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ORIGINAL ARTICLE
Year : 2021  |  Volume : 24  |  Issue : 8  |  Page : 1225-1233

Bacteriological Profile and Antibiotic Sensitivity Patterns in Clinical Isolates from the Out-Patient Departments of a Tertiary Hospital in Nigeria


1 Institute of Lassa Fever Research and Control, Irrua Specialist Teaching Hospital, Irrua, Edo State, Nigeria
2 Department of Microbiology, Irrua Specialist Teaching Hospital, Irrua, Edo State, Nigeria
3 Department of Biological Sciences, Ondo State University of Science and Technology, Nigeria

Date of Submission08-Jan-2020
Date of Acceptance14-May-2021
Date of Web Publication14-Aug-2021

Correspondence Address:
Dr. E A Tobin
Institute of Lassa Fever Research and Control, Irrua Specialist Teaching Hospital, Irrua
Nigeria
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/njcp.njcp_8_20

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   Abstract 


Background: Antimicrobial resistance (AMR) is a rising global public health threat. Knowledge of the circulating pathogens in a particular area and their antibiotic resistance profile is essential to direct clinicians on rational antibiotic prescribing. Aim: The study was conducted to determine the microbial isolates and antibiotic susceptibility profiles of pathogens from a range of clinical samples in a tertiary hospital in Edo Central Senatorial District in Edo State, Nigeria. Settings and Design: The study was a retrospective analysis of microbiological isolates from clinical specimens collected between January 2016 and December 2019, using standard techniques from outpatient clinic attendees. Chi-square test was used to compare the association of the type of bacterial isolates with patients' sex and level of significance P set as < 0.05. Prevalence rates of bacterial isolates and resistance rates were calculated for each antibiotic used in the microbiological culture. Results: Of the 3,247 clinical specimens processed, 994 (30.6%) showed microbial growth with 436 (43.9%) as gram-positive and 558 (56.1%) as gram-negative bacterial isolates. Escherichia coli (E. coli) made up 286 (28.8%) of all the isolates. Resistance to cotrimoxazole, tetracycline and cloxacilin for gram-poisitive pathogens was 93.1%, 86.4% and 72.5% respectively. For gram-negative pathogens, resistance to amoxycilin, cloxacilin and erythromycin was 100%, 96.9% and 95.6% respectively. Sensitivity to carbapenems, nitrofurantoin, and cefixime was high for gram-negative bacteria (100.0 %,76.8 % and 82.5 % respectively). Gram-positive bacteria exhibited high sensitivity to carbapenems ceftriaxone and cefixime. Conclusion: High rates of resistance to common antibiotics were observed for gram-positive and gram-negative isolates. Hospital pharmacies and treatment guidelines should be made to reflect the current patterns of resistance to available antibiotics.

Keywords: Antibiotic, bacterial isolates, outpatients, resistance


How to cite this article:
Tobin E A, Samuel S O, Inyang N J, Adewuyi G M, Nmema E E. Bacteriological Profile and Antibiotic Sensitivity Patterns in Clinical Isolates from the Out-Patient Departments of a Tertiary Hospital in Nigeria. Niger J Clin Pract 2021;24:1225-33

How to cite this URL:
Tobin E A, Samuel S O, Inyang N J, Adewuyi G M, Nmema E E. Bacteriological Profile and Antibiotic Sensitivity Patterns in Clinical Isolates from the Out-Patient Departments of a Tertiary Hospital in Nigeria. Niger J Clin Pract [serial online] 2021 [cited 2022 Jan 25];24:1225-33. Available from: https://www.njcponline.com/text.asp?2021/24/8/1225/323869




