Drugs - Real World Outcomes (2018) 5:101–108 https://doi.org/10.1007/s40801-018-0132-2 OR IGINAL RESEARCH ARTIC L E Pattern of Antimicrobial Resistance among Bacterial Isolates from Urogenital Clinical Specimens: A Descriptive Study from the Buea Health District, Cameroon 1,2,3 1,2,3 3,4,5 • • • Elvis Tajoache Amin Charles Njumkeng Belmond T. Kika 6 6 Akemfua Fualefac Patrick Njukeng Published online: 12 April 2018 The Author(s) 2018 Abstract Cameroon, from June to August 2017. All culture and Introduction Antimicrobial resistance has become a global antimicrobial susceptibility test results of patients who concern and is particularly affecting developing countries presented at each of the laboratories for urine, vaginal swab where infectious diseases and poverty are endemic. The or urethral swab cultures from January 2012 to December effectiveness of currently available antimicrobials is 2016 were included in the study. Data were analysed using decreasing as a result of increasing resistant strains among SPSS Windows version 20.0. The comparisons between clinical isolates. different isolates’ resistance to antimicrobials were per- Objectives The aim of this study was to determine the formed using the chi-square test. The difference in the resistance pattern of bacterial isolates from different clin- resistance of urogenital isolates to various antimicrobials ical urogenital specimens at different hospitals in the Buea within different years was also compared by the chi-square Health District, Cameroon. test. Methods A retrospective study was conducted in three Results A total of 423 bacterial isolates were obtained hospital laboratories in the Buea Health District, from clinical urogenital specimens such as: urine 93 (21.9%), vaginal swab 175 (41.4%) and urethral swab cultures 155 (36.6%). The predominant bacterial isolates & Elvis Tajoache Amin were Staphylococcus spp. 320 (75.5%), Escherichia coli 37 Charles Njumkeng (8.7%) and Enterococcus spp. 24 (5.7%). All the isolates firstname.lastname@example.org showed signiﬁcantly high resistance rates to amoxi- Belmond T. Kika cillin/clavulanic acid (67.6% resistant rate, p = 0.025), but email@example.com most isolates, except those of Staphylococcus, were rela- Akemfua Fualefac tively more susceptible to nitrofurantoin (82.6% suscepti- firstname.lastname@example.org bility rate, p = 0.045). However, Staphylococcus spp. was Patrick Njukeng more susceptible to ceftriaxone (91.0% susceptibility rate, email@example.com p \ 0.0001) and cefotaxime (74.4% susceptibility rate, St. Albert The Great Reference Medical Diagnostic Center, p = 0.034). Generally, most of the isolates showed signif- Buea, Cameroon icantly rising rates of resistance to the majority of the Global Research Education and Health Foundation, Buea, antimicrobials tested from 2012 to 2017. Cameroon Conclusion Our ﬁndings showed a progressively rising Ministry of Public Health, Yaounde, Cameroon rate of antimicrobial resistance in urogenital bacterial iso- lates over the last 5 years in the Buea Health District. Thus, Atlantic Medical Foundation Hospital, Mutengene, Cameroon uncontrolled and irrational use or prescription of these drugs should be avoided to maintain low resistance of Clinical Research Education, Networking and Consultancy, highly susceptible antimicrobials. Douala, Cameroon Global Health Systems Solutions, SONARA Road, Limbe, Cameroon 102 E. T. Amin et al. genital tract infections (pelvic inﬂammatory diseases, urethritis, etc.) are empirically based on the pre- Key Points dictable spectrum of aetiological micro-organisms and available data reﬂecting antimicrobial resistance of previ- In Cameroon, lack of bacterial testing, circulation of ous infections . Lack of bacterial testing, circulation of fake drugs, and irrational use of un-prescribed fake drugs, and irrational use of un-prescribed antimicro- antimicrobials has led to a progressive rise in bials are the possible reasons for antimicrobial resistance, antimicrobial resistance. and are responsible for recurrence of infections as well as Our ﬁndings showed a progressively rising rate of complicated UTIs [12, 14, 15]. Recent studies show a antimicrobial resistance in the uropathogens isolated, growing problem of antimicrobial resistance in Cameroon with highest rates of resistance to [11, 16, 17], thereby necessitating the need for continuous amoxicillin/clavulanic acid while most surveillance of antimicrobial susceptibility to pathogens, except Staphylococcus spp., remain uropathogens. susceptible to nitrofurantoin. Uncontrolled and irrational use or prescription of 2 Methods antimicrobials should be avoided so as to maintain low resistance of highly susceptible antimicrobials. 