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 Table of Contents  
Year : 2022  |  Volume : 10  |  Issue : 2  |  Page : 48-53

Staphylococcal nasal colonisation amongst medical students: Importance of imparting knowledge about infection control practices during undergraduates training

1 Department of Microbiology, Institute of Medical Sciences, Banaras Hindu University, Datia, Madhya Pradesh, India
2 MBBS Student, Institute of Medical Sciences, Banaras Hindu University, Datia, Madhya Pradesh, India
3 Division of Infectious Disease, Model Rural Health Research Unit, Badoni, Datia, Madhya Pradesh, India

Date of Submission02-Apr-2022
Date of Acceptance04-Nov-2022
Date of Web Publication01-Mar-2023

Correspondence Address:
Dr. Munesh Kumar Gupta
Department of Microbiology, Institute of Medical Sciences, Banaras Hindu University, Varanasi, Uttar Pradesh
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/jpsic.jpsic_9_22

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Background: Staphylococcus aureus is a common cause of hospital-acquired infections. Medical undergraduates are frequently exposed to hospital-adapted bacterial strains especially S. aureus and therefore are always at risk of colonisation.
Materials and Methods: A prospective study was conducted on 150 undergraduate students, of different semesters, to detect S. aureus nasal colonisation. A detailed history regarding attending the hospital ward teaching, hospitalisation, frequency of nose touching and immunocompromised condition was unequivocally obtained from all the participants. Anterior nares were swabbed and inoculated on mannitol salt and blood agar plates. S. aureus isolates were subsequently verified by conventional microbiological techniques. The antibiotic susceptibility testing was done by the modified Kirby–Bauer disc diffusion method. In addition, PCR-based detection of mecA gene and pvl gene was performed.
Results: Out of 150 students, we found 18 students (3 of 1st, 10 of 5th and 5 of 9th semester, respectively) to be colonised by S. aureus. Of these 18 isolates, 8 were found to be methicillin-resistant. We observed a significant association (P < 0.05) of hospital exposure, ward teaching/hospitalisation with S. aureus colonisation. These S. aureus isolates exhibited varying susceptibility towards different antibiotics with multiple antibiotic resistance indexes ranging from 0.08 to 0.58. Interestingly, all eight methicillin-resistant S. aureus isolates displayed mecA positivity while all were found to be pvl negative.
Conclusion: The results indicate the importance of imparting knowledge about infection control practices during the initial years of undergraduate training in medical schools, which may increase awareness amongst students before getting outpatient or ward postings.

Keywords: Multiple antibiotic resistance index, mupirocin, pvl gene, vancomycin screen agar

How to cite this article:
Gupta MK, Sinha G, Singh AK, Prakash P. Staphylococcal nasal colonisation amongst medical students: Importance of imparting knowledge about infection control practices during undergraduates training. J Patient Saf Infect Control 2022;10:48-53

How to cite this URL:
Gupta MK, Sinha G, Singh AK, Prakash P. Staphylococcal nasal colonisation amongst medical students: Importance of imparting knowledge about infection control practices during undergraduates training. J Patient Saf Infect Control [serial online] 2022 [cited 2023 Mar 30];10:48-53. Available from: https://www.jpsiconline.com/text.asp?2022/10/2/48/370889

  Introduction Top

The growing menace of hospital-acquired infections now a day is of major concern for health care personnel. These hospital-acquired infections are usually caused by t microbes such as Pseudomonas aeruginosa, Klebsiella pneumoniae, Acinetobacter baumannii, Staphylococcus aureus and Enterobacter species which are found to be drug resistant.[1] These nosocomial pathogens may be transferred to other patients and even to the distant sites of the same in patients through the hospital environment, and other health care personnel either through direct contact, inhalation or ingestion of contaminated water.[2]

