attending selected health centres in Tanzania. This study represents patients from the community with signs and symptoms of UTI from the two largest cities in Tanzania. These data are important because, currently, there is a lack of antimicrobial resistance (AMR) data regarding community infections. The fact that multidrug-resistant, gram-negative, and gram-positive bacteria is the predominant cause of community acquired UTI highlights the coordinated effort required to address the AMR problem in Tanzania and other low-income countries through improved quality healthcare provision.

In the current study, the overall prevalence of community acquired urinary tract infections was 27.4%, with site-specific prevalence rates being 26.5% in Mwanza and 28.4% in Dar es Salaam. Our observed prevalence is slightly lower compared to another study in Tanzania, reporting a prevalence of community acquired urinary tract infections of 38.5% [14]. Similarly, a higher prevalence of community acquired urinary tract infections (39.1%) was reported in Uganda [3]. However, our prevalence matches the prevalence of 26.7% observed in a study in Senegal [15]. These variations could be attributable to differences in antibiotic usage, age, and gender, as well as in the handling and processing of urine samples [16].Notably, more than one half of isolated uropathogens causing community acquired urinary tract infections were Gram-negative bacteria, of which E. coli was frequently isolated, which is in keeping with community acquired urinary tract infection studies conducted in Tanzania [14], Uganda [3], India [17], and Senegal [15]. Besides E. coli, Enterococcus spp., S. aureus and K. pneumoniae were the second, third, and fourth most frequent causes of community acquired urinary tract infections in our setting, which is in keeping with findings reported elsewhere [18,19]. Interestingly, other uropathogens included coagulase negative Staphylococci (CoNS) such as S. haemolyticus (n = 32), S. epidermidis (n = 20), and S. hominis (n = 3), which have also been reported in previous studies [14,19,20]. Similar to previous reports [21,22,23,24,25], we also found uropathogens that are rarely associated with UTI, including Corynebacterium aurimucosum, Corynebacterium striatum, Escherichia hermannii, Stenotrophomonas maltophilia, Mammaliicoccus sciuri (formerly Staphylococcus sciuri), Acidovorax temperans, and Comamonas testosterone (formerly Pseudomonas testosterone); moreover, A. temperans, S. maltophilia, and M. sciuri were isolated in Dar es Salaam only, whereas C. testosterone was isolated in Mwanza only. Collectively, these findings indicate that the spectrum of potential uropathogens is wide, warranting the need to employ advanced molecular studies, such as whole-genome sequencing, to screen for their pathogenic and virulence factors. For example, previously, CoNS, Corynebacterium spp., and C. testosterone were considered skin flora and/or possible laboratory contaminants, while M. sciuri was considered to colonize animals; however, increasingly, the bacteria have become associated with opportunistic infections in humans, including UTIs [22,23,26].

Overall, antibiotic resistance of Gram-negative bacteria was less (<30%) to carbapenems, third generation cephalosporins, gentamicin, nitrofurantoin, and trimethoprim–sulfamethoxazole. However, we observed variations in the percentages of the resistance of bacteria pathogens to different antibiotics between the Dar es Salaam and Mwanza samples. For example, E. coli isolated from Dar es Salaam showed resistance of 15.1% and 0.0% towards nitrofurantoin and carbapenems, while those isolated from Mwanza showed a resistance of 38.9% and 1.1% towards nitrofurantoin and carbapenems, respectively. Further, other Enterobacterales, excluding E. coli, exhibited a resistance of 61.7%, 44.7%, and 27.7% to ampicillin, ciprofloxacin and gentamicin, respectively, in Dar es Salaam, whereas the resistance of 96.8%, 22.6%, and 9.7% towards ampicillin, ciprofloxacin, and gentamicin in respective was observed in Mwanza.

On the other hand, Gram-positive bacteria, particularly S. aureus isolated in the current study, generally showed less resistance to nitrofurantoin (26.6%) and linezolid (20.0%); Enterococcus spp. showed less resistance towards ampicillin (14.3%); coagulase negative Staphylococci (CoNS) exhibited less resistance to linezolid (2.8%) and nitrofurantoin (16.9%); and Streptococcus spp. had low resistance to linezolid (4.6%) and clindamycin (9.1%). Similar to Gram-negative bacteria, differences in the percentage of the resistance of Gram-positive bacteria to different antibiotics were observed between Dar es Salaam and Mwanza. For instance, 43.8%, 31.3%, and 43.8% of S. aureus isolated from Dar es Salaam were resistant to ciprofloxacin, clindamycin, and nitrofurantoin compared to 78.6%, 71.5%, and 7.1% of the S. aureus isolated from Mwanza towards similar antibiotics, respectively.

The possible reasons for this observation, namely, the variations in the frequencies of antibiotics’ resistance between the two regions, which are about 1100 km apart, could be due to differences in the drivers responsible for the emergence and spreading of MDR pathogens. These drivers include, but are not limited to, the misuse of antibiotics in clinics, the community, and farms, as well as sanitation infrastructures and waste disposal [27]. Indeed, a previous study demonstrated a clear link between widespread irrational use of antibiotics in the community and the subsequent consecutive induction of resistance [28].From our observations in the general antibiotic susceptibility profiles of uropathogens isolated during this study, nitrofurantoin, gentamicin, and third generation cephalosporins may be prescribed for Gram-negative bacteria, whereas nitrofurantoin, clindamycin, and linezolid may be prescribed for Gram-positive bacteria. These antibiotics are effective since they are rarely prescribed compared with ampicillin and tetracycline, which are cheaper and widely used [12,13].The high rate of resistance shown by E. coli and other Enterobacterales against ciprofloxacin is concerning since this antibiotic is listed as the first line for an uncomplicated UTI, which is largely caused by Enterobacterales, predominantly E. coli [11]. Ciprofloxacin is overly prescribed not only for UTI, but also for many other bacterial infections, often without prescription or proper diagnosis [14,29].

Finally, we would like to acknowledge as a limitation the fact that, for some isolates, there may be a lack of differences in antibiotic resistance between the two regions due to the small sample, such as, for example, in the resistance to ciprofloxacin, clindamycin, and nitrofurantoin for S. aureus isolated in Dar es Salaam, which occurred in only 16 cases (7, 5, and 7 cases, respectively), and for n = 14 in Mwanza (11, 10, and 1 cases, respectively). The comparison of these specific isolates does not include many people.

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