2.1 Study Area and Sites This study was conducted in the Buea Health District, Cameroon. The Buea Health District is among the four 1 Introduction health districts that make up the Fako Division of Camer- oon with a total population of 131,325 . It has an Over the past years, antimicrobial resistance (AMR) has average temperature, humidity and rainfall of 23 C, 83.5% become a global concern. It has particularly affected and 58 mm, respectively. The Buea Health District is developing countries where infectious diseases are ende- divided into seven health areas, which include: Molyko, mic . Infections that are caused by resistant bacteria Muea, Buea Town, Bova, Bokwaongo, Tole and Buea have often been associated with increased morbidity and Road health areas. The health district has 66 communities mortality compared with those caused by susceptible and a total of 21 health facilities (both private and state pathogens . Infections of the urogenital system are owned). The study was conducted in all eligible laborato- among the commonest bacterial infections encountered in ries within the health district where culture and sensitivity daily clinical practice . Urinary tract infections (UTIs) testing is done. are a major cause of morbidity in both the hospital and community settings, occurring in all age groups, with most 2.2 Study Design and Population of the infections being treated empirically with broad- spectrum antimicrobials. However, antimicrobial resistance A retrospective study was conducted in three health facil- in bacteria causing UTIs has progressively increased since ities (St Albert Medical Centre, Mount Mary Hospital and the introduction of UTI chemotherapy [4, 5]. Solidarity Clinic) in the Buea Health District, Cameroon, Several studies [6, 7] show geographic variations in from June to August 2017. All cultures and antimicrobial bacterial uropathogens and their resistance patterns to susceptibility test results of patients who presented at each antimicrobials. Escherichia coli, Klebsiella, Pseudomonas of the laboratories for urine, vaginal swab or urethral swab aeruginosa and Enterococcus species were the most com- cultures from January 2012 to December 2016 were mon bacterial pathogens isolated from the urinary tracts of included in the study. All data were extracted from labo- infected patients [8, 9]. The antimicrobial susceptibility ratory records using a structured checklist. patterns of bacteria isolated from urinary tracts differ for different bacteria and antimicrobials [8, 10, 11], with 2.3 Ethical Considerations increased susceptibility to the quinolones and increased resistance to nitrofurantoin, ampicillin and cotrimoxazole. Ethical approval was obtained from the Cameroon Baptist E. coli has been reported in studies in Nigeria and Turkey Convention Health System Institutional review board as the most resistant microorganism, [8, 12] contributing to (CBCHB IRB) (Re: IRB2017-23). recurrent infections . Administrative authorization for this study was obtained In Cameroon and other resource-limited countries, from the South West Regional Delegation of Public Health. treatment choices for the majority of urinary and other Permission to collect the information from registers was Pattern of Antimicrobial Resistance among Bacterial Isolates from Urogenital Clinical Specimens 103 obtained from the administration of the various hospitals Culture plates were incubated at 37 C for 18–24 h. involved. Considering that the study does not directly Gram’s stain and biochemical procedures were then used to involve human subjects a consent waiver was applied. All identify the bacteria. data collected were treated with strict conﬁdentiality through coding (anonymous) of the cases. Within each 2.6 Antimicrobial Susceptibility Testing selected laboratory, the data were extracted by the labo- ratory staff to avoid breaching the patient’s conﬁdentiality Antimicrobial susceptibility was determined using the disc since the registers have patient