DISTRIBUTION AND ANTIBACTERIAL RESISTANCE OF WOUND PATHOGENIC BACTERIA IN PATIENTS OF SANA’A HOSPITALS, YEMEN

Mohammed Mohammed Al-Shehari1image, Khaled Saad Abdulrahman Al-Khamesy2image, Khaled Abdulkareem Al-Moyed3image, Hassan Abdulwahab Al-Shamahy3,4image, Ahmed Mohamed Al-Haddad5image, Azhar Azher Mohammed Al-Ankoshy6image, Emad Hassan Al-Shamahi 1image

1General surgery Department, Faculty of Medicine and Health Sciences, Sana’a University.

2ENT Department, Faculty of Medicine and Health Sciences, Sana’a University, Republic of Yemen.

3Medical Microbiology and Clinical Immunology Department, Faculty of Medicine and Health Sciences, Sana’a University.

4Medical Microbiology department, Faculty of Medicine, Genius University for Sciences &  Technology, Dhamar city.

5Department of Medical Microbiology, Faculty of Medicine and Health Sciences, Hadhramout University, Republic of Yemen.

6Physiology Department, Jabir ibn Hayyan Medical University, Faculty of Medicine, Iraq.

ABSTRACT 

Background and objectives:  Cutaneous wounds are a common symptom in human medical practice. Understanding the physiology of the wound healing process and using the right therapeutic intervention are necessary for managing the existing healing in wound patients. Infection can cause wounds to take longer to heal, cosmetic surgery outcomes to be less satisfactory, and medical expenses to rise. Due to the dearth of studies in Yemen and other Arabic-nations that describe the different forms, locations, and current understanding of the bacterial causes of wound infection. So, general care hospitals in Sana'a, Yemen, undertook a study to identify the different types, locations, and prevalence of wound contamination caused by various bacteria, as well as to examine the antibiotic susceptibility pattern of wound-isolated bacteria.

Subjects and methods: This cross-sectional study was carried out among 699 wound patients with clinically diagnosed wound infections at NCPHL during the years 2021-2022. Pus and wound swab samples were processed using standard microbiological procedures at NCPHL. A modified Kirby Bauer disc diffusion technique was used to investigate the susceptibility of bacteria to various antibiotics. From pre-questionnaire and laboratory records of the NCPHL, clinical information about patients was gathered, including the types and locations of wounds.

Results: Out of 699 samples, 580 (82.98%) were positive for bacterial cultures. The most common wound was postoperative (30.8%), followed by diabetic foot ulcer (24.5%), traumatic wound (18.7%) and bullet wound (16.9%), while it was less frequent for caesarean section (5.7%) and sharp cut (2%). The present study revealed that Gram-negative bacteria were less frequent than Gram-positive bacteria (43.3% vs. 56.7%). Also gram-positive bacteria show a very high percentage (92.1%) of multidrug resistant (MDR) in compared to gram-negative bacteria (37.8%).

Conclusion: In the current study's wound bacteriological profile, Staphylococcus aureus was shown to be highly prevalent, followed by Escherichia coli, S. epidermidis (CoNS), Acinobacter spp., and Pseudomonas aeruginosa. Their sensitivity to widely used antibiotics showed a pattern of decline. It is crucial to be informed of the current bacterial profile trend and to adjust the antibiotic schedule in accordance with sensitivity. 

Keywords: Antibiotic sensitivity, bacteriological profile, multidrug resistant (MDR), wound infections.

 

INTRODUCTION

 

