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Whole Genome Sequencing and Antimicrobial Resistance of Staphylococcus Aureus from Surgical Site Infections in Ghana

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Whole Genome Sequencing and Antimicrobial Resistance of Staphylococcus Aureus from Surgical Site Infections in Ghana pathogens Article Whole Genome Sequencing and Antimicrobial Resistance of Staphylococcus aureus from Surgical Site Infections in Ghana Beverly Egyir 1,*, Jeannette Bentum 1,2 , Naiki Attram 2, Anne Fox 2, Noah Obeng-Nkrumah 3, Labi Appiah-Korang 4, Eric Behene 2, Selassie Kumordjie 2, Clara Yeboah 2, Bright Agbodzi 2, Ronald Essah Bentil 2, Rhodalyn Tagoe 1, Blessing Kofi Adu Tabi 1, Felicia Owusu 1,2, Nicholas T. K. D. Dayie 5 , Eric S. Donkor 5, Josephine Nsaful 6, Kwaku Asah-Opoku 7 , Edward Nyarko 8, Edward Asumanu 8, Anders Rhod Larsen 9 , David M. Wolfe 2 and Andrew G. Letizia 2 1 Bacteriology Department, Noguchi Memorial Institute for Medical Research, University of Ghana, Accra 00233, Ghana; [email protected] (J.B.); [email protected] (R.T.); kofi[email protected] (B.K.A.T.); [email protected] (F.O.) 2 Naval Medical Research Unit—Three, Ghana Detachment, Accra 00233, Ghana; [email protected] (N.A.); Ghana; [email protected] (A.F.); [email protected] (E.B.); [email protected] (S.K.); [email protected] (C.Y.); [email protected] (B.A.); [email protected] (R.E.B.); [email protected] (D.M.W.); [email protected] (A.G.L.) 3 Department of Medical Laboratory Sciences, School of Biomedical and Allied Health Sciences, University of Ghana, Accra 00233, Ghana; [email protected] 4 Department of Microbiology, Korle-Bu Teaching Hospital, Accra 00233, Ghana; [email protected] 5 Department of Medical Microbiology, University of Ghana Medical School, University of Ghana, Accra 00233, Ghana; [email protected] (N.T.K.D.D.); [email protected] (E.S.D.) 6 Department of Surgery, Korle-bu Teaching Hospital, Accra 00233, Ghana; [email protected] Citation: Egyir, B.; Bentum, J.; 7 Department of Obstetrics and Gynaecology, University of Ghana Medical School, University of Ghana, Attram, N.; Fox, A.; Obeng-Nkrumah, Accra 00233, Ghana; [email protected] 8 N.; Appiah-Korang, L.; Behene, E.; 37 Military Hospital, Accra 00233, Ghana; [email protected] (E.N.); [email protected] (E.A.) 9 Kumordjie, S.; Yeboah, C.; Agbodzi, Statens Serum Institut, Department of Bacteria, Parasites and Fungi, Reference Laboratory for Antimicrobial B.; et al. Whole Genome Sequencing Resistance, Artillerivej 5, DK-2300 Copenhagen, Denmark; [email protected] * Correspondence: [email protected] and Antimicrobial Resistance of Staphylococcus aureus from Surgical Site Infections in Ghana. Pathogens Abstract: Staphylococcus aureus (S. aureus) is a common cause of surgical site infections (SSIs) globally. 2021, 10, 196. https://doi.org/ Data on the occurrence of methicillin-susceptible S. aureus (MSSA) as well as methicillin-resistant 10.3390/pathogens10020196 S. aureus (MRSA) among patients with surgical site infections (SSIs) in sub-Saharan African are scarce. We characterized S. aureus from SSIs in Ghana using molecular methods and antimicrobial Academic Editor: Bryan Heit susceptibility testing (AST). Wound swabs or aspirate samples were collected from subjects with SSIs. S. aureus was identified by matrix-assisted laser desorption ionization–time of flight mass Received: 20 January 2021 spectrometry (MALDI-TOF-MS); AST was performed by Kirby-Bauer disk diffusion, and results were Accepted: 5 February 2021 interpreted according to the Clinical and Laboratory Standards Institute (CLSI) guideline. Detection Published: 12 February 2021 of spa, mecA, and pvl genes was performed by polymerase chain reaction (PCR). Whole-genome sequencing (WGS) was done using the Illumina MiSeq platform. Samples were collected from Publisher’s Note: MDPI stays neutral 112 subjects, with 13 S. aureus isolates recovered. Of these, 92% were sensitive to co-trimoxazole, 77% with regard to jurisdictional claims in to clindamycin, and 54% to erythromycin. Multi-drug resistance was detected in 5 (38%) isolates. The published maps and institutional affil- iations. four mecA gene-positive MRSA isolates detected belonged to ST152 (n = 3) and ST5 (n = 1). In total, 62% of the isolates were positive for the Panton-Valentine leukocidin (pvl) toxin gene. This study reports, for the first time, a pvl-positive ST152-t355 MRSA clone from SSIs in Ghana. The occurrence of multi-drug-resistant S. aureus epidemic clones suggests that continuous surveillance is required to monitor the spread and resistance trends of S. aureus in hospital settings in the country. Copyright: © 2021 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article Keywords: surgical site infections; MRSA; whole-genome sequencing; Africa distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https:// creativecommons.org/licenses/by/ 4.0/). Pathogens 2021, 10, 196. https://doi.org/10.3390/pathogens10020196 https://www.mdpi.com/journal/pathogens Pathogens 2021, 10, 196 2 of 13 1. Introduction Surgical site infections (SSIs) are infections that occur at the surgical site within 30 or 90 days