names. diffusion method on Mueller Hinton agar as described in the guidelines of the Clinical and Laboratory Standard 2.4 Data Collection Institute . The families of drugs studied were quino- lones (norﬂoxacin, oﬂoxacin and ciproﬂoxacin), nitrofuran After obtaining ethical clearance and administrative (nitrofurantoin), cephalosporins (cefuroxime, ceftriaxone authorization, a modiﬁed WHO Antimicrobial Resistance and cefotaxime), penicillins (amoxicillin, piperacillin, Surveillance Questionnaire was used to assess the labora- amoxicillin/clavulanic acid and ampicillin), macrolides tory’s capacity to perform culture and sensitivity testing (clarithromycin and erythromycin), aminoglycosides . The data quality was assessed (for availability, con- (gentamicin, rifampicin and vancomycin) and tetracyclines sistency and completeness) as proposed by the DAMA UK (tetracycline and doxycycline). Working Group on ‘Data Quality Dimensions’ . Given The plates were incubated for 24 h against Staphylo- the doubtful quality of data from our health system, lack of cocuss spp. and 16–18 h for all other isolates. The diam- studies in this area and the uncertainty of compliance with eters of the zones of complete inhibition (as judged by the data management practices, we anticipated that an overall unaided eye) were measured, including the diameter of the data quality of 60% was reasonable enough to be included disk to the nearest whole millimetre. The diameter was in the study. Therefore, 60% was set as the minimum score compared to the critical values of each antimicrobial disc for any facility to be included in the study. The data on to qualify the target bacteria as sensitive, resistant or culture results (isolates and sensitivity results) and demo- intermediate. Control tests were performed with Staphy- graphics (age and sex) were collected with the use of a lococcus aureus ATCC25923 and E. coli ATCC25922 checklist drawn from the laboratory registers. reference strains. 2.5 Sample Collection and Processing 2.7 Data Analysis The samples collected in this study were urine, urethral Data analysis was done with SPSS version 20 (IBM, Chi- swabs and vaginal swabs. For urine samples, about 50 ml cago, IL, USA). Comparison between different isolates’ of midstream urine specimen was collected in a sterile resistance to an antimicrobial was performed using the chi- Jeanne specimen container. The semi-quantitative tech- square test. The difference in the resistance of urogenital nique to determine signiﬁcant bacteriuria was employed by bacteria to various antimicrobials over different years was using 0.01 ml calibrated wire loop to inoculate the urine on also compared by the chi-square test, while Pearson’s 5% blood agar, eosin-methylene blue (EMB) agar and correlation was used to study the trends of antimicrobial CLED agar (cystine lactose-electrolyte-deﬁcient). A urine resistance over time. The threshold for statistical signiﬁ- specimen was considered positive if a single organism was cance was p \ 0.05. isolated at a concentration greater than 10 CFU/ml and with a corresponding microscopy ﬁnding of greater than 10 leucocytes per high-power ﬁeld. 3 Results For the urethral swab, the urethra opening was cleared using a swab moistened with sterile physiological saline. A total of 502 records were reviewed within the study After inoculation of media, the remaining sample was period. Out of the 502 records reviewed, 79 had incomplete centrifuged at 2000 rpm for 5 min and the sediment was data and were rejected. The remaining 423 records were used for microscopy. included in the study. Of the total 423 records reviewed, 93 Vaginal swabs were collected with the aid of a specu- (21.9%) were urine culture, 175 (41.4%) were vaginal lum. They were moistened with warm sterile water and smear culture and 155 (36.6%) were urethral smear culture. inserted into the vagina following the guidelines found in The majority of the records reviewed were of female the second edition of Cheesbrough . Vaginal and ure- patients 243 (57.3%). The age of the study participants thral specimens were inoculated on Sabouraud agar, blood ranged from 3 years to 83 years, with the mean age of agar, chocolate agar, Mannitol salt agar and EMB agar. 33.5 years (SD ± 14.3). Most of the participants were 104 E. T. Amin et al. within the sexually active age groups of 20–39 