S. aureus is the most common cause of suppurative pyogenic infections as well as surgical site infections.[3] S. aureus is a metabolically adapted pathogen, which bestows it with an extraordinary capacity to colonise and persist even in hostile environments. S. aureus is versatile in its capacity to colonise different habitats and thus can be isolated from fomites in the hospital environment, as well as from the moist areas of the human body including anterior nares, axilla and perineum.[4] It can dwell as a commensal, occupying the skin or mucous membranes or can cause varied infections at different body sites, ranging from superficial skin infections to deep-seated infections. This ability to survive makes S. aureus a prominent cause of both community-and hospital-acquired infections. This bacterium is becoming more difficult to treat due to the increasing incidence of methicillin-resistant S. aureus (MRSA) and glycopeptide resistance. Patients come in close contact with health care personnel such as doctors, nursing staff, laboratory technicians and other supporting staff during their stay in the hospital. Students pursuing their medical training as undergraduates and postgraduates are frequently exposed to patients during their clinical postings in hospitals. Many recent studies report the role of these medical undergraduates colonised with S. aureus as a significant source of transmission with an estimated prevalence of 34.6% Staphylococcal nasal carriage amongst all health workers.[5] Taking this into account, we designed a cross-sectional study to determine the status of Staphylococcal nasal carriage and their antibiogram amongst medical undergraduates at a tertiary care centre in North India. In addition, we also checked the prevalence of mecA and pvl genes in isolated S. aureus strains.

  Materials and Methods Top

Bacterial isolates and culture condition

This cross-sectional study was approved by the Institute Ethical Committee (Dean/2019/EC/1025), Institute of Medical Sciences, Banaras Hindu University. A written informed consent having a detailed sample collection procedure with the significance of the study was obtained from all the participating undergraduate medical students.

A total of 150 students (50 students each from 1st, 5th to 9th semesters of MBBS curriculum of IMS, BHU, Varanasi, India) were enrolled in the present study. All relevant details regarding age, sex, history of hospitalisation in the last 3 months, recurrent boil, the habit of nose picking and intake of any immunosuppressive drugs were obtained from all the participants. A sterile cotton swab dipped in normal saline was rolled in the anterior nares of the enrolled students. The collected swabs were immediately inoculated on blood agar (BA) and mannitol salt agar (MSA) plates. After overnight incubation at 37°C, the plates were examined for the presence of growth. Any yellow-coloured colony on MSA and small, opaque, haemolytic yellow-coloured colony on BA served as preliminary identification for S. aureus, which was identified by confirmatory tests as per standardised bacteriological protocol.[6]

Antibiotic susceptibility testing

After identification, we checked the antibiogram of the isolated confirmed S. aureus isolates by modified Kirby–Bauer disc diffusion method using different antibiotics, namely, penicillin (10Units), erythromycin (15 μg), clindamycin (2 μg), trimethoprim and sulfamethoxazole (1.25 μg/23.75 μg), linezolid (30 μg), ciprofloxacin (5 μg), moxifloxacin (5 μg), gentamicin (10 μg) and mupirocin (200 μg). In addition, a 30 μg disc of cefoxitin was used to determine methicillin resistance.[7] Vancomycin screen agar (6 μg/ml) was further used to screen the vancomycin susceptibility against the isolated S. aureus strains. The multiple antibiotic resistance (MAR) index for each of the isolated S. aureus strains from anterior nares was determined by the following:

MAR index for each isolated strain = number of antibiotics to which bacteria are resistant/number of antibiotics tested.[8]

Polymerase Chain Reaction targeting mecA and pvl genes

The PCR was performed by targeting mecA gene and pvl toxin genes separately. For this, at first, DNA was extracted utilising glass beads as described previously. Briefly, the cell wall of S. aureus was broken down by glass beads utilising cetyltrimethylammonium bromide extraction buffer, with subsequent purification of DNA using phenol: chloroform: isoamyl alcohol. The purified DNA was then precipitated by chilled isopropanol and finally dissolved in TE buffer (pH 8.6).

