Original Research

Multicentre study of the burden of multidrug-resistant bacteria in the aetiology of infected diabetic foot ulcers

Adeyemi T. Adeyemo, Babatope Kolawole, Vincent O. Rotimi, Aaron O. Aboderin
African Journal of Laboratory Medicine | Vol 10, No 1 | a1261 | DOI: https://doi.org/10.4102/ajlm.v10i1.1261 | © 2021 Adeyemi T. Adeyemo, Babatope Kolawole, Vincent O. Rotimi, Aaron O. Aboderin | This work is licensed under CC Attribution 4.0
Submitted: 03 May 2020 | Published: 23 March 2021

About the author(s)

Adeyemi T. Adeyemo, Department of Medical Microbiology and Parasitology, Obafemi Awolowo University Teaching Hospitals, Ile-Ife, Nigeria
Babatope Kolawole, Department of Medicine, Faculty of Clinical Science, Obafemi Awolowo University, Ile-Ife, Nigeria
Vincent O. Rotimi, Department of Microbiology, Faculty of Medicine, Kuwait University, Kuwait City, Kuwait
Aaron O. Aboderin, Department of Medical Microbiology and Parasitology, Obafemi Awolowo University Teaching Hospitals, Ile-Ife, Nigeria; and, Department of Medical Microbiology and Parasitology, Faculty of Basic Medical Science, Obafemi Awolowo University, Ile-Ife, Nigeria

Abstract

Background: Infected diabetic foot ulcer (IDFU) is a public health issue and the leading cause of non-traumatic limb amputation. Very few published data on IDFU exist in most West African countries.

Objective: The study investigated the aetiology and antibacterial drug resistance burden of IDFU in tertiary hospitals in Osun state, Nigeria, between July 2016 and April 2017.

Methods: Isolates were cultured from tissue biopsies or aspirates collected from patients with IDFU. Bacterial identification, antibiotic susceptibility testing and phenotypic detection of extended-spectrum beta-lactamase and carbapenemase production were done by established protocols. Specific resistance genes were detected by polymerase chain reaction.

Results: There were 218 microorganisms isolated from 93 IDFUs, comprising 129 (59.2%) Gram-negative bacilli (GNB), 59 (27.1%) Gram-positive cocci and 29 (13.3%) anaerobic bacteria. The top five facultative anaerobic bacteria isolated were: Staphylococcus aureus (34; 15.6%), Escherichia coli (23; 10.6%), Pseudomonas aeruginosa (20; 9.2%), Klebsiella pneumoniae (19; 8.7%) and Citrobacter spp. (19; 8.7%). The most common anaerobes were Bacteroides spp. (7; 3.2%) and Peptostreptococcus anaerobius (6; 2.8%). Seventy-four IDFUs (80%) were infected by multidrug-resistant bacteria, predominantly methicillin-resistant S. aureus and GNB producing extended-spectrum β-lactamases, mainly of the CTX-M variety. Only 4 (3.1%) GNB produced carbapenemases encoded predominantly by blaVIM. Factors associated with presence of multidrug-resistant bacteria were peripheral neuropathy (adjusted odds ratio [AOR] = 4.05, p = 0.04) and duration of foot infection of more than 1 month (AOR = 7.63, p = 0.02).

Conclusion: Multidrug-resistant facultative anaerobic bacteria are overrepresented as agents of IDFU. A relatively low proportion of the aetiological agents were anaerobic bacteria.


Keywords

infection; diabetic foot; ulcers; multidrug-resistance; bacteria; antibiotic; anaerobic culture; samples

Metrics

Total abstract views: 7188
Total article views: 8690

 

Crossref Citations

1. Identifying multidrug-resistant organisms in diabetic foot ulcers: a study of risk factors and antimicrobial resistance genes
Mohd Saleem, Soha Abdallah Moursi, Tahani Nasser Almofeed Altamimi, Alharbi Mohammed Salem, Alwaleed Mohammad Alaskar, Sahar Adly Hassan Hammam, Ehab Rakha, Syed Muhammad Ozair Ilyas, Hamoud Abdulmohsin Al-Malaq, Metab Nasser Alshammari, Azharuddin Sajid Syed Khaja
World Journal of Microbiology and Biotechnology  vol: 41  issue: 1  year: 2025  
doi: 10.1007/s11274-024-04209-2

2. Investigation of Antimicrobial Potential of Medicinal Plants Against Pseudomonas aeruginosa
Nosheen Bibi, Shazia Perveen, Sumaira Kanwal, Fariha Latif, Rehmana Rashid, Sara Janiad, Iram Qadeer, Fatima Naseem, Abdullah R. Alanzi, Rashed N. Herqash, Imran Haider, Mehraj A. Abbasov, Sadaf Kayani, Mohd Asif Shah
Food Science & Nutrition  vol: 13  issue: 11  year: 2025  
doi: 10.1002/fsn3.70999

3. Aerobic pathogen profiles and antibiotic resistance in diabetic foot ulcers: Data from a Specialized Diabetes Center in Jordan
Dana Hyassat, Mohammad Al Gazo, Faris Bakri, Yousef Khader, Laith Baqain, Amro Al-Simadi, Eid Samara, Mohammad Al Masri, Jood Aladwan, Shiraz Mheidat, Dalia Hanash, Jamal Wadi Al Ramahi, Mohammad El-Khateeb, Kamel Ajlouni
Medicine  vol: 105  issue: 10  first page: e47908  year: 2026  
doi: 10.1097/MD.0000000000047908

4. Antimicrobial Remedies and Emerging Strategies for the Treatment of Diabetic Foot Ulcers
Muzammil Husain, Yogeeta O. Agrawal
Current Diabetes Reviews  vol: 19  issue: 5  year: 2023  
doi: 10.2174/1573399818666220228161608

5. Antimicrobial resistance in bacterial wound, skin, soft tissue and surgical site infections in Central, Eastern, Southern and Western Africa: A systematic review and meta-analysis
Edward J. M. Monk, Timothy P. W. Jones, Felix Bongomin, Winnie Kibone, Yakobo Nsubuga, Nelson Ssewante, Innocent Muleya, Lauryn Nsenga, V. Bhargavi Rao, Kevin van Zandvoort, Janelisa Musaya
PLOS Global Public Health  vol: 4  issue: 4  first page: e0003077  year: 2024  
doi: 10.1371/journal.pgph.0003077

6. Multidrug resistance, biofilm formation, and genetic determinants in diabetic foot infections from Uttar Pradesh, India: a clinical-microbiological insight from a prospective study
Mohd Saleem, Mohd Shahid Khan, Arslan Neyaz, Irfan Ahmad, Malak Yahia Qattan, Nadeem Ahmad
Naunyn-Schmiedeberg's Archives of Pharmacology  vol: 398  issue: 11  first page: 15965  year: 2025  
doi: 10.1007/s00210-025-04284-8

7. Antibiotic Resistance of Acinetobacter baumannii in Women with Polycystic Ovary Syndrome
Nawal B. Yazea, Dhuha M. Abbas, Rand Moshtaq Talib
International Journal of Innovative Science and Research Technology  first page: 2746  year: 2025  
doi: 10.38124/ijisrt/25may343

8. Bacterial profile and antimicrobial resistance patterns of infected diabetic foot ulcers in sub-Saharan Africa: a systematic review and meta-analysis
Fiseha Wadilo Wada, Michael Fekadu Mekonnen, Edlawit Desta Sawiso, Sitotaw Kolato, Lideta Woldegiorgis, Gemechu Kebede Kera, Ziad El-Khatib, Akililu Alemu Ashuro, Mulatu Biru, Minyahil Tadesse Boltena
Scientific Reports  vol: 13  issue: 1  year: 2023  
doi: 10.1038/s41598-023-41882-z

9. Prevalence of multidrug‐resistant bacterial infections in diabetic foot ulcers: A meta‐analysis
Shaoling Yang, Liye Hu, Yue Zhao, Guangzhe Meng, Sijia Xu, Rui Han
International Wound Journal  vol: 21  issue: 4  year: 2024  
doi: 10.1111/iwj.14864

10. Modification of Zn-Metal Organic Framework with Nano Silver as an Antibacterial Material for Diabetic Ulcers (In vitro)
Tri Ana Mulyati, Juni Ekowati, Yohanes Andy Rias, Binti Mu’ arofah, Fery Eko Pujiono
Research Journal of Pharmacy and Technology  first page: 4347  year: 2025  
doi: 10.52711/0974-360X.2025.00623

11. An Overview of Diabetic Foot Ulcers and Associated Problems with Special Emphasis on Treatments with Antimicrobials
Mirza Shahed Baig, Ahmadi Banu, Mehrukh Zehravi, Ritesh Rana, Sushil S. Burle, Sharuk L. Khan, Fahadul Islam, Falak A. Siddiqui, Ehab El Sayed Massoud, Md. Habibur Rahman, Simona Cavalu
Life  vol: 12  issue: 7  first page: 1054  year: 2022  
doi: 10.3390/life12071054

