• Users Online: 60
  • Print this page
  • Email this page

 Table of Contents  
Year : 2021  |  Volume : 5  |  Issue : 3  |  Page : 128-131

Nasal colonization and antibiotic resistance of staphylococcus species isolated from healthy veterinary personnel at veterinary medical care facilities in Tripoli

1 Department of Microbiology and Parasitology, Faculty of Veterinary Medicine, University of Tripoli, Tripoli, Libya
2 Institute of Veterinary Research of Tunisia, University of Tunis El Manar, Bab Saadoun, Tunis, Tunisia
3 Internal Medicine, Faculty of Veterinary Medicine, University of Tripoli, Tripoli, Libya

Date of Submission20-Aug-2020
Date of Acceptance31-Aug-2021
Date of Web Publication11-Oct-2021

Correspondence Address:
Dr. Mohamed Omar Ahmed
Department of Microbiology and Parasitology, Faculty of Veterinary Medicine, University of Tripoli, P.O. Box 13662, Tripoli
Login to access the Email id

Source of Support: None, Conflict of Interest: None

DOI: 10.4103/ljms.ljms_53_21

Rights and Permissions

Background/Aim: Veterinary medical personnel may carry important antibiotic-resistant organisms playing important role in their dissemination and emergence. The purpose of the study was to investigate nasal colonization and antibiotic resistance of Staphylococcus species isolated from veterinary personnel (VP). Methods: A total of 47 VP were sampled, whereby nasal samples were subjected to selective and typical laboratory protocols. Presumptive isolates were further confirmed and fully characterized by the Phoenix automated microbiological system then further tested by polymase chain reactions for mecA and panton-valentine leukocidin (pvl) genes. Results: A total of 34 (72%) VP were colonized with various species, mostly coagulase-negative staphylococci. A collection of 34 staphylococci isolates were collected of which 21% and 6% were, respectively, positive for mecA and pvl genes expressed exclusively by Staphylococcus aureus and S. epidermidis. Conclusion: VP may carry various staphylococci species of public health importance expressing multidrug resistant and virulent traits. Preventative measures and continuous monitoring are required to control the spread of methicillin-resistant staphylococci in veterinary clinics.

Keywords: Libya, methicillin-resistant staphylococci, mecA, panton-valentine leukocidin, staphylococcus, veterinary personnel

How to cite this article:
Ahmed MO, Othman AA, Abbassi MS, Elnageh HR, Almshawt NF, Abouzeed YM, Hiblu MA. Nasal colonization and antibiotic resistance of staphylococcus species isolated from healthy veterinary personnel at veterinary medical care facilities in Tripoli. Libyan J Med Sci 2021;5:128-31

How to cite this URL:
Ahmed MO, Othman AA, Abbassi MS, Elnageh HR, Almshawt NF, Abouzeed YM, Hiblu MA. Nasal colonization and antibiotic resistance of staphylococcus species isolated from healthy veterinary personnel at veterinary medical care facilities in Tripoli. Libyan J Med Sci [serial online] 2021 [cited 2021 Nov 29];5:128-31. Available from: https://www.ljmsonline.com/text.asp?2021/5/3/128/328088

  Introduction Top

Staphylococcus species are commensal bacteria of mammals birds and frequently responsible for opportunistic and hospital-acquired infections in humans.[1] Staphylococci species are frequently associated with animal skin and soft-tissue infections and have been mainly associated with pathogenic coagulase-positive staphylococci (CoPS), with less attention to the coagulase-negative staphylococci (CoNS).[2] Similar to human health-care settings, veterinary clinics have created similar conditions contributing to the emergence and spread of hospital-acquired and antibiotic-resistant pathogens.[3] These settings may also play a role in the circulation and further evolution of pathogenic and multidrug-resistant organisms in humans, animals, and the environment.[4]

Methicillin-resistant staphylococci (MRS) are known public health pathogens and are involved in the community and health-care settings.[5],[6] These are also reported from companion and food animals and veterinary personnel (VP) showing distinctive epidemiological characteristics causing serious outbreaks and persistent infections.[7],[8] However, the available epidemiological and clinical information on such dynamics are limited particularly during the nonoutbreak periods. The objective of the current study was to investigate the colonization rate and antimicrobial resistance of Staphylococcus species isolated from VP working at veterinary clinics in Tripoli. The involved clinics provide different medical and health services for pet and companion animals.