and up to a year (if there is an implant) of a surgical procedure [1]. Globally, SSIs constitute 14–33% of hospital-acquired infections [2–6], and approximately 2–5% of surgical patients have been estimated to develop an infection [2]. SSIs result in delayed wound healing, prolonged hospitalization, increased readmission rates, and increased healthcare cost, as well as increased morbidity and mortality [4,7–10]. Staphylococcus aureus (S. aureus) is a frequent cause of SSI [11–13]. Among S. aureus strains, the prevalence of methicillin resistant S. aureus (MRSA) is rising on the African continent [14–17]. This is of major concern due to the multi-drug-resistant nature of MRSA and the limited therapeutic options available to treat infected patients. In Ghana, SSIs are the most common healthcare-associated infections and account for up to 33% of all hospital-acquired infections [5]. Although S. aureus, particularly MRSA, in SSI can have severe adverse prognostic implications, scant epidemiologic in- formation exists, including information on its occurrence, antimicrobial resistance and molecular characteristics. In this study, we describe the antimicrobial resistance patterns and molecular characteristics of S. aureus recovered from subjects with SSIs at two hospitals in Accra, Ghana. 2. Results Of the 112 subjects, 56 (50%) and 56 (50%) were enrolled at the 37 Military Hospital (37-MH) and Korle-Bu Teaching Hospital (KBTH), respectively. Subjects recruited at the 37-MH consisted of 28 (50%) males; those from KBTH comprised 50 (89.3%) females. Table1 describes the population sampled at the two hospitals. Data collected on antibiotic use before and after surgery indicate that metronidazole, amoxicillin/clavulanic acid, clindamycin, and ciprofloxacin were frequently administered to subjects in both hospitals. Table 1. Demographic characteristics of patients enrolled at the two hospitals. 37 Military Korle Bu Total Hospital Teaching Hospital Characteristics N = 112 N = 56 N = 56 n(%) n%) n(%) Gender Male 28(50.0) 6(10.7) 34(30.4) Female 28(50.0) 50(89.3) 78(69.6) Age ≤13 years 1(1.8) 6(10.7) 7(6.3) >13 years 55(98.2) 50(89.3) 105(93.8) Department/ward General surgery 20(35.7) − Trauma and Surgical emergency unit 10(17.9) − Surgical OPD 16(28.6) − Obstetrics and Gynecology 10(17.9) 5(8.9) Maternity − 38(67.9) Neurosurgery − 2(3.6) Pediatric Unit − 6(10.7) Surgical Unit − 3(5.4) Orthopedic ward − 2(3.6) S. aureus positivity 8(14.3) 5(8.9) 13(11.6) Pathogens 2021, 10, 196 3 of 13 Pathogens 2021, 10, 196 3 of 13 2.1. Proportions of Subjects Positive for Staphylococcus aureus and Antimicrobial Resistance 2.1. ProportionsCulturing of of one Subjects sample Positive per patient for Staphylococcus showed bacterial aureus growth and (i.e.,AntimicrobialS. aureus, K.Resistance pneumoniae , E. coliCulturing, and P. aeruginosa of one sample) in 70 per (62.5%) patient of theshowed 112 samples. bacterial S.growth aureus (i.e.,was S. identified aureus, K. inpneu 13‐ ofmoniae, 70 culture-positive E. coli, and P. aeruginosa samples (18.6%).) in 70 (62.5%) Of the of 13 theS. 112 aureus samples.positive S. aureus patients, was two identified were co-infectedin 13 of 70 culture with E.coli,‐positivetwo withsamplesP. aeruginosa, (18.6%). Ofand the five 13 S. with aureusK. pneumoniae. positive patients, two were co‐infectedAntimicrobial with E.coli, susceptibility two with P. testing aeruginosa, showed and full five susceptibility with K. pneumoniae. to gentamicin but re- Antimicrobialsistance to penicillin susceptibility (100%; testing 13/13), showed tetracycline full susceptibility (46%; 6/13), to erythromycin gentamicin but (46%; resistance 6/13), tocefoxitin penicillin (31%; (100%; 4/13), 13/13), clindamycin tetracycline (23%; 3/13),(46%; and6/13), co-trimoxazole erythromycin (8%; (46%; 1/13). 6/13), Multi-drug cefoxitin (31%;resistance 4/13), was clindamycin detected in(23%; 5 (38%) 3/13), isolates. and co‐ Thetrimoxazole four cefoxitin-resistant (8%; 1/13). Multi (MRSA)‐drug resistance isolates wasoriginated detected from in 37-MH5 (38%) and isolates. were susceptibleThe four cefoxitin to vancomycin‐resistant but (MRSA) resistant isolates to clindamycin originated (50%;from 37 2/4),‐MH erythromycin and were susceptible (75%; 3/4), to and vancomycin tetracycline but (50%; resistant 2/4). to Whole-genome clindamycin (50%; sequenc- 2/4), erythromycining indicated that(75%; the 3/4), three and MRSA tetracycline ST152 isolates(50%; 2/4). were Whole related‐genome despite sequencing differences indicated in AST (Figurethat the1 three). MRSA ST152 isolates were related despite differences in AST (Figure 1). Figure 1. The whole-genome phylogeny of the 13 S. aureus isolates. The maximum likelihood phylogeny was constructed Figure 1. The whole‐genome phylogeny of the 13 S. aureus isolates. The maximum likelihood phylogeny was constructed usingusing RAxML RAxML v v 4.0 4.0 and and based based on on the the GTR GTR GAMMA GAMMA nucleotide nucleotide substitution substitution model. model. The whole-genome The whole‐genome alignment alignment was done was usingdone Mauveusing Mauve v 1.1.1.
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