years resistance to tetracycline, though this was not statistically (271 patients; 63.9%), while the elderly (age [ 60 years) signiﬁcant (Fig. 1). were the least represented (30; 7.1%). All records reviewed A total of 18 antimicrobials were analysed over a period had at least one bacterial isolate. Eight different species of of 5 years. It was observed that the isolated pathogens had urogenital pathogens were isolated. All staphylococcus average resistance of over 50% to six antimicrobials (te- species (S. aureus and S. saprophyticus) were group tracycline, erythromycin, amoxicillin/clavulanic acid, together while E. coli and the remaining isolates were also clarithromycin, ampicillin and amoxicillin) throughout the grouped together to facilitate data analysis, since the study period. The highest resistance rates were seen with number of some pathogens isolated was too small to be ampicillin and tetracycline, with average resistant rates of analysed individually. Among the isolates, Staphylococcus 64.9 and 64.0%, respectively. On the other hand, four drugs spp.—320 (75.5%), E. coli—37 (8.7%) and Enterococcus (cefotaxime, ceftriaxone, ciproﬂoxacin and gentamicin) spp.—24 (5.7%), were the most predominant (Table 1). showed resistance rates below 20%, and all the isolated All pathogens isolated were classiﬁed as either resistant uropathogens were most susceptible to gentamicin (as or susceptible to each of the antimicrobials tested. Sta- shown in Table 2). All the isolated pathogens demonstrated phylococcus spp. and most of the other isolates (dominated a ﬁvefold increase in resistance to cefotaxime from 2012 by E. coli) showed signiﬁcantly high resistance to amoxi- and 2016. Similarly, there was a progressive increase in cillin/clavulanic acid, with resistance rates of 45.3 and resistance to amoxicillin from 20% in 2012 to over 80% in 67.6%, respectively. On the other hand, all isolates except 2016. No signiﬁcant increase in resistance to ciproﬂoxacin, Staphyloccocus spp. were relatively more susceptible to ceftriaxone and gentamicin between 2012 and 2015 was nitrofurantoin (82.6% susceptibility rate, p = 0.045). noted. However, there was a dramatic rise in resistance However, Staphylococcus spp. demonstrated a greater rates to ciproﬂoxacin from 6.1% in 2015 to 38.2% in 2016. susceptibility to ceftriaxone with a low resistance rate of All isolates found in this study showed a positive cor- 9%. All the isolates also demonstrated a high rate of relation of their resistance rate to antimicrobials over the years except for tetracycline. However, only gentamicin showed a strong correlation (r = 0.900, p = 0.037) Table 1 Distribution of study participants from various laboratories (Table 3). according to sex, age, specimen and isolates Variable Frequency N (%) N = 423 4 Discussion Sex Female 243 (57.3) Infections of the urogenital system are among the most Male 180 (42.7) common bacterial infections encountered in daily clinical Age group in years practice. Uropathogens and their antibiotic susceptibility \ 20 36 (8.5) pattern have continued to change . This study deter- 20–39 271 (63.9) mined the resistance pattern of bacterial isolates from 40–59 87 (20.5) different clinical urogenital specimens, at different hospi- [ 60 30 (7.1) tals in the Buea Health District, Cameroon. The most Specimen predominantly isolated bacteria were Staphylococcus spp., Urine 93 (21.9) E. coli and Enterococcus spp. Similar ﬁndings have been Vaginal smear 175 (41.4) reported in two studies in Ethiopia [24, 25]. The high rate of Staphylococcus spp. isolated was mainly because the Urethral smear 155 (36.6) different subtypes of staphylococci were grouped together Isolate since most of them were not well represented. However, S. Staphylococcus aureus 286 (67.6) aureus was the most predominant subtype and can be Staphylococcus saprophyticcus 34 (8.0) attributed to the patients’ normal endogenous ﬂora . Streptococcus 13 (3.1) The second highest isolate in our study was E. coli. It has Enterococcus spp. 24 (5.7) been the most frequently reported isolate causing urinary Neisseria gonorrhoeae 12 (2.8) tract infections in similar studies [6, 11, 12]. The lower Escherichia coli 37 (8.7) number of isolated E. coli from our study can be explained Klebsiella spp. 5 (1.2) by the fact that the data we obtained from urine cultures Pseudomonas aeruginosa 