  Methods Top

During April 2018, 47 VP volunteered from 13 veterinary clinics (mean age was 38.8 years; ages ranged from 22 to 56 years). VP were involved on the basis that they were neither suffering from any clinical conditions nor under therapeutic treatments, including antibiotic drugs, at least 3 months before sampling. A nasal sample was obtained from each participant using a moist cotton swab and processed in the laboratory within 2h. Each swab was streaked directly onto mannitol salt agar and incubated aerobically at 35°C for 48h. A typical colony was selected from each plate and grown overnight on Columbia blood agar at 35°C for 24h; afterward, presumptive laboratory identification was performed by Gram stain, catalase, and coagulase tests. Presumptive isolates (regardless of coagulase productivity) were further tested by the BD Phoenix automated microbiology system (BD Diagnostic Systems, Sparks, MD, US) for definitive confirmation at the species level and for the determination of susceptibility to antimicrobial agents. Staphylococci species were subjected to polymerase chain reaction (PCR) adapted protocols and screened for mecA and Panton-valentine Leukocidin (pvl) genes.[9],[10] The significant difference of colonization between the methicillin resistance staphylococci was carried out using Epi Info™ of the Center for Disease Control and Prevention (P ≤ 0.05).

  Results Top

Staphylococcus species were recovered from 72% (n = 34/47) of VP yielding 34 staphylococci isolates represented by five subspecies of coagulase-negative staphylococci (62%; n = 21 of 34) and one subspecies of coagulase-positive staphylococci (38%; n = 13 of 34). These respectively included S. epidermidis (47%; n = 16), S. aureus (38%; n = 13), S. warneri (6%; n = 2), S. lugdunensis (3%; n = 1), S. cohnii (3%; n = 1) and S. auricularis (3%; n = 1). PCRs confirmed 15% (7 of 47) of VP were carriers of mecA-MRS with no significant difference between MRCoPS and MRCoNS carriage (P > 0.05). In total, 21% (n = 7/34) of the isolates were positive for mecA; four S. aureus and three S. epidermidis. Furthermore, 6% (n = 2/34) of isolates expressed the pvl gene expressed exclusively by S. aureus. The multidrug resistance phenotype (>4 antibiotic classes) was expressed exclusively by S. epidermidis and S. aureus. A mecA-S. epidermidis isolates expressed extended MDR resistance including to trimethoprim-sulfamethoxazole, nitrofurantoin, and ciprofloxacin [Table 1]. Two S. aureus expressed the MLSB resistance phenotype but were negative for PCRs. No resistance was detected against mupirocin, fusidic acid, linezolid, rifampin, and daptomycin.
Table 1: Number of staphylococci species resistant to antimicrobial classes (n=34)

Click here to view

  Discussion Top

Colonization with Staphylococcus species is considered an early step in the pathogenesis of infections.[11] The colonization rate of S. aureus and pvl-S. aureus among VP was reported at 39% and 28%, respectively, mainly expressing the mecA gene among the characterized MRS strains.[12] Recent studies have estimated that between 7% and 15% of VP may carry MRSA but vary significantly between regions and countries.[8],[13] In the current study, 72% of VP were found to be positive carriers for different staphylococci, mostly of the CoN group. Also, 15% and 4% of VP carried MRS-mecA and MRSA pvl-isolates exclusively carried by S. aureus and S. epidermidis species.