12. Bacterial isolates from diabetic foot ulcers and their antimicrobial resistance profile from selected hospitals in Addis Ababa, Ethiopia
Asegdew Atlaw, Habtamu Biazin Kebede, Abdurezak Ahmed Abdela, Yimtubezinash Woldeamanuel
Frontiers in Endocrinology  vol: 13  year: 2022  
doi: 10.3389/fendo.2022.987487

13. Antibiotic Stewardship in the Management of Infected Diabetic Foot Ulcer Disease in Less Developed Countries
Zulfiqarali G. Abbas, Raidah R. Gangji, Ilker Uçkay
Endocrinology, Diabetes & Metabolism  vol: 7  issue: 4  year: 2024  
doi: 10.1002/edm2.503

14. Modulations of the skin microbiome in skin disorders: A narrative review from a wound care perspective
Antonia Piazzesi, Matteo Scanu, Guido Ciprandi, Lorenza Putignani
International Wound Journal  vol: 21  issue: 10  year: 2024  
doi: 10.1111/iwj.70087

15. Assessment of the impact of pH of wound fluid on the associated microbial distribution in the cases of infected diabetic foot ulcer
Aradhana Singh, Shailendra Rai, Arvind Pratap, Tuhina Banerjee, Mumtaz Ahmed Ansari, Somprakas Basu, Vijay Kumar Shukla
Journal of Family Medicine and Primary Care  vol: 14  issue: 5  first page: 1925  year: 2025  
doi: 10.4103/jfmpc.jfmpc_1286_24

16. Risk factors and clinical outcomes of multidrug-resistant and biofilm-producing infections in diabetic foot ulcers: a two-year cohort study
Mohd Shahid Khan, Noor Jahan, Razia Khatoon, Faisal Moin Ansari, Siraj Ahmad
World Journal of Microbiology and Biotechnology  vol: 41  issue: 10  year: 2025  
doi: 10.1007/s11274-025-04546-w

17. Phenotypic Profile and Antibiogram of Biofilm-Producing Bacteria Isolates from Diabetic Foot Ulcers in Zaria, Nigeria
Yahaya Usman, Adamu Girei Bakari, Idris Nasir Abdullahi, Abdurrahman El-Fulaty Ahmad, Fatima Sani-Bello, Atiene Solomon Sagay, Adebola Tolulope Olayinka
Nigerian Postgraduate Medical Journal  vol: 28  issue: 4  first page: 233  year: 2021  
doi: 10.4103/npmj.npmj_552_21

18. Anaerobes in diabetic foot infections: pathophysiology, epidemiology, virulence, and management
Fanny Villa, Hélène Marchandin, Jean-Philippe Lavigne, Sophie Schuldiner, Nicolas Cellier, Albert Sotto, Paul Loubet, Audrey N. Schuetz, Eric Senneville
Clinical Microbiology Reviews  vol: 37  issue: 3  year: 2024  
doi: 10.1128/cmr.00143-23

19. Diabetes-related lower limb wounds: Antibiotic susceptibility pattern and biofilm formation
Raha Orfali, Safina Ghaffar, Lateefa AlAjlan, Shagufta Perveen, Eman Al-Turki, Fuad Ameen
Saudi Pharmaceutical Journal  vol: 32  issue: 6  first page: 102069  year: 2024  
doi: 10.1016/j.jsps.2024.102069

20. Antimicrobial resistance and beta-lactamase gene distribution among clinical isolates: a two-year cohort study
Yasser Alraey, Mohammed Mushabub Assiry, Irfan Ahmad, Abdulaziz Alqahtani, Nada Basheer, Mohammed A. M. AlAsiri, Saleh A. M. Alshehri, Saeed M. S. Alhamhhum, Sultan Mohammed Alhefdi, Mohd Shahid Khan, Mohd Saleem, Abdulah A. S. Bawazeer
Scientific Reports  vol: 15  issue: 1  year: 2025  
doi: 10.1038/s41598-025-08445-w

21. Risk Factors and Nomogram Model for Multidrug‐Resistant Bacterial Infections in Diabetic Foot Wounds
Guangzhe Meng, Liye Hu, Xuan Gao, Sijia Xu, Xiuhui Wang, Yiwen Yang, Xiaoling Li, Libo Zhang, Shaoling Yang
International Wound Journal  vol: 23  issue: 5  year: 2026  
doi: 10.1111/iwj.70929

22. Characteristic Correlation between Staphylococcal Isolates from Wounds and Nares of Diabetic Foot Patients Living in Erbil City, Iraq
Samira Fattah Hamid, Fatih Koksal, Tulin Guven Gokmen, Tulay Knademir
Current Diabetes Reviews  vol: 22  issue: 9  year: 2026  
doi: 10.2174/0115733998413217251206210451

23. An Update on Diabetic Foot Ulcer and Its Management Modalities
Mohd Shahid Khan, Noor Jahan, Razia Khatoon, Faisal Moin Ansari, Siraj Ahmad
Indian Journal of Microbiology  vol: 64  issue: 4  first page: 1401  year: 2024  
doi: 10.1007/s12088-023-01180-8

24. Diabetic foot ulcer, antimicrobial remedies and emerging strategies for the treatment
Ancha Kishore Babu, M. Pradeep Kumar, B. Krupavaram, Sandhya Rani Mandadi, Lakshmi, R. Manikandhan, M. Akiful Haque, Rokeya Sultana
International journal of health sciences  first page: 2835  year: 2022  
doi: 10.53730/ijhs.v6nS3.6199

25. Hemolytic Activity, Cytotoxicity, and Antimicrobial Effects of Human Albumin- and Polysorbate-80-Coated Silver Nanoparticles
Dmitry Korolev, Michael Shumilo, Galina Shulmeyster, Alexander Krutikov, Alexey Golovkin, Alexander Mishanin, Andrew Gorshkov, Anna Spiridonova, Anna Domorad, Alexander Krasichkov, Michael Galagudza
Nanomaterials  vol: 11  issue: 6  first page: 1484  year: 2021  
doi: 10.3390/nano11061484

26. Increase in antibiotic resistance in diabetic foot infections among peruvian patients: a single-center cross-sectional study
Jeel Moya-Salazar, Jackelina M. Chamana, Daniela Porras-Rivera, Eliane A. Goicochea-Palomino, Carmen R. Salazar, Hans Contreras-Pulache
Frontiers in Endocrinology  vol: 14  year: 2023  
doi: 10.3389/fendo.2023.1267699

27. A narrative review of coagulase-negative staphylococci in diabetic foot infections
Chloé Magnan, Lucile Plumet, Madjid Morsli, Catherine Dunyach-Remy, Cassandra Pouget, Albert Sotto, Virginie Molle, Jean-Philippe Lavigne, Audrey N. Schuetz, Benjamin A. Lipsky
Clinical Microbiology Reviews  vol: 38  issue: 4  year: 2025  
doi: 10.1128/cmr.00121-25

28. Distribution of multidrug-resistant bacterial infections in diabetic foot ulcers and risk factors for drug resistance: a retrospective analysis
Huihui Guo, Qiwei Song, Siwei Mei, Zhenqiang Xue, Junjie Li, Tao Ning
PeerJ  vol: 11  first page: e16162  year: 2023  
doi: 10.7717/peerj.16162

29. Antimicrobial Activity of Chromolaena Odorata and Syzygium Aromaticum against multi-drug resistant clinical isolates from diabetic foot ulcer patients: A cross-sectional study
Solomon Wireko, Jacob Amonoo-Neizer, Samuel Nii Boadu, Jessica Neebo, Oumar Ramatu, Jemimah Aggrey Appiah, Elizabeth Akua Baidoo, Ebenezer Senu, Alexander Kwarteng, Mina Ofosu
Scientific African  vol: 28  first page: e02764  year: 2025  
doi: 10.1016/j.sciaf.2025.e02764

30. Prevalence of Extended-Spectrum β-Lactamase and Carbapenemase Producers of Gram-Negative Bacteria, and Methicillin-Resistant Staphylococcus aureus in Isolates from Diabetic Foot Ulcer Patients in Ethiopia
Asegdew Atlaw Woldeteklie, Habtamu Biazin Kebede, Abdurezak Ahmed Abdela, Yimtubezinash Woldeamanuel
Infection and Drug Resistance  vol: Volume 15  first page: 4435  year: 2022  
doi: 10.2147/IDR.S371431

31. The diabetic foot ulcer: Biofilm, antimicrobial resistance, and amputation
Mohd Shahid Khan, Noor Jahan, Razia Khatoon, Faisal Moin Ansari, Siraj Ahmad
International Journal of Diabetes in Developing Countries  vol: 45  issue: 3  first page: 568  year: 2025  
doi: 10.1007/s13410-024-01423-4

32. Antimicrobial resistance profiles and detection of mecA, blaCTX-M-1, and blaSHV genes in bacteria among diabetic foot ulcer patients from selected referral hospitals in Uganda
Alice Namatovu, Bienfait Mumbere Vahwere, Ibrahim Ntulume, Robinson Ssebuufu, Rebecca Nalubega, Theophilus Pius, Franck K. Sikakulya, Gidio Agaba, Emmanuel Seremba, Patrick Kyamanywa, George William Nasinyama
BMC Infectious Diseases  vol: 25  issue: 1  year: 2025  
doi: 10.1186/s12879-025-11909-z