1 (0.2) accounted for only 36.6%; in addition, bacterial isolates Proteus spp. 11 (2.6) vary with different clinical specimens, study designs, geographic locations and study populations. Pattern of Antimicrobial Resistance among Bacterial Isolates from Urogenital Clinical Specimens 105 Fig. 1 Comparison of the 80 resistance of Staphylococcus p = 0.213 isolates and all other isolates to p = 0.025 the various antimicrobials from selected laboratories in the Buea Health District, Cameroon, from p = 0.202 2012 to 2017 p = 0.072 p =0.045 p = 0.034 p < 0.001 p = 0.447 p <= 0.213 p = 0.220 Staphylococcus spp. all other isolates With regard to the pattern of antimicrobial resistance to Pseudomonas aeruginosa and Proteus spp.) together the different isolates, Staphylococcus spp. showed a sig- showed a signiﬁcant susceptibility to nitrofurantoin. The niﬁcantly high resistance rate to nitrofurantoin compared to high resistance rate of the other isolates, particularly all other isolates. On the other hand, all other isolates were E. coli, which was most predominant, has also been more resistant to ceftriaxone, cefotaxime and amoxi- reported by Yaounde . This increasing resistance rate cillin/clavulanic acid. The high resistance rate of Staphy- could be attributed to the rapidly growing population as lococcus spp. to these drugs limits their use as empirical well as to progressive urbanization of the Buea Health treatment of urinary tract as well as other genital tract District, which now has greater access to antimicrobials, infections. A high rate of resistance to amoxicillin has also hence a greater consumption rate leading to an increase in been reported in Nigeria . Also, Staphylococcus spp. resistance . It was also noted that all the urogenital pathogens isolated had very high resistance rates to tetra- are normal body ﬂora and frequently found in the envi- ronment with consistent human infection, thus the resis- cycline, ampicillin and erythromycin, but these rates were tance proﬁle of Staphylococcus spp. to commonly available not statistically signiﬁcant. This was in line with ﬁndings antimicrobials such as amoxicillin may not be unexpected by Alo et al. . in environments with frequent self-medication and irra- Over the past years, studies have shown the emergence tional use of un-prescribed antimicrobials. Staphylococcus of widespread resistance to commonly available ﬁrst-line spp. on the other hand were relatively more susceptible to antimicrobial agents (cephalosporins and ﬂuoroquinolones) ceftriaxone and cefotaxime, with relatively low resistance in sub-Saharan Africa . Likewise, our ﬁndings indicate rates. This can be explained further by the fact that these that there is also a gradual increase in resistance of bac- particular drugs are not readily available in most pharma- terial species to these classes of drugs. This was illustrated cies and drug stores in the form of tablets but rather as by the ﬁvefold increase in resistance to cefotaxime. On the injections. Thus, they are not common at most roadside contrary, no signiﬁcant increase in resistance to cipro- drug vendors and some pharmacies for easy consumption ﬂoxacin, ceftriaxone and gentamicin was observed between without prescription, thereby keeping the rate at which the 2012 and 2015, though there was a sudden rise in cipro- drugs can be misused to relatively low levels. This ﬁnding ﬂoxacin resistance from 6.1% in 2015 to 38.2% in 2016. was also in accordance with results by Alo et al. in Nigeria This can be accounted for by the fact that microbial . resistance to drugs built up over the years. The resistant The other isolates found in this study (E. coli, Entero- pattern observed in Senegal, Nigeria and Malawi indicated coccus spp., Neisseria gonorrhoeae, Klebsiella, a statistically signiﬁcant rise of resistance to ciproﬂoxacin, Percentage Resistance 106 E. T. Amin et al. Table 2 Resistance patterns of the isolated uropathogens to common antimicrobials in the Buea Health District, Cameroon between 2012 and 2016 Year Ceftriaxone Gentamicin Amoxicillin Amoxicillin/clavulanic acid Nitrofurantoin R % OR (95% CI) p value R % OR (95% CI) p value R % OR (95% CI) p value R % OR (95% CI) p value R % OR (95% CI) p value 2012 4.8 1.88 (0.29–11.91) 0.51 2.7 0.52 (0.05–5.89) 0.60 21.2 6.19 (1.91–20.04) 0.00 38.5 2.00 (0.59–6.78) 0.27 20.0 3.00 (0.74–12.11) 0.12 2013 8.6 9.09 (1.55–3.39) 0.02 1.4 1.29 (0.18–9.47) 0.80 62.5 8.82 (2.73–28.54) 0.00 55.6 1.14 (0.29–4.60) 0.85 42.9 1.45 (0.37–5.68) 0.59 2014 31.2 2.90 (0.46–15.53) 0.28 3.5 1.87 (0.25–13.79) 0.54 70.4 1.86 (0.28–12.31) 0.52 41.7 1.60 (0.19–13.24) 0.66 26.7 4.00 (0.20–78.7) 0.36 2015 11.8 4.90 (1.04–23.17) 0.04 5.0 6.32 (1.38–29.03) 0.02 33.3 16.10 0.00 50.0 2.08 (0.83–5.23) 0.12 50.0 1.00 (243–4.11) 1.00 (3.57–72.68) 2016 19.7 1 – 15.1 1 – 81.8 1 – 56.5 1 – 20.0 1 – Year Ciproﬂoxacin Vancomycin Tetracycline Doxycycline Cefotaxime R % OR (95% CI) p value R % OR (95% CI) p value R % OR (95% CI) p value R % OR (95% CI) p value R % OR (95% CI) p value 2012 3.2 5.62 (0.68–46.66) 0.11 18.2 1.08 (0.18–6.36) 0.93 75.3 1.07 (0.31–3.57) 0.92 40.0 2.00 (0.25–16.9) 0.51 5.9 8.73 (0.99–82.96) 0.05 2013 15.8 5.00 (0.55–45.3) 0.15 19.4 2.38 (0.42–13.47) 0.32 76.5 0.26 (0.12–0.57) 0.00 57.1 0.26 (0.04–1.88) 0.18 35.3 2.40 (0.23–25.34) 0.47 2014 14.3 1.93 (0.17–22.5) 0.60 34.6 1.35 (0.18–10.01) 0.80 44.4 1.31 (0.39–4.40) 0.66 14.6 0.55 (0.08–4.04) 0.56 13.0 3.00 (0.28–31.99) 0.36 2015 6.1 18.57 (0.39–10.90) 0.01 23.1 1.80 (0.30–10.90) 0.52 80.0 0.34 (0.15–0.77) 0.01 26.9 0.79 (0.12–5.09) 0.80 15.8 5.05 (0.61–22.1) 0.14 2016 38.2 1 – 28.6 1 – 51.2 1 – 34.4 1 – 24.0 1 – Bold text indicates p \ 0.05 OR odds ratio, R resistance Pattern of Antimicrobial Resistance among Bacterial Isolates from Urogenital Clinical Specimens 107 Table 3 Resistance trends of the isolated uropathogens to common (Staphylococcus spp., E. coli and Enterococcus spp.) iso- antimicrobials in the Buea Health District, Cameroon, between 2012 lated showed signiﬁcantly high resistance rates to amoxi- and 2017 cillin/clavulanic acid, while most of the isolates found in Drug Correction coefﬁcient p value the study, except Staphylococcus spp., remain susceptible to nitrofurantoin. However, Staphylococcus spp. were rel- Ceftriaxone 0.658 0.198 atively more susceptible to ceftriaxone and cefotaxime. All Gentamicin 0.900 0.037 pathogens isolated demonstrated a progressive rise in Amoxicillin 0.687 0.178 antimicrobial resistance from 2012 to 2016. Thus, the Amoxicillin/clavulanic acid 0.700 0.188 irrational use or prescription of these drugs should be Nitrofurantoin 0.103 0.870 avoided to keep the resistance to highly susceptible Ciproﬂoxacin 0.600 0.285 antimicrobials low. Vancomycin 0.678 0.169 Tetracycline - 0.100 0.873 Acknowledgements We thank the staff in the ﬁle rooms and the data Cefotaxime 0.400 0.505 collectors for assisting with the data collection phase of this study. We acknowledge the Directors of St. Albert Clinic, Mount Mary and Bold text indicates p \ 0.05 Solidarity Hospitals who assisted in providing the essential docu- ments required for obtaining ethical clearance. Compliance with Ethical Standards ceftriaxone and gentamicin [5, 28, 29]. This was contrary to our ﬁndings and can be explained by the fact that Sta- Conﬂict of interest ETA, NC, BTK, AF and GT have no conﬂicts of interest. phylococcus spp. were the predominant isolates in our study instead of E. coli, which was predominant in most of Funding No external funding was received for this study. the other studies. Furthermore, a progressive increase in resistance to antimicrobials over the years in this study area Open Access This article is distributed under the terms of the can be due to urbanization, since it leads to increases in Creative Commons Attribution-NonCommercial 4.0 International License (http://creativecommons.org/licenses/by-nc/4.0/), which per- population, increases in the availability of roadside drug mits any noncommercial use, distribution, and reproduction in any vendors and pharmacies, and poor regulatory mechanisms medium, provided you give appropriate credit to the original to prevent the irrational sale and consumption of un-pre- author(s) and the source, provide a link to the Creative Commons scribed antimicrobials. license, and indicate if changes were made. Over the last 5 years (2012–2017), the resistance rate of the bacterial isolates to amoxicillin/clavulanic acid, nitro- References furantoin, tetracycline, doxycycline and vancomycin has been progressively rising. 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Drugs - Real World Outcomes – Springer Journals
Published: Apr 12, 2018
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