The presence of both genes was confirmed by PCR analysis using primers: Luk-PV-1 (5′-ATCATTAGGTAAAATGTC TGGACATGATCCA-3′), Luk-PV-2 (5′-GCATCAAGTGTATTGGATAGCAAAAGC-3 ′), mecA1 (5'-GTGAAGATATACCAAGTGATT-3') and mecA2 (5′-ATGCGCTATAGATTGAAAGGAT-3′) to amplify the pvl and mecA loci. PCRs were executed with Taq DNA polymerase (Invitrogen) under the following conditions: initial denaturation at 94°C for 10 min, followed by 10 cycles of denaturation at 94°C for 30s, annealing at 55°C for 45s and extension at 72°C for 1.5 min, with a final extension step at 72°C for 10 min. GCC Biotech (Kolkata, India) and Genii (Bangalore, India), respectively, supplied the oligonucleotide primers for mecA gene and pvl gene in this study. Amplicon was gel electrophoresed on 1.5% agarose gel containing 0.5 μg/ml ethidium bromide described elsewhere.[9],[10]

  Results Top

A total of 150 medical undergraduates including 50 students each from the 1st, 5th and 9th semesters were selected randomly and screened for the presence of S. aureus in their anterior nares. Male: female sex ratio amongst the participants was 1:1. Mean age of the participants in each semester 1st, 5th and 9th was 19.86, 21.86 and 25.34 years, respectively. In toto, 18 S. aureus strains were isolated from 1st-, 5th- and 9th-semester students (3, 10 and 5). A significant association (P < 0.05) of hospital exposure (ward teaching/hospitalisation) was observed for S. aureus colonisation whereas no significant difference for the recurrent boil, the frequent habit of nose picking and immunosuppressive drug intake (steroid) was observed [Table 1].
Table 1: Association of predisposing risk-factors to S. aures nasal colonisation among undergraduate medical students

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In the present study, 12% of the medical undergraduate students (18/150) were found to have S. aureus colonised in their nares with a point prevalence of 5.33% MRSA (8/150) nasal carriage. All the clinical isolates were found resistant to penicillin but all (100%) were sensitive to vancomycin and linezolid. About 5.56%, 11.11%, 22.22%, 22.22%, 27.78%, 38.9% and 55.56% of the isolated strains were found resistant to gentamicin, mupirocin, ciprofloxacin, moxifloxacin, clindamycin, co-trimoxazole and erythromycin, respectively [Table 2]. MAR index of each isolated S. aureus strains was determined, and none of the isolates had MAR of zero or one [Figure 1].
Figure 1: Number of isolated Staphylococcus aureus strains having different MAR index. MAR: Multiple antibiotic resistance

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Table 2: Antimicrobial susceptibility of the isolated Staphylococcus aureus strains

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Simultaneously, molecular detection of the mecA gene, responsible for the mutation in penicillin-binding protein2a (PBP2a) and lukS/F-PV genes, encoding the pvl S/F bicomponent proteins was performed. mecA gene was detected in all MRSA strains (identified by cefoxitin 30 μg disc diffusion) whereas the lukS/F-PV gene was observed in none of the isolated MRSA strains [Figure 2].
Figure 2: Gel electrophoresis image showing the amplification of mecA gene. Lane 1,10:100 bp ladder, Lane 2,11: negative control, Lane 3, 4, 6, 7, 9, 12, 13, 15 MRSA strains, Lae 5, 6, 14, 16, 17 MSSA strains. MRSA: Methicillin-resistant Staphylococcus aureus

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  Discussion Top

S. aureus is a Gram-positive pathogen that causes a variety of human diseases such as infections of the skin, wound, bone, joints and surgical site infection, bloodstream infection as well as ventilator-associated pneumonia.[11] The infections by S. aureus result in asymptomatic carriage, nevertheless, it poses a severe health burden in hