Skip directly to site content Skip directly to page options Skip directly to A-Z link Skip directly to A-Z link Skip directly to A-Z link
Volume 24, Number 5—May 2018

Antimicrobial-Resistant Bacteria in Infected Wounds, Ghana, 20141

Hauke Janssen2, Iryna Janssen2, Paul Cooper, Clemens Kainyah, Theresia Pellio, Michael Quintel, Mathieu Monnheimer, Uwe Groß, and Marco H. SchulzeComments to Author 
Author affiliations: University Medical Center Goettingen, Goettingen, Germany (H. Janssen, I. Janssen, M. Quintel, M. Monnheimer, U. Groß, M.H. Schulze); St. Martin de Porres Hospital, Eikwe, Ghana (P. Cooper, C. Kainyah, T. Pellio)

Cite This Article


Wound infections are an emerging medical problem worldwide, frequently neglected in under-resourced countries. Bacterial culture and antimicrobial drug resistance testing of infected wounds in patients in a rural hospital in Ghana identified no methicillin-resistant Staphylococcus aureus or carbapenem-resistant Enterobacteriaceae but identified high combined resistance of Enterobacteriaceae against third-generation cephalosporins and fluoroquinolones.

Bacteriologic investigation of clinical specimens is an essential tool for active surveillance of antimicrobial drug resistance. Knowledge of causative bacterial species and their resistance profile enables targeted antimicrobial therapy, limits ineffective antimicrobial therapy, and avoids in part unnecessary antimicrobial pressure to noninvolved bacterial pathogens (1). Available antimicrobial resistance data will sensitize clinicians and policy makers and are a prerequisite for updating national treatment guidelines (1,2). These data contribute to prevention and control of antimicrobial drug resistance (1).

Wound infections are an emerging medical problem worldwide; the economic burden and morbidity and mortality rates are huge (3,4). Because of the frequent polymicrobial nature of infected wounds, bacteriologic investigations are demanding and frequently neglected in sub-Saharan Africa countries (5).

The Study

Since 2000, the Institute for Medical Microbiology of the University Medical Center Goettingen, Goettingen, Germany, has assisted the running of the bacteriology laboratory in St. Martin de Porres Hospital in Eikwe, Ghana (2). Eikwe is a rural coastal village in the Western Region of Ghana; its mission hospital has an admission capacity of ≈200 beds and serves ≈380,000 persons.

During March–July 2014, we conducted a prospective study at St. Martin de Porres Hospital, performing bacteriologic investigations of infected wounds of inpatients and outpatients during routine working hours (Monday–Friday, 8 am–4 pm). The hospital administration (the local ethics review panel) authorized the study. Patients from whom wound swab samples were investigated provided consent to be included in the study.

Medical doctors diagnosed wound infections clinically, according to the classic signs of inflammation. After wounds were carefully cleaned with sterile gauze moistened with a sterile solution of 0.9% sodium chloride, samples were collected from the wound ground and edge on sterile cotton swabs and immediately transported to the bacteriology laboratory in Amies transport medium (Copan, Brescia, Italy). The samples were inoculated onto MacConkey agar and 7% sheep blood agar (Tulip Diagnostics, Goa, India) and thereafter incubated aerobically at 35°C. Both plates were read after 24 and 48 hours. Gram staining was performed to ensure wound specimen quality and to check for bacteria, neutrophils, and epithelial cells.

Bacterial isolates were initially identified (to genus level) by colony morphology, Gram staining, catalase reaction, oxidase reaction, coagulase reaction, indole reaction, and growth on Kligler iron agar, as described by Cheesbrough (6). Bacterial isolates were stored in microbanks at −20°C. Species identification was completed (to species level) at the Institute for Medical Microbiology in Goettingen, Germany, by using MALDI Biotyper 3.0 (Bruker Daltonics, Bremen, Germany).

According to locally available resources, antimicrobial resistance testing was performed through disk diffusion, which guided the treatment of the wound infections. Antimicrobial resistance testing was repeated with VITEK 2 (bioMérieux, Marcy-l’Étoile, France) at the Institute for Medical Microbiology by using AST-P632, AST-P586, AST-N214, and AST-N248 cards with respect to bacterial species and according to the breakpoint tables for interpretation of MICs in EUCAST version 4.0 (7). Quality control was performed with the reference strains Pseudomonas aeruginosa ATCC 27853, Escherichia coli ATCC 25922, and Staphylococcus aureus ATCC 29213.

Of the 67 wound swab samples, 39 (58.2%) were from female patients. The mean age of the 67 patients was 40.1 ± 20.8 years (range 1–90 years, median 39 years). Of the 67 samples, collection sites were upper extremity for 4 (6.0%), trunk/head for 15 (22.4%), lower extremity for 39 (58.2%), and laparotomy site for 9 (13.4%) (Technical Appendix). A hospital-acquired wound infection was diagnosed for 21 (31.3%) patients.