A wound is a sudden onset of injury characterized by torn or punctured skin (an open wound), or bruising (a closed wound) from pressure or blunt trauma. In pathology, a wound is an acute injury that damages the epidermis of the skin1,2. A bacterial infection of a wound can impede healing and result in potentially fatal consequences1,3. Wounds that do not heal should be examined for their causes; several factors, including microbiological ones, may be responsible.  A baseline work-up comprises an assessment of the wound, its degree and severity1. Cultures are normally acquired from blood circulation or from the wound site1. One or more resistance mechanisms to each of the major classes of antimicrobial drugs have been detected in bacteria species isolated from a variety of body samples2,3. However, a wound offers a moist, warm, and nourishing environment that is complimentary for microbial colonization, growth, and infection4,5. An imbalanced cellular defense mechanism, prolonged inflammation, and a high bacterial burden are the hallmarks of infected wounds6. Escherichia coli, Pseudomonas aeruginosa, Staphylococcus aureus, Klebsiella pneumoniae, Proteus species, Streptococcus species, Streptococcus pyogenes, and Enterococcus species are the normal bacterial pathogens connected to wound infection7. Wound infections are a major cause of mortality in underdeveloped nations like Yemen; these infections are both preventable and treatable8. It has been discovered that the spectrum of bacteria that cause diseases and their susceptibility pattern differ depending on the environment8-14. Despite the fact that overusing antibiotics in both humans and animals has significantly sped up the emergence of resistance. Inhibiting particular antimicrobial processes, such as cell wall construction, nucleic acid synthesis, ribosome activity, protein synthesis, foliate metabolism, and cell membrane function, frequently results in the development of antibiotic resistance15,16. Access to and abuse of antimicrobials are further influenced by the lack of stringent laws governing their sales. Antimicrobials can normally be obtained without a prescription in underdeveloped nations17. Additionally, it is typical in Yemen to purchase antibiotics without a prescription from a licensed physician; this encourages public antibiotic overuse and aids in the formation and growth of antimicrobial resistance8. There have been a few studies done in Yemen to determine the antimicrobial resistance pattern of various samples18,19,20. Studies focusing on the types and locations of wounds as well as the resistance of bacterial isolates to antibiotics are extremely uncommon. Determining the types and locations of wounds, the prevalence of various bacteria in wound contamination, and studying the antibiotic suscepti-bility pattern of isolated bacteria were the goals of this study, which was conducted at public hospitals in Sana'a, Yemen.

 

SUBJECTS AND METHODS 

 

Study population:  This cross sectional study was carried out at National Center for Public Health Laboratories (NCPHL) belonged to Ministry of Public Health and Population. Patients were selected from both public and private hospitals in Sana'a, Yemen, over a two-year period and transferred to the department of microbiology at the National Center for Public Health Laboratories (NCPHL). Over the course of two years, from January 2021 to December 2022, 699 wound patients were gathered.

Clinical data: A thorough clinical history was gathered, including information on the patient's age, gender, length of discharge, type of wound, and prior antibiotic usage. While attending the NCPHL, data were gathered.

Wound specimens: Under sterile conditions, a sample of the wound fluids was taken from the wound using a cotton swab, or pus was drawn from the site using a sterile 21 G syringe. Following collection, the samples were immediately cultured directly in the proper medium.

Microbiological procedure: Three loops were inoculated: one to McConkey agar, one to chocolate agar, and one to blood agar. MacConkey agar and blood agar were incubated for 24 hours in an aerobic environment at 37°C. The inoculated chocolate agar was incubated for 24 hours at 37°C in a carbon dioxide-rich environment. Standard bacteriological techniques were then used to identify the growth20.

Antibiotic sensitivity: In Mueller-Hinton agar, the modified Kirby-Bauer disc diffusion technique was used to test the antibiotic sensitivity of bacterial isolates. The 2022 Clinical Laboratory Standards Institute recommendation was used to interpret the inhibitory zone diameter22,23.  

Ethical consideration: All participants gave their consent after being informed that participation was optional and that they might decline at any time without providing a justification.

Statistical analysis: The Epi Info statistical tool version 6 (CDC, Atlanta, USA) was used to analyze the data. Quantitative information, such as mean values and standard deviation (SD), should be communicated because the data were regularly distributed. Percentages were used to express the qualitative data. 

 

RESULTS

 

The study included 699 wounded patients, 53.2% of whom were males and 46.8% were females. Among them, 580 (82.98%) positive cultures were isolated.  Patients were distributed among all age groups with the highest rates in the age groups 16-25 years (24.7%), 26-35 years (27.2%) and ≥46 years (24.9%). The ages ranged from 1 to 75 years, with a mean of 34.4 ± 17.2 years (Table 1).  The most common type of wound was postoperative (30.8%), followed by diabetic foot ulcer (24.5%), traumatic wound (18.7%) and bullet wounds with 16.9% while it was less frequent for caesarean section (5.7%) and sharp cut (2%). Also, the most common body site of the wounds was foot (33.8%), abdominal part (27.3%), legs (15.6%), and hands (11.4%). While backside, breast, chest, and head and neck region were less frequent (Table 2).

Gram-negative bacteria were less frequent than Gram positive bacteria (43.3% vs 56.7%). About 14 different bacterial species were isolated and identified. S. aureus (41.6%) was the most common isolate followed by E. coli (12.2%), S. epidermidis (CoNS) (10.5%), P. aeruginosa (5.2%), Citrobacter freundii (5.3%). Proteus mirabilis (2.6%), K. pneumoniae (1.4%), and P. vulgaris (1.2%)  (Table 3).  S. aureus showed a high rate of resistant to penicillin G (85.5%), azithromycin (77.2%) and cefixime (99.2%).  CoNS showed a high rate of resistance to penicillin G (73.8%), azithromycin (45.9%) and cefixime (95.1%). S. pyogen showed a high rate of resistance to trimethoprim/ sulfamethoxa-zole (68.4%), rifampin (42.1%), ciprofloxacin (63.2%) and azithromycin (63.2%).  

S. pneumoniae showed a high rate of resistance to trimethoprim/sulfamethoxazole (50%), clindamycin (50%), penicillin g (50%) and azithromycin (50%) (Table 5).  E. coli showed a high rate of resistance more than 50% for co-trimoxazole (50.7%), amoxicillin-clavulanic acid (52.1%), ceftriaxone (54%), cefuroxime (56.3%), cefotaxime (66.2%), ciprofloxacin (54.9%) and ampicillin (88.7%). Citrobacter spp showed a high rate of resistance to co-trimoxazole (65.3%), amoxicillin-clavulanic acid (88%), ceftriaxone (78.7%), cefuroxime (89.3%), ceftazidime (74.7%), ciprofloxacin (64%) and ampicillin (94.7%).  Acinetobacter spp showed a high rate of resistance to ampicillin (87.1%), amoxicillin-clavulanic acid (77.4%), ceftriaxone (80.6%), cefuroxime (90.3%), ceftazidime (64.5%), ciprofloxacin (64.5%) and cefixime (90.3%). P. aeruginosa showed a high rate of resistance to ceftazidime (40%), cefixime (46.7%), cefotaxime (40%), and gentamicin (73.3%). Proteus spp showed a high rate of resistance to amoxillin clavulanate (40.9%), ampicillin (81.8%), trimethoprim/sulfame-thazole (77.3%), and colistin (86.3%).  

Enterobacter spp showed a high rate of resistance to cefuroxime (60%), amoxillin clavulanate  (80%), ampicillin (80%), and trimethoprim/sulfamethazole (70%) (Table 6). All isolated organisms from the wound specimens displayed varying degrees of multi-drug resistance (MDR), Gram-positive bacteria exhibit a very high percentage of MDR (92.1%) in comparison to gram-negative bacteria (37.8%). Among the gram-positive bacteria isolated, S. aureus (98%), followed by  CoNS  (91.8%), Showed the highest percentage of MDR (Table 7).  Among the gram-negative bacteria isolated, E. coli (57.7%), followed by Citrobacter spp (48%), showed the highest percentage of MDR (Table 8).

 

DISCUSSION

 

In the current study, 539 (77.1%) of the positive cultured samples showed mono- microbial growth, and 17% were negative for aerobic bacterial growth. This result is higher than that reported in Nepal24 who reported that 60% of wounds had positive growth of aerobic bacteria. The study included 699 patients, 53.2% of whom were males and 46.8% were females. In this study, male patients differentially outnumbered female patients from Rajput et al., study where female patients were predominant25 but other studies showed that wound infection was higher in males than in females as was our findings26,27. Patients were distributed among all age groups and the highest rates were in the age groups 16-25 years (24.7%), 26-35 years (27.2%) and 46 years (24.9%) and the ages of the patients ranged from 1 to 75 years, with a mean of 34.4±17.2 years. This differs with the study of Alam et al., where a higher prevalence of wound incidence has been reported among patients aged 60-80 years28. Also, our result was different from the study in Ethiopia, where 87.5% of wound infection was in patients ≥ 60 years of age29.

Gram-negative bacteria were marginally less common than Gram-positive bacteria, according to the current study (43.3% vs. 56.7%). These results differ from those observed in earlier studies, which showed 71.6% for Gram-negative and 28.4% for Gram-positive bacteria23.  Another distinction is that a prior study found that Gram-negative bacilli (70%) are more common than Gram-positive bacteria (30%), which is another difference. In addition, Gram-negative rods were the prevalent and main source of wound infection in a different study, and these results diverge from those of earlier investigations conducted in Asia and Africa30-32. Other studies, however, revealed about comparable frequencies of both Gram-positive and negative bacteria33. S. aureus in our study was one of the dominant bacteria in wound infections (41.6%) followed by E. coli (12.2%), and S. epidermidis (CoNS) (10.5%) and this result is consistent with some previous studies22. S. aureus may have a dominant cause since it is a typical component of human skin flora and is very easily spread through wounds.

According to Upreti et al.,34 13 distinct bacteria were recovered from pus samples, accounting for 82.5% of the bacterial growth, with S. aureus predominating (57.7%), followed by E. coli (11%), and CoNS (3%). Other microorganisms from pus samples that were discovered included P. aeruginosa (5.2%), C. freundii (5.3%). P. mirabilis (2.6%), K. pneumoniae (1.4%), and P. vulgaris (1.2%) (Table 5) is roughly similar to that reported in Iran28 in which S. aureus was the most common bacteria (49%) found in wound infections followed by E. coli (25.9%), Klebsiella spp. (9.5%), P. aeruginosa (8.6%), and Proteus spp. (4%). Current research showed that, with the exception of Proteus spp., colistin (CST) is the most effective antibiotic in sensitivity tests for most gram-negative bacteria. More than 96% of Proteus species were discovered to be colistin resistant. Resistant was 2.8% to 12.5% for other gram-negative bacteria isolates. In a sensitivity test, the carbapenem group (imipenem and meropenem) and piperacillin-tazobactam displayed the highest levels of activity against Proteus spp. A low percentage of resistance to carbapenems was also demonstrated by several other kinds of bacteria. Additionally, our results are comparable to those of a recent systematic review and meta-analysis35. In the current analysis, it was observed that vancomycin (VAN) followed linezolid (LZD) were the most active antimicrobials in sensitivity against gram-positive bacteria species includes S. aureus, coagulase negative staphylococci, S. pneumoniae and S. pyogens in which there was no vancomycin resistant coagulase negative staphylococci, S. pneumoniae and S. pyogens observed; however 2 (0.83%), S. aureus were resistant to vancomycin (Table 6). Moreover, Al-Khawlany et al., revealed that vancomycin was the most effective antibacterial against all the MRSA isolates recovered from infected wound38. Also, 1.2% S. aureus were found resistant against linezolid. Studies conducted in Bangladesh28, India36 and Colombia37 also revealed similar findings, where S. aureus was found to be less than resistant to linezolid. Since isolates with resistance to more than three classes of tested antibiotics were referred to be multi-drug resistant (MDR) isolates, (MDR index>3)9, therefore all isolated organisms from the wound specimens showed different level of MDR. This study also demonstrated that gram-positive bacteria from wound infections exhibit a very high percentage of MDR (92.1%) in comparison to gram-negative bacteria (37.8%).

Current study's overall MDR rate for gram-positive bacteria is higher than those done in Bangladesh (68.8%)28,  and Ethiopia38. The variation in the study population, where high MDR studies may have included hospitalized inpatients where greater MDR strains are anticipated, may be the likely explanation for such unevenness. In the current study patients consists of both hospitalized and non-hospitalized patients. All isolated organisms from the wound specimens displayed varying degrees of multi-drug resistance (MDR), which was defined as resistance to >3 classes of antimicrobial tested (MDR index >3). This study also demonstrated that gram-positive bacteria from wound infections exhibit a very high percentage of MDR (92.1%) in comparison to gram-negative bacteria (37.8%). In comparison to studies done in Bangladesh (68.8%)28 and Ethiopia38, the total MDR rate of gram positive bacteria in our study is greater. The variation in the study population, where high MDR studies may have included hospitalized inpatients where greater MDR strains are anticipated, may be the likely explanation for such unevenness.

Among the gram-negative bacteria isolated, E. coli (57.7%), followed by Citrobacter spp (48%), Showed the highest percentage of MDR, while Acinetobacter spp (12.9%), P. aeruginosa (13.3%), Klebsiella spp (25%), Proteus spp (27.3%) and Enterobacter spp (20%) showed the lowest percentage of MDR.  The overall MDR rate in the case of gram-negative bacteria in our study is (37.8%) is lower than the previously conducted studies in Yemen and elsewhere39-44. In Yemen, it is usual practice to provide antibiotics orally, which may limit bloodstream absorption of the drugs. Bacteria may acquire resistance if long-term oral antibiotic usage is undertaken. Inflamed wounds' MDR bacterial diversity may also be explained by a variety of factors, such as demography, age disparities, gender, length of hospitalization, and prior antibiotic use2,9,13. Hospitalization may also have a significant impact on the occurrence and type of MDR bacteria because patients are susceptible to nosocomial infections that are resistant to several prescription antibiotics38,39.

Limitations of the study 

This document focuses on bacterial wound infections, but other microorganisms such as fungi or viruses that may cause wound infections have not been studied and verified. It is known that the bacteria multiply, the healing is disrupted, and the wound tissues are damaged, and this leads to a local infection, but the bacteria present in the wound may cause other problems due to the spread of infection, which causes a systemic disease, and this was not studied in the current study. Further research is required to fully understand the factors involved in the transition from colonization to local infection and this may facilitate future guidance regarding the timing and nature of intervention for wound treatment.

 

CONCLUSION

 

This study has attempted to capture and address microbiological features that are crucial to the successful management of bacteria in wounds by giving a complete examination of wound microbiology, along with current opinion and issues regarding wound assessment and therapy.  In the current study's wound bacteriological profile, S. aureus was shown to be highly prevalent, followed by E. coli, S. epidermidis (CoNS), Acinobacter spp., and P. aeruginosa. Their sensitivity to widely used antibiotics showed a pattern of decline. It is crucial to be informed of the current bacterial profile trend and to adjust the antibiotic schedule in accordance with sensitivity. Additionally, this study made the case for the necessity of routinely monitoring the clinical isolates' antibiotic sensitivity in order to control the spread of microorganisms that are resistant to antibiotics and to determine the most effective antibacterial treatments. Glycopeptide (vancomycin) and oxazolidinone (linezolid) antibiotics have been discovered to be efficient against gram-positive isolates. Contrarily, polypeptides and carbapenems were found to be effective against the majority of gram-negative isolates. Also,  a significant proportion of MDR among frequently isolated bacteria was discovered in this investigation, which is a severe, worrying problem.

 

ACKNOWLEDGEMENTS 

 

We appreciate the help from the National Center for Public Health Laboratories (NCPHL), Sana'a, Yemen, especially Dr. Fuad Ali Bazel Al-Qupti, director of the Microbiology Department. 

 

CONFLICT OF INTEREST 

 

There is no conflict of interest around this work.

 

AUTHOR CONTRIBUTIONS

 

The research was given their unanimous approval after being revised, drafted, and data-analyzed by all authors.

 

REFERENCES

 

  1. Singhal H, Kaur K. Talavera F, Friedman AL (eds.). "Wound infection" wound infection clinical presentation. medscape 2023.https://emedicine.medscape.com/article/188988-clinical
  1. Shahidullah M, Yusuf M, Khatun Z, Ara U, Mitul M. Antibiotic sensitivity pattern of bacterial isolates from different clinical specimens: Experience at NICVD, Dhaka. Cardiovasc J 2012; 5:67e72.https://doi.org/10.3329/cardio.v5i1.12276
  1. Moges F, Endris M, Mulu A, et al. The growing challenges of antibacterial drug resistance in Ethiopia. J Glob Antimicrob Resist 2014; 2:148e54.https://doi.org/10.1016/j.jgar.2014.02.004
  1. Ohalete CN, Obi RK and EmeaKoroha MC. Bacteriology of different wound infection and their antimicrobial susceptibility patterns in Imo State, Nigeria. World J Pharm Sci 2012; 13, 1155-1172.
  2. Du Y, Han S, Zhou Y, Chen HF, Lu YL, Kong ZY, Li WP. Severe wound infection by MRCNS following bilateral inguinal herniorrhaphy. BMC Infect Dis 2023; 7; 23(1):85.https://doi.org/10.1186/s12879-023-08039-9
  1. Zhao G, Hochwalt PC, Usui ML, Underwood RA, Singh PK, James GA, et al. Delayed wound healing in diabetic (db/db) mice with Pseudomonas aeruginosa biofilm challenge: a model for the study of chronic wounds. Wound Repair Regen 2010; 18:467e77.https://doi.org/10.1111/j.1524-475X.2010.00608.x
  1. Sani RA, Garba SA, Oyewole OA, Ibrahim A. Antibiotic resistance profile of gram positive bacteria isolated from wound infections in Minna, Bida, Kontagora and Suleja area of Niger state. Int J Health Sci 2012; 2:19e22.https://doi.org/10.5923/j.health.20120203.01
  1. Al-Safani AA, Al-Shamahy HA, Al-Moyed KA. Prevalence, antimicrobial susceptibility pattern and risk factors of MRSA isolated from clinical specimens among military patients at 48 medical compound in Sana’a city-Yemen. Universal J Pharm Res 2018; 3(3):40-44.https://doi.org/10.22270/ujpr.v3i3.165
  1. French GL. The continuing crisis in antibiotic resistance. Int J Antimicrob Agents 2010; 36:S3e7.https://doi.org/10.1016/S0924-8579(10)70003-0
  1. Abbas AM, Al-Kibsi TAM, Al-Shamahy HA, et al. Characterization and antibiotic sensitivity of bacteria in orofacial abscesses of odontogenic origin. Universal J Pharm Res 2020; 5(6):36-42. https://doi.org/10.22270/ujpr.v5i6.510
  2. Al-Akwa AAY, Zabara AQM, Al-Shamahy HA, et al. Prevalence of Staphylococcus aureus in dental infections and the occurrence of MRSA in isolates. Universal J Pharm Res 2020; 5(2):1-6. https://doi.org/10.22270/ujpr.v5i2.384
  3. Al-Eryani SA, Alshamahi EYA, Al-Shamahy HA, Alfalahi GHA, Al-Rafiq AA. Bacterial conjunctivitis of adults: Causes and ophthalmic antibiotic resistance patterns for the common bacterial isolates. Universal J Pharm Res 2021; 6(1):25-28. https://doi.org/10.22270/ujpr.v6i1.535
  4. AL-Haddad KA, Ali Al-Najhi MM, Al-Shamahy HA, et al. Antimicrobial Susceptibility of Aggregatibacter Actino-mycetemcomitans Isolated from Localized Aggressive Periodontitis (Lap) Cases. J Dent Ora Heal Ad Re: 2021; 103.
  5. Al-Haifi AY, Al Makdad ASM, Salah MK, Al-Shamahy, Al Shehari WAA. Epidemiology, bacterial profile, and antibiotic sensitivity of lower respiratory tract infections in Sana’a and Dhamar city, Yemen. Universal J Pharm Res 2020; 5 (2):1-6. https://doi.org/10.22270/ujpr.v5i2.386
  6. Kohanski MA, Dwyer DJ, Collins JJ. How antibiotics kill bacteria: from targets to networks. Nat Rev Microbiol 2010; 8:423e35. https://doi.org/10.1038/nrmicro2333
  7. Bouki C, Venieri D, Diamadopoulos E. Detection and fate of antibiotic resistant bacteria in wastewater treatment plants: A review. Ecotoxicol Environ Saf 2013;91:1e9.https://doi.org/10.1016/j.ecoenv.2013.01.016
  1. Sakeena MHF, Bennett AA, McLachlan AJ. Non-prescription sales of antimicrobial agents at community pharmacies in developing countries: A systematic review. Int J Antimicrob Agents 2018; 52:771e82.https://doi.org/10.1016/j.ijantimicag.2018.09.022  
  1. Alshamahi EYA, Al-Shamahy HA, Musawa YA. Bacterial causes and antimicrobial sensitivity pattern of external ocular infections in selected ophthalmology clinics in Sana’a city. Universal J Pharm Res 2020; 5(3):12-16.https://doi.org/10.22270/ujpr.v5i3.329
  1. Saleh A AM, Al-Shamahy HA, Al-Hrazi RAM,  et al. Biofilm formation and antibiotic susceptibility of uropathogens in patients with catheter associated urinary tract infections in Ibb city -Yemen. Universal J Pharm Res 2020; 4 (6):1-6. https://doi.org/10.22270/ujpr.v4i6.329
  2. Alhlale MF, Humaid A, Saleh AH, et al. Effect of most common antibiotics against bacteria isolated from surgical wounds in Aden governorate hospitals, Yemen. Universal J Pharm Res 2020; 5(1): 21-24.https://doi.org/10.22270/ujpr.v5i1.358  
  1. Cheesbrough M. District laboratory practice in tropical countries. Cambridge: Cambridge University Press; 2010.https://doi.org/10.1017/CBO9780511581304  
  1. Church DL. Biochemical tests for the identification of aerobic bacteria. Clinical Microbiology Procedures Handbook. 4th Washington, DC: American Society of Microbiology; 2016:3-17.
  2. Wayne PA. Performance Standards for Antimicrobial Disc Susceptibility Testing. 30th edition, National Committee for Clinical Laboratory Standards; 2022.
  3. Kumari K. Pattern of bacterial isolates and antibiogram from open wound infection among the indoor patients of Bir Hospital. Master degree.https://elibrary.tucl.edu.np/handle/123456789/9392
  1. Rajput A, Singh KP, Kumar V, Sexena R, Singh RK. Antibacterial resistance pattern of aerobic bacteria isolates from burn patients in tertiary care hospital. Biomed Res 2008;19 (1)1-6. http://www.alliedacademies.org/biomedical-research/archive
  2. Gelaw A, Gebre-Selassie S, Tiruneh M, Mathios E, Yifru S. Isolation of bacterial pathogens from patients with postoperative surgical site infections and possible sources of infections at the University of Gondar Hospital, Northwest Ethiopia. J Environ Occup Sci 2014;3(2): 103–8.https://doi.org/10.5455/jeos.20140512124135
  1. Goswami NN, Trivedi HR, Goswami AP, Patel TK, Tripathi CB. Antibiotic sensitivity profile of bacterial pathogens in postoperative wound infections at a tertiary care hospital in Gujarat, India. J Pharmacol Pharmacother 2011; 2(3):158-64.https://doi.org/10.4103/0976-500X.83279
  1. Alam MM, Islam MN, Hawlader MDH, et al. Prevalence of multidrug resistance bacterial isolates from infected wound patients in Dhaka, Bangladesh: A cross-sectional study. Int J Surg Open 2021; 56-62.https://doi.org/10.1016/j.ijso.2020.12.010 
  1. Thanni LO, Osinupebi OA, Deji-Agboola M. Prevalence of bacterial pathogens in infected wounds in a tertiary hospital, 1995-2001: Any change in trend? J Natl Med Assoc 2003; 95(12):1189-95. PMID: 14717475
  2. Kassam NA, Damian DJ, Kajeguka D, Nyombi B, Kibiki GS. Spectrum and antibiogram of bacteria isolated from patients presenting with infected wounds in a tertiary hospital, Northern Tanzania. BMC Res Notes 2017; 10 (1).https://doi.org/10.1186/s13104-017-3092-9
  1. Yang H, Wang WS, Tan Y, Zhang DJ, Wu JJ, Lei X. Investigation and analysis of the characteristics and drug sensitivity of bacteria in skin ulcer infections. Chinese J Traumatol 2017; 20 (4), 194–197.https://doi.org/10.1016/j.cjtee.2016.09.005 
  1. Moges F, Eshetie S, Abebe W, et al. High prevalence of extended-spectrum beta-lactamase-producing gram-negative pathogens from patients attending Felege Hiwot comprehensive specialized Hospital, Bahir Dar, Amhara region. PLoS ONE 2019; 14 (4), e0215177.https://doi.org/10.1371/journal.pone.0215177
  1. Asres GS, Legese MH, Woldearegay GM. Prevalence of multidrug resistant bacteria in postoperative wound infections at Tikur Anbessa Specialized Hospital, Addis Ababa, Ethiopia. Arch Med 2017; 9(4):12-24.
  2. Upreti N, Rayamajhee B, Sherchan SP, Choudhari MK, Banjara MR. Prevalence of methicillin resistant  aureus, multidrug resistant and extended spectrum β-lactamase producing gram negative bacilli causing wound infections at a tertiary care hospital of Nepal. Antimicrob Resist Infect Control 2018 Oct 8; 7:121.https://doi.org/10.1186/s13756-018-0408-z
  1. Azzopardi EA, Azzopardi E, Camilleri L, Villapalos J, Boyce DE, Dziewulski P, et al. Gram negative wound infection in hospitalised adult burn patientssystematic review and metanalysis-. PLoS One 2014; 9:e95042.https://doi.org/10.1371/journal.pone.0095042
  1. Kulkarni AP, Nagvekar VC, Veeraraghavan B, Warrier AR, Deepak TS, Ahdal J, et al. Current perspectives on treatment of gram-positive infections in India: What is the way forward? Interdiscip Perspect Infect Dis 2019.https://doi.org/10.1155/2019/7601847
  1. Vanegas Múnera JM, Ocampo Ríos AM, Urrego DM, Jim_enez Quiceno JN. In vitro susceptibility of methicillin-resistant Staphylococcus aureus isolates from skin and soft tissue infections to vancomycin, daptomycin, linezolid and tedizolid. Braz J Infect Dis 2017;21:493e9.https://doi.org/10.1016/j.bjid.2017.03.010
  1. Godebo G, Kibru G, Tassew H. Multidrug-resistant bacterial isolates in infected wounds at Jimma University specialized hospital, Ethiopia. Ann Clin Microbiol Antimicrob 2013; 12:17. https://doi.org/10.1186/1476-0711-12-17
  2. Al-Shami HZ, Al-Haimi MA, Al-Shamahy HA, et al. Patterns of antimicrobial resistance among major bacterial pathogens isolated from clinical samples in two tertiary’s hospitals, in Sana’a, Yemen. Universal J Pharm Res 2021; 6 (5):1-6. https://doi.org/10.22270/ujpr.v6i5.674
  3. Ishak AA, Alhadi AM, Al-Moyed KAA, Al-Shamahy HA. Childhood urinary tract infection: Clinical signs, bacterial causes and antibiotic susceptibility. Universal  J Pharm Res 2021; 6(4):1-6. https://doi.org/10.22270/ujpr.v6i4.643
  4. Kallen AJ, Hidron AI, Patel J, Srinivasan A. Multidrug resistance among Gram negative pathogens that caused healthcare-associated infections reported to the national healthcare safety network, 2006e2008. Infect Control Hosp Epidemiol 2010; 31:528e31. https://doi.org/10.1086/652152
  5. Taufik A, Wiweko A, Yudhanto D, Wardoyo EH, Habib P, Rizki M, Rosyidi RM. Bacterial infection and antibiotic resistance pattern in open fracture cases in Indonesia. Ann Med Surg (Lond). 2022 Mar 28;76:103510.https://doi.org/10.1016/j.amsu.2022.103510
  1. Edrees WH. Antibacterial susceptibility and Sider honey activity against isolated bacteria from wound patients attending at Al-Gmohori hospital in Hajja City, Yemen. Al-Razi Univ J Med Sci 2021; 5 (2):1-8.https://doi.org/10.51610/rujms5.2.2021.108
  1. Al-Khawlany RS, et al. Prevalence of methicillin-resistant aureus and antibacterial susceptibility among patients with skin and soft tissue infection at Ibb city, Yemen. PSM Microbiol 2021: 6(1): 1-11.https://psmjournals.org/index.php/microbiol/article/view/535