   Introduction Top


Bacterial infections continue to contribute significantly to the overall morbidity and mortality from infectious diseases in developing countries despite the availability of antibiotics.[1] The rising threat of antimicrobial resistance (AMR) described as a global public health challenge of the twenty-first century, increases the frailty of human existence by increasing the vulnerability to bacterial infections that were hitherto treatable with available antibiotics.[2] Antibiotic-resistant bacteria are difficult to treat, limit therapeutic options, prolong hospitalization, and require higher doses, and probably drugs, with higher tendencies for toxicity.[3] The slow progress with the development of new antibiotics to replace the first-line drugs to which bacteria have become resistant further compounds the problem. In the past 50 years, only two new classes of antibacterial drugs have been developed and introduced into clinical practice.[4] Even when a promising drug or vaccine exists, the high cost of production and length of time between the regulatory approval and deployment reduces its availability.[5],[6] Several studies in developed and developing countries describe the rising patterns of bacterial resistance. In a study of uropathogens in Western Nigeria, 35.8% of urine samples yielded bacterial growth with the commonly used drugs.[7] In another study, Nmema et al.[8] investigated the antibiotic susceptibilities and resistance mechanisms of Pseudomonas aeruginosa isolated from clinical samples collected from patients in a tertiary hospital in Lagos, Nigeria. Half of the isolates were multidrug-resistant, and 40% were resistant to imipenem and meropenem, a group of antibiotics considered as the last line for gram-negative infections.[8]

The increasing occurrence of resistant bacterial pathogens necessitates that patterns of infection and antibiogram profile of community-acquired bacterial infections are reviewed periodically, and the information used to guide the development of local treatment guidelines and hospital antibiotic policies that will guide the use of antibiotics.[9] This is also vital for empirical treatment of patients—a common practice where medical microbiology laboratory diagnostic capacity is limited.[10]

The present study was carried out to investigate the bacteria and their prevalence in clinical samples submitted for microbiological analysis from the outpatient clinics at a tertiary teaching hospital in Edo State, Nigeria, to determine the antimicrobial susceptibility pattern of isolates and describe the patients' age and sex distribution for the isolates.


   Materials and Methods Top


Study area

The study was carried out in a 375-bed tertiary teaching hospital in rural Edo State, South-South Nigeria. Located along the Benin-Abuja expressway in Irrua, the headquarters of Esan Central Local Government Area (LGA) in Edo Central Senatorial District, the hospital serves the state and neighboring states of Delta, Kogi, and Ondo. The hospital is one of the two tertiary health institutions in the state and provides a comprehensive spectrum of clinical, promotive, preventive, and rehabilitative services to the people in the Edo state, particularly the Esan Central Senatorial District, and neighboring states.

Study design

The study was a retrospective cross-sectional analysis of medical microbiology laboratory test results of samples collected between January 2016 and December 2019. Bacteriological data over this period were retrieved from the laboratory result logbook using a pre-designed data extraction sheet. Age and sex of the patient, clinic name, specimen type, bacteriological culture, and antibiotic susceptibility profile were documented.

Sample collection and characterization

Specimens were collected from all patients attending the outpatient clinics of the hospital over the study period. These clinical specimens were collected using standard methods of specimen collection and were in line with the standard operating procedures in use in the laboratory.[11] They were delivered to the laboratory within 1 hour of collection and the analysis was started the same day. Inoculated agar plates were incubated at 37°C for 16–48 hours. Culture and identification of bacteria followed the standard operating procedures of the Medical Microbiology Department. Culture media used for isolation of the microorganisms included blood agar, MacConkey agar, Cystine–lactose–electrolyte-deficient (CLED) agar, and chocolate agar. Presumptive identification was based on Gram staining reaction and colony characteristics. Discrete colonies were subcultured for 24 hours at 37°C on nutrient agar to purify the isolates. Confirmatory tests were based on the enzymatic and biochemical properties of the pure colonies. Gram-negative rods were identified by biochemical tests including oxidase, motility, indole, citrate, lysine decarboxylase, urease, and triple sugar iron (TSI). Gram-positive cocci were identified based on their Gram reaction, catalase, and coagulase test results. All procedures were carried out in line with the standard microbiological methods.[12],[13] Patients' age and sex were also collected.

Antibiotic agents

Antibiotic disks containing Ceftazidime CAZ (30 μg), Cefuroxime CRX (30 μg), Cefixime CMX (5 μg), Gentamicin GEN (10 μg), Ofloxacin OFL (5 μg), Amoxicillin–clavulanic acid AUG (30 μg), nitrofurantoin NIT (300 μg), Cloxacillin CXC (5 μg), Ceftriaxone CTR (30 μg) Tetracycline TE (30 μg), Streptomycin S (30 μg), Clindamycin DA (30 μg), Erythromycin ERY (5 μg), Nalidixic acid NA (30 μg), Ceftazidime CAZ (30 μg), Chloramphenicol C (30 μg), amoxycillin AMC (10 μg), cotrimoxazole SXT (25 μg), Azithromycin AZM (15 μg), Retapamulin RET (2 μg), Ciprofloxacin CIP (30 μg), and Meropenem MEM (10 μg) were chosen based on local utilization patterns obtained from Oxoid Laboratories (Oxoid, UK) and used as instructed by the manufacturer.

Antibiotic susceptibility testing

Antimicrobial susceptibility testing was carried out using the Kirby-Bauer disk diffusion method and was reported in conformity with the Clinical and Laboratory Standards Institute (CLSI) guidelines (CLSI, 2017). After adjustment to 0.5 McFarland, a standard inoculum of each isolate was swabbed on a Mueller-Hinton agar plate using a sterile cotton swab stick. Using sterile forceps, the antibiotic disks were placed aseptically on the seeded agar plates and incubated in an inverted position at 35°C for 16–18 hours, and thereafter, examined for clear zones of inhibition. The inhibition zone diameters (IZD) around each antibiotic disk were measured using a calibrated transparent ruler and recorded in millimeters. A standardized table was used to determine if each bacterium was 'resistant', 'intermediate,' or 'sensitive.'[14] For analysis, isolates with intermediate or resistant results were merged as resistant.[15]

Quality control of culture and susceptibility testing were achieved using American Type Culture Collection (ATCC) standard reference strains Staphylococcus aureus (ATCC-25923),  Escherichia More Details coli (E. coli) (ATCC-25922), and Pseudomonas aeruginosa (ATCC 25853). Negative control was by a random selection of uninoculated culture media and incubation overnight for evidence of growth.

Data analysis

Data were analyzed with SPSS version 20 (IBM Corporation, Armonk, NY, USA). Proportions of bacterial isolates and antibiotic sensitivities and resistances were presented as frequency tables. Prevalence rates of bacteria isolates were calculated as the frequency of identification of the bacterial species divided by the total number of all the bacteria species identified. Resistance rates were calculated for each antibiotic and each bacterial isolated by dividing the number of resistant isolates by the total number of isolates.[16] The overall resistance rate of each antibiotic were calculated as the number of bacteria resistant to antibiotics over the total number of bacteria isolates tested.[17] Chi-square test of association was used to compare the proportion of bacterial isolates with patients' age and sex, with the level of significance P set as < 0.05. Multiple antibiotic resistance (MAR) index was calculated for each isolate as the number of antibiotics to which the isolate is resistant/the total number of antibiotics against which the isolate was tested.[18]

Ethical consideration

Ethical approval was obtained from the Ethics Committee of Irrua Specialist Teaching Hospital. Patients' names were not entered into the data extraction sheet, and all other required demographic information, as well as information on bacterial isolates, were kept confidential by the researchers.