All investigated wound swab samples grew bacterial pathogens. Overall, 32 species of bacteria were isolated; median was 3 (range 1–7) species/specimen. Of the 189 isolated species, 72 (38.1%) were Enterobacteriaceae, 69 (36.5%) were gram positive, and 48 (25.4%) were nonfermenters (Technical Appendix Table 2). Of the 67 samples, infection was monomicrobial in 17 (25.4%) and polymicrobial in 50 (74.6%). The most frequently detected bacterium in monomicrobial and polymicrobial infections was S. aureus. The predominant bacteria in polymicrobial infections were Enterobacteriaceae and nonfermenters (Technical Appendix Table 3). Results of VITEK 2 antimicrobial resistance testing of the most frequently found bacterial species are shown in Table 1.

The spectrum of isolated bacteria is comparable to that reported by other studies from sub-Saharan Africa countries, such as Nigeria (9), Tanzania (3), and Rwanda (10). Frequently, studies describe detected pathogens at the genus level only (3,10). Concerning the proportion of gram-positive to gram-negative pathogens, we isolated slightly more gram-positive pathogens than others (3,911).

One of the most common bacteria found in wound infections is S. aureus (3,5,1012), which was most frequently identified in our study (Technical Appendix Table 2); however, we detected no methicillin-resistant S. aureus (MRSA). In contrast, studies from urban areas in sub-Saharan Africa countries found MRSA rates of >80% (10,12). Urban areas are centers of specialized healthcare, where many patients who may already have a long medical history are referred. Such referrals predispose urban patients, staff, and others to more MRSA colonization and infection than experienced by those in rural areas (13). The hospital in Eikwe is a general hospital; the villagers are mainly fishermen, and there are no big animal farms in the area. Predisposition to MRSA in this area may be low.

We found no carbapenem resistance in Enterobacteriaceae (Table 1). Of great concern were the high rates of resistance of E. coli, Klebsiella pneumoniae, and Enterobacter cloacae complex against third-generation cephalosporins, fluoroquinolones, or both (Table 2), as have been found in other studies from urban areas (3,5,10). The indiscriminate use of antimicrobial drugs contributes to this factor (14). Officially, selling antibiotics without prescription is not allowed in Ghana; however, almost every oral antimicrobial drug is available over the counter without any prescription. Eikwe is no exception, although the spectrum of available antimicrobial drugs may be smaller there than in cities. Development of antimicrobial drug resistance may also be enhanced by circulation of counterfeit drugs (15).

Resistance of E. coli and K. pneumoniae against third-generation cephalosporins probably occurs through production of extended spectrum β-lactamase; in E. cloacae complex, it is probably through AmpC–β-lactamase. However, this statement is only an assumption because we did not perform molecular analyses.

In Eikwe, rain falls throughout the year and humidity is almost constant at 70%–90% despite 2 rainfall peaks (May–June and October–November). The effect of seasonality on the incidence of wound infections and the frequency of infection with gram-negative bacteria may not be so pronounced as that found in other studies from sub-Saharan Africa countries with high variations in humidity (9). However, because we analyzed only swab samples collected during March–July, the effect of seasonality is difficult to evaluate.


Antimicrobial drug resistance among gram-negative organisms seems to be widespread in Ghana, even among community-onset infections in rural, resource-limited settings, although MRSA was surprisingly absent. Future research efforts should focus on the transmission dynamics and prevention of gram-negative antimicrobial resistance in those settings. Microbiological investigation of the worldwide problem of wound infections should be encouraged in areas of limited resources and might provide a valuable contribution to the surveillance of increasing antimicrobial resistance, especially in Enterobacteriaceae, and for the treatment of affected patients.

Dr. Janssen is an anesthesiologist who during the study worked as a volunteer at St. Martin de Porres Hospital. He supported the medical personnel in the operating theater and trained them in anesthesiology, resuscitation, and general medicine.



We thank the patients in Ghana for their participation in this study. We also thank the staff from St. Martin de Porres Hospital and the staff from the Institute for Medical Microbiology of the University Medical Center Goettingen for their commitment to perform the study.