MRSA may circulate simultaneously between the community and health-care settings leading to the emergence of evolved and more virulent clones.[14],[15] In veterinary hospitals, MRSA can be introduced continuously and circulate for up to 9 months, causing postsurgical outbreaks and occupational transmission.[16],[17],[18] The identification of VP carrying pvl-MRSA strains in the current study is worrisome due to their documented virulent role and association with severe clinical complications.[14],[19] In addition, the frequency rate of mecA-and pvl-MRSA among VP may reflect the level of exposure to pets and companion animals[20] but also raises serious concerns regarding the spread of MRS and pvl positive staphylococci within human populations. In Libya, MRSA has been exclusively isolated from human clinical samples carrying mecA and pvl genes belonging to the frequently reported global clones (i.e., CC5 and CC80).[19] In addition, the recent emergence of critical hospital-acquired pathogens (i.e., vancomycin-resistant Enterococcus faecium and colistin-resistant carbapenemase-producing Gram-negative isolates) raises alarming concerns about the status of the health-care system in Libya.[21],[22]

CoNS are emerging opportunistic bacteria with a high rate of reported methicillin resistance from companion animals.[23] In Africa, CoNS are increasingly reported ranging from 6% to 68% in susceptible human infections and from 3% to 61.7% in suspected animal infections.[24] In Africa, CoNS of animal origins were mainly reported from cattle expressing varying antibiotic resistance patterns, high MRS phenotypes, and cross-resistance against many antibiotics.[24] Of these, S. epidermidis, S. haemolyticus, S. capitis, S. lugdunensis and S. xylosus are clinically the most significant species.[25] Furthermore, CoNS are considered hidden reservoirs for antibiotic resistance and virulence traits, including methicillin-resistant with reduced susceptibility to important antibiotic classes (e.g., glycopeptides). S. epidermidis is especially important as a reservoir of antimicrobial-resistant genes that may be transferred to other staphylococci, mainly S. aureus.[26] This particular staphylococci species may also possess the secretion of serine protease Esp inhibiting and preventing the colonization of S. aureus and biofilm formation.[27] Such characteristics may play a significant role in the evolving and continuous emergence of MRS spreading into environmental reservoirs, including companion and food animals.[15]

Staphylococci species of veterinary relevance are difficult to differentiate due to the under-developed diagnostic protocols in veterinary medicine. The phoenix automated microbiology system has been widely reported as an effective tool for the identifications and antimicrobial susceptibility of staphylococci, including CoNS; however, a few species are unable to be differentiated using this molecular method.[28] Of these, S. pseudintermedius (formerly known as S. intermedius) are known animal pathogens and are increasingly responsible for clinical complications in humans.[29] S. pseudintermedius is easily misdiagnosed with other staphylococci, particularly S. aureus, due to similar phenotypic characteristics requiring advanced molecular methods for definite identification such as PCR or MALDI-TOF MS.[2] Furthermore, only the most significant genes associated with clinical complications were screened (i.e., mecA and pvl genes) in the present study due to limited available resources, and further in-depth molecular and epidemiological analysis are required.

  Conclusion Top

This is the first study that investigated veterinary medical settings for important hospital-acquired bacteria in Libya. The concerning rate of colonization with different staphylococci and MRS strains among the studied VP, highlights the necessity to introduce infection control measures in veterinary clinics. The application of decolonization using topical antimicrobials (e.g., intranasal mupirocin) and antiseptics are needed to reduce the incidence of recurrent infections. Monitoring of MRS in veterinary medical settings is required and further studies are needed to investigate the duration of colonization in VP and the associated risk factors.


The authors would like to thank all participants and veterinary colleagues at the veterinary clinics in Tripoli.

Financial support and sponsorship


Conflicts of interest

There are no conflicts of interest.