   Results Top


A total of 3,247 patient specimens from the outpatient clinics met the eligibility criteria. Out of 3,247 samples, 967 (42.5%) from the general outpatient clinic (GOPD), 850 (52.3%) from the Children's emergency room (CHER), 444 (13.7%) from the Accident and Emergency, and 164 (5.1%) from the Medical Outpatient Clinic (MOPD). Other clinics from where samples were collected are shown in [Figure 1].
Figure 1: Clinic name: GOPD:: General outpatient clinic; CHER: Children's emergency room; A&E: Accident and Emergency; PNC: Post-natal clinic; MOPD: Medical outpatient clinic; MCH: Maternal and child health unit; SOPC: Surgical outpatient clinic; Gynae clinic: Gynecology clinic; POPC: Pediatric outpatient clinic; OOPD: Orthopedic outpatient clinic; COPD: Consultants outpatient clinic; ENT: Ear nose and throat clinic

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The samples were from females 1,581 (48.7%) and from males 1,666 (51.3%). The <9-year range group made up the highest proportion of patients accounting for 43.0%. Urine was the predominant specimen submitted 2,058 (59.3%); followed by blood 366 (19.6%)[Table 1].
Table 1: Distribution of clinical specimens (n=994)

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Nine hundred and ninety-four (30.6%) samples showed a significant microbial growth while 10 (0.3%) showed mixed growth and were excluded from further analysis. The remaining samples 2,243 (69.1%) either had no growth or insignificant growth. Four hundred and thirty-six (43.9%) isolates were gram-positive, while 558 (56.1%) isolates were gram-negative. Urine yielded the most isolates 337 (33.9%), followed by wound swab 149 (15.0%), throat swab 120 (12.1%), and sputum 115 (11.6%) [Table 1]. The most common bacterial species isolated were E. coli 286 (28.8%), followed by Staphylococcus aureus 239 (24.0%), and Streptococcus pneumoniae 188 (18.9%). Others included Citrobacter species 50 (5.0%), Enterobacter species 62 (6.2%), Klebsiella species 53 (5.3%),  Moraxella More Details species 6 (0.6%), Proteus vulgaris 32 (3.2%), Pseudomonas aeruginosa 67 (6.7%), Serratia marcescens 1 (0.1%), Providencia species 1 (0.1%), coagulase-negative Staphylococcus species 6 (0.6%), and Xanthomonas species 1 (0.1%). Significantly, more blood samples and wound swabs were received from males compared to females (P = 0.02 and P = 0.04 respectively), and urine from females compared to males (P = 0.03). There was no significant association between sample type and sex for other samples. Isolates of E. coli were significantly more predominant in samples from females compared to males (P = 0.03) and Pseudomonas species in males compared to females (P < 0.01). [Table 2]
Table 2: Bivariate analysis of specimen type and isolates by gender of the patient

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E. coli was the most frequently isolated pathogen accounting for 28.8% (286/994) of all isolates and 51.3% of gram-negative pathogens (286/558). Staphylococcus aureus 239 (54.8%) was the predominant gram-positive isolate.

Staphylococcus aureus was the predominant isolate from blood 35 (62.5%), ear swab 24 (42.1%), endocervical swab 20 (57.1%), high vaginal swab (HVS) 15 (48.4%), pus aspirate 9 (52.9%), seminal fluid 4 (80.0%), urethral swab 4 (80.0%), and wound swab 64 (42.7%). E. coli was the predominant isolate in urine 192 (57.0%) and stool 41 (82.0%). The predominant isolates from throat and sputum were Streptococcus pneumoniae 98 (81.7%) and 72 (62.6%), respectively. Cerebrospinal fluid yielded Enterobacter species 1 (100.0%) [Table 3].
Table 3: Distribution of bacterial isolates from clinical specimens (n=994)

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Gram-positive pathogens generally showed high-resistant rates to cotrimoxazole, tetracycline, cloxacillin, erythromycin (93.1%, 86.4%, 72.5%, and 68.1% respectively), and least resistance to meropenem (0.0%), retapamulin (0.0%), azithromycin (0.0%), cefixime (28.0%), ceftazidime (35.8%), ceftriaxone (24.5%), and chloramphenicol (30.6%). All isolates had a MAR > 0.2 [Table 4].
Table 4: Antibiotic resistance profile of gram -positive bacteria isolates

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The gram-negative isolates showed high rates of resistance to erythromycin (95.6%), amoxycillin (100.0%), tetracycline (88.3%), cloxacillin (96.9%), amoxicillin–clavulanic acid (96.9%), and cotrimoxazole (93.2%). The lowest resistances were shown against nitrofurantoin (23.2%), cefixime (17.5%), and meropenem (0.0%). All isolates had MAR index >0.2 [Table 5].
Table 5: Antibiotic response to gram-negative organisms

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The resistance profiles of the isolates showed that all the isolates were resistant to at least one or more antimicrobial agents and a majority (75%) of the isolates were resistant to more than three antimicrobial agents.


   Discussion Top


In the study, the majority of the specimens had no bacterial growth possibly because the patients may have taken antibiotics before coming to the clinic as the practice of self-medication is high in the country.[19] The higher proportion of isolates from females tallies with the findings from other studies.[20],[21]

In this study, gram-positive pathogens were the predominant isolates, unlike other studies where gram-negative pathogens dominated.[6],[9],[22],[23] The high prevalence of Streptococcus pneumoniae in respiratory specimens has been similarly reported in other studies[24],[25] at variance with a study in India where Klebsiella pneumoniae was the predominant isolate from respiratory tract specimens.[22] Streptococcus pneumoniae is responsible for 80% of community-acquired pneumonia across all age groups.[25],[26] Streptococcus pneumoniae was found to have high rates of resistance to readily available first-line antibiotics and low rates of resistance to cephalosporins, carbapenems, ofloxacin, and chloramphenicol. This finding corroborates a report from the Nigeria Centre for Disease Control.[27] A high rate of resistance to streptomycin is corroborated by other studies.[9] Contrary to this, Beyene et al. (2015)[24] in their study in Ethiopia reported that Streptococcus pneumoniae isolates showed high resistance rates to oxacillin and low resistance to common first-line antibiotics. High rates of resistance to carbapenems and quinolones have also been documented.[6]

The most common pathogen isolated from blood specimen was Staphylococcus aureus in agreement with other studies.[9],[23] The higher prevalence in the younger age group has similarly been documented.[28] Staphylococcus aureus showed high resistance to amoxycillin, tetracycline, cotrimoxazole, and low resistance to Gentamicin, meropenem, and amoxycillin-clavulanic acid. Similar results have been reported.[23],[24]

The high prevalence of E. coli isolates from urine specimen has been reported in other studies,[29],[30],[31] and contrary to studies where Staphylococcus aureus[32] and Klebsiella spp[6] were the dominant uropathogens, E. coli was significantly isolated more from females than males as similarly reported.[23],[29],[31] E. coli was found to be highly resistant to tetracycline, cotrimoxazole, amoxycillin, and erythromycin and sensitive to nitrofurantoin, gentamicin, amoxycillin-clavulanic acid, and the extended-spectrum cephalosporins, in tandem with findings from other studies.[17],[24],[27],[33],[34] Nitrofurantoin, Gentamicin, and cephalosporins are indeed recommended for the empirical treatment of uncomplicated urinary tract infections and are available as oral preparations.[35] On the other hand, high resistance to nitrofurantoin was observed in a study carried out in Cameroon.[30] Klebsiella species, the second common uropathogen in this study, showed high resistance to nalidixic acid and tetracycline and sensitivity to the cephalosporins. In contrast, high levels of resistance to cephalosporins have been documented in some studies.[6],[10] The isolation of E. coli and Klebsiella species as primary pathogens responsible for urinary tract infection in this study agrees with other studies.[36]

The frequency of isolation of other gram-negative pathogens (Citrobacter species, Proteus species, Pseudomonas aeruginosa, Serratia marcescens, Providencia species, and Xanthomonas species) was low, consistent with other studies[32] and susceptibility ranged from highly sensitive to cephalosporins to resistant to common first-line antibiotics in tandem with some studies,[34] and contrary to another study where resistance to cephalosporins was high.[6]

The finding in this study that gram-positive and gram-negative bacterial pathogens are generally resistant to common inexpensive antibiotics is a reflection of the damage caused by inappropriate prescription practices including over-prescription and under-prescription, misuse by the public fueled by the availability of these cheap antibiotics over-the-counter and the sale of substandard antibiotics. This is in addition to the selection pressures that cause mutations and the spread of resistant strains in the community. Of note is the rising resistance to cefuroxime as has been documented.[37]

Enterococcus faecium, Staphylococcus aureus, Klebsiella pneumoniae, Acinetobacter baumannii, Pseudomonas aeruginosa, and Enterobacter species have been given the acronym ESKAPE as they tend to be multidrug-resistant and capable of “escaping” the biocidal action of antimicrobial agents.[38] They pose a threat in healthcare settings particularly among patients on invasive devices such as ventilators and blood catheters causing severe, and often, deadly bloodstream infections and pneumonia. Bacteria within the group have been demonstrated to be resistant to many antibiotics, including carbapenems and third-generation cephalosporins.[12] In this study, four of the ESKAPE pathogens were identified from the clinical samples together making up 24.2% of the total isolates in the study. They included Staphylococcus aureus (15.9%), Klebsiella pneumoniae (6.2%),  Pseudomonas aeruginosa Scientific Name Search .4%), and Enterobacter species (0.7%).

The study has some limitations. Clinical specimens were collected from attendees in a tertiary hospital—a situation that may introduce selection bias as they may have different health-seeking behavior from persons who seek care from other levels of healthcare. The study utilized secondary data so it was not possible for an analysis of the clinical profile of the study participants to be carried out. Also, the extended-spectrum beta-lactamase status of the isolates from the study was not assessed. The influence of antibiotic medication use prior to hospital visitation on pathogen culture could not be assessed.


   Conclusion Top


Gram-positive bacteria predominated among the outpatient samples tested. Gram-positive bacteria showed high resistance rates to cotrimoxazole, erythromycin, cloxacillin, tetracycline, amoxycillin-clavulanic acid, and amoxycillin. Gram-negative bacteria showed high resistance to tetracycline, cotrimoxazole, and cloxacillin. The high rate of resistance to cefuroxime observed may be due to its availability over-the-counter, oral formation, poor dosing, and poor compliance among the outpatient population. Prescribers are left with a limited range of routinely used antibiotics to choose from as well as the the increasing risk of resistance developing in the more expensive newer generation antibiotics. Hospital pharmacies should be stocked to reflect the current patterns of sensitivity to available antibiotics. Treatment guidelines should reflect the antibiotic resistance pattern to community-acquired infections. Interventions to reduce resistance including restrictions on over-the-counter sale of antibiotics should be strengthened. First-line antibacterial drugs showing marked reduction of efficacy should be withdrawn and reintroduced after a few decades (antimicrobial recycling).

Acknowledgments

The authors are grateful to Professor Danny Asogun and PANDORA for funding the data collection and publication, the Resident Doctors, Medical Laboratory Scientists and laboratory technicians who took part in the laboratory analysis of the clinical samples, and the Irrua Speccilist Teaching Hospital staff who assisted with data retrieval.

Financial support and sponsorship

Funding for data collection, analysis, and article processing charge was provided as part of the PANDORA-ID-NET EDCTP Reg/Grant RIA2016E-1609. The grant is funded by the European and Developing Countries Clinical Trials Partnership (EDCTP2) program which is supported under Horizon 2020 the European Union's Framework Program for Research and Innovation. The views and opinions of the author herein do not necessarily state or reflect those of EDCTP.

Conflicts of interest

There are no conflicts of interest.



 
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    Tables

  [Table 1], [Table 2], [Table 3], [Table 4], [Table 5]



 

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