  1. Vernet  G, Mary  C, Altmann  DM, Doumbo  O, Morpeth  S, Bhutta  ZA, et al. Surveillance for antimicrobial drug resistance in under-resourced countries. Emerg Infect Dis. 2014;20:43441. DOIPubMedGoogle Scholar
  2. Gross  U, Amuzu  SK, de Ciman  R, Kassimova  I, Gross  L, Rabsch  W, et al. Bacteremia and antimicrobial drug resistance over time, Ghana. Emerg Infect Dis. 2011;17:187982. DOIPubMedGoogle Scholar
  3. Kumburu  HH, Sonda  T, Mmbaga  BT, Alifrangis  M, Lund  O, Kibiki  G, et al. Patterns of infections, aetiological agents and antimicrobial resistance at a tertiary care hospital in northern Tanzania. Trop Med Int Health. 2017;22:45464. DOIPubMedGoogle Scholar
  4. Sen  CK, Gordillo  GM, Roy  S, Kirsner  R, Lambert  L, Hunt  TK, et al. Human skin wounds: a major and snowballing threat to public health and the economy. Wound Repair Regen. 2009;17:76371. DOIPubMedGoogle Scholar
  5. Leopold  SJ, van Leth  F, Tarekegn  H, Schultsz  C. Antimicrobial drug resistance among clinically relevant bacterial isolates in sub-Saharan Africa: a systematic review. J Antimicrob Chemother. 2014;69:233753. DOIPubMedGoogle Scholar
  6. Cheesbrough  M. District laboratory practice in tropical countries. Part 2. 2nd ed. Cambridge (UK): Cambridge University Press; 2006.
  7. The European Committee on Antimicrobial Susceptibility Testing. Breakpoint tables for interpretation of MICs and zone diameters. Version 4.0. 2014 [cited 2017 Sep 9].
  8. Clinical and Laboratory Standards Institute. Performance standards for antimicrobial susceptibility testing: twenty-fourth informational supplement (M100–S24). Wayne (PA): The Institute; 2014.
  9. Nwankwo  E, Edino  S. Seasonal variation and risk factors associated with surgical site infection rate in Kano, Nigeria. Turk J Med Sci. 2014;44:67480. DOIPubMedGoogle Scholar
  10. Ntirenganya  C, Manzi  O, Muvunyi  CM, Ogbuagu  O. High prevalence of antimicrobial resistance among common bacterial isolates in a tertiary healthcare facility in Rwanda. Am J Trop Med Hyg. 2015;92:86570. DOIPubMedGoogle Scholar
  11. Manyahi  J, Matee  MI, Majigo  M, Moyo  S, Mshana  SE, Lyamuya  EF. Predominance of multi-drug resistant bacterial pathogens causing surgical site infections in Muhimbili National Hospital, Tanzania. BMC Res Notes. 2014;7:500. DOIPubMedGoogle Scholar
  12. Mengesha  RE, Kasa  BG, Saravanan  M, Berhe  DF, Wasihun  AG. Aerobic bacteria in post surgical wound infections and pattern of their antimicrobial susceptibility in Ayder Teaching and Referral Hospital, Mekelle, Ethiopia. BMC Res Notes. 2014;7:575. DOIPubMedGoogle Scholar
  13. Falagas  ME, Karageorgopoulos  DE, Leptidis  J, Korbila  IP. MRSA in Africa: filling the global map of antimicrobial resistance. PLoS One. 2013;8:e68024. DOIPubMedGoogle Scholar
  14. Morgan  DJ, Okeke  IN, Laxminarayan  R, Perencevich  EN, Weisenberg  S. Non-prescription antimicrobial use worldwide: a systematic review. Lancet Infect Dis. 2011;11:692701. DOIPubMedGoogle Scholar
  15. Elder  DP, Kuentz  M, Holm  R. Antibiotic resistance: the need for a global strategy. J Pharm Sci. 2016;105:227887. DOIPubMedGoogle Scholar




Cite This Article

DOI: 10.3201/eid2405.171506

Original Publication Date: March 28, 2018

1Preliminary results from this study were presented at the Annual Meeting of the German Society of Tropical Medicine and International Health; October 7–8, 2016; Bonn, Germany; and at the 69th Annual Meeting of the German Society for Hygiene and Microbiology; March 5–8, 2017; Wuerzburg, Germany.

2These authors contributed equally to this article.

Table of Contents – Volume 24, Number 5—May 2018

EID Search Options
presentation_01 Advanced Article Search – Search articles by author and/or keyword.
presentation_01 Articles by Country Search – Search articles by the topic country.
presentation_01 Article Type Search – Search articles by article type and issue.



Please use the form below to submit correspondence to the authors or contact them at the following address:

Marco H. Schulze, University Medical Center Goettingen, Institute for Medical Microbiology and Goettingen International Health Network, Kreuzbergring 57, D-37075 Goettingen, Germany

Send To

10000 character(s) remaining.


Page created: April 17, 2018
Page updated: April 17, 2018
Page reviewed: April 17, 2018
The conclusions, findings, and opinions expressed by authors contributing to this journal do not necessarily reflect the official position of the U.S. Department of Health and Human Services, the Public Health Service, the Centers for Disease Control and Prevention, or the authors' affiliated institutions. Use of trade names is for identification only and does not imply endorsement by any of the groups named above.