  References Top

Grice EA, Segre JA. The skin microbiome. Nat Rev Microbiol 2011;9:244-53.  Back to cited text no. 1
Guardabassi L, Damborg P, Stamm I, Kopp PA, Broens EM, Toutain PL, et al. Diagnostic microbiology in veterinary dermatology: Present and future. Vet Dermatol 2017;28:146-e30.  Back to cited text no. 2
Walther B, Tedin K, Lübke-Becker A. Multidrug-resistant opportunistic pathogens challenging veterinary infection control. Vet Microbiol 2017;200:71-8.  Back to cited text no. 3
van Duijkeren E, Moleman M, Sloet van Oldruitenborgh-Oosterbaan MM, Multem J, Troelstra A, Fluit AC, et al. Methicillin-resistant Staphylococcus aureus in horses and horse personnel: An investigation of several outbreaks. Vet Microbiol 2010;141:96-102.  Back to cited text no. 4
World Health Organization. Media Centre. News Release. WHO Publishes List of Bacteria for Which New Antibiotics are Urgently Needed; 2017. Available from: http://www.who.int/mediacentre/news/releases/2017/bacteria-antibiotics-needed/en/. [Last accessed on 2018 Jul 12].  Back to cited text no. 5
Turner NA, Sharma-Kuinkel BK, Maskarinec SA, Eichenberger EM, Shah PP, Carugati M, et al. Methicillin-resistant Staphylococcus aureus: An overview of basic and clinical research. Nat Rev Microbiol 2019;17:203-18.  Back to cited text no. 6
Feßler AT, Schuenemann R, Kadlec K, Hensel V, Brombach J, Murugaiyan J, et al. Methicillin-resistant Staphylococcus aureus (MRSA) and methicillin-resistant Staphylococcus pseudintermedius (MRSP) among employees and in the environment of a small animal hospital. Vet Microbiol 2018;221:153-8.  Back to cited text no. 7
Sato T, Usui M, Maetani S, Tamura Y. Prevalence of methicillin-resistant Staphylococcus aureus among veterinary staff in small animal hospitals in Sapporo, Japan, between 2008 and 2016: A follow up study. J Infect Chemother 2018;24:588-91.  Back to cited text no. 8
Frebourg NB, Lefebvre S, Baert S, Lemeland JF. PCR-Based assay for discrimination between invasive and contaminating Staphylococcus epidermidis strains. J Clin Microbiol 2000;38:877-80.  Back to cited text no. 9
Jarraud S, Mougel C, Thioulouse J, Lina G, Meugnier H, Forey F, et al. Relationships between Staphylococcus aureus genetic background, virulence factors, agr groups (alleles), and human disease. Infect Immun 2002;70:631-41.  Back to cited text no. 10
Sakr A, Brégeon F, Mège JL, Rolain JM, Blin O. Staphylococcus aureus nasal colonization: An update on mechanisms, epidemiology, risk factors, and subsequent infections. Front Microbiol 2018;9:2419.  Back to cited text no. 11
Drougka E, Foka A, Koutinas CK, Jelastopulu E, Giormezis N, Farmaki O, et al. Interspecies spread of Staphylococcus aureus clones among companion animals and human close contacts in a veterinary teaching hospital. A cross-sectional study in Greece. Prev Vet Med 2016;126:190-8.  Back to cited text no. 12
Neradova K, Jakubu V, Pomorska K, Zemlickova H. Methicillin-resistant Staphylococcus aureus in veterinary professionals in 2017 in the Czech Republic. BMC Vet Res 2020;16:4.  Back to cited text no. 13
Peng H, Liu D, Ma Y, Gao W. Comparison of community- and healthcare-associated methicillin-resistant Staphylococcus aureus isolates at a Chinese tertiary hospital, 2012-2017. Sci Rep 2018;8:17916.  Back to cited text no. 14
Lakhundi S, Zhang K. Methicillin-resistant Staphylococcus aureus: Molecular characterization, evolution, and epidemiology. Clin Microbiol Rev 2018;31:e00020-18.  Back to cited text no. 15
Loeffler A, Boag AK, Sung J, Lindsay JA, Guardabassi L, Dalsgaard A, et al. Prevalence of methicillin-resistant Staphylococcus aureus among staff and pets in a small animal referral hospital in the UK. J Antimicrob Chemother 2005;56:692-7.  Back to cited text no. 16
van Balen J, Kelley C, Nava-Hoet RC, Bateman S, Hillier A, Dyce J, et al. Presence, distribution, and molecular epidemiology of methicillin-resistant Staphylococcus aureus in a small animal teaching hospital: A year-long active surveillance targeting dogs and their environment. Vector Borne Zoonotic Dis 2013;13:299-311.  Back to cited text no. 17
Waqar N, Amin Q, Munir T, Ikram MS, Shahzad N, Mirza A, et al. A cross-sectional study of methicillin-resistant Staphylococcus aureus at the equine-human interface. Trop Anim Health Prod 2019;51:1927-33.  Back to cited text no. 18
Ahmed MO, Baptiste KE, Daw MA, Elramalli AK, Abouzeed YM, Petersen A. Spa typing and identification of pvl genes of meticillin-resistant Staphylococcus aureus isolated from a Libyan hospital in Tripoli. J Glob Antimicrob Resist 2017;10:179-81.  Back to cited text no. 19
Boost MV, So SY, Perreten V. Low rate of methicillin-resistant coagulase-positive staphylococcal colonization of veterinary personnel in Hong Kong. Zoonoses Public Health 2011;58:36-40.  Back to cited text no. 20
Ahmed MO, Elramalli AK, Baptiste KE, Daw MA, Zorgani A, Brouwer E, et al. Whole genome sequence analysis of the first vancomycin-resistant Enterococcus faecium isolates from a Libyan hospital in Tripoli. Microb Drug Resist 2020;26:1390-8.  Back to cited text no. 21
Kieffer N, Ahmed MO, Elramalli AK, Daw MA, Poirel L, Álvarez R, et al. Colistin-resistant carbapenemase-producing isolates among Klebsiella spp. and Acinetobacter baumannii in Tripoli, Libya. J Glob Antimicrob Resist 2018;13:37-9.  Back to cited text no. 22
Bagcigil FA, Moodley A, Baptiste KE, Jensen VF, Guardabassi L. Occurrence, species distribution, antimicrobial resistance and clonality of methicillin- and erythromycin-resistant staphylococci in the nasal cavity of domestic animals. Vet Microbiol 2007;121:307-15.  Back to cited text no. 23
Asante J, Amoako DG, Abia AL, Somboro AM, Govinden U, Bester LA, et al. Review of clinically and epidemiologically relevant coagulase-negative staphylococci in Africa. Microb Drug Resist 2020;26:951-70.  Back to cited text no. 24
Becker K, Heilmann C, Peters G. Coagulase-negative staphylococci. Clin Microbiol Rev 2014;27:870-926.  Back to cited text no. 25
Otto M. Coagulase-negative staphylococci as reservoirs of genes facilitating MRSA infection: Staphylococcal commensal species such as Staphylococcus epidermidis are being recognized as important sources of genes promoting MRSA colonization and virulence. Bioessays 2013;35:4-11.  Back to cited text no. 26
Iwase T, Uehara Y, Shinji H, Tajima A, Seo H, Takada K, et al. Staphylococcus epidermidis Esp inhibits Staphylococcus aureus biofilm formation and nasal colonization. Nature 2010;465:346-9.  Back to cited text no. 27
Carroll KC, Borek AP, Burger C, Glanz B, Bhally H, Henciak S, et al. Evaluation of the BD phoenix automated microbiology system for identification and antimicrobial susceptibility testing of staphylococci and enterococci. J Clin Microbiol 2006;44:2072-7.  Back to cited text no. 28
Bannoehr J, Ben Zakour NL, Waller AS, Guardabassi L, Thoday KL, van den Broek AH, et al. Population genetic structure of the Staphylococcus intermedius group: Insights into agr diversification and the emergence of methicillin-resistant strains. J Bacteriol 2007;189:8685-92.  Back to cited text no. 29


  [Table 1]


Similar in PUBMED
   Search Pubmed for
   Search in Google Scholar for
 Related articles
Access Statistics
Email Alert *
Add to My List *
* Registration required (free)

  In this article
Article Tables

 Article Access Statistics
    PDF Downloaded23    
    Comments [Add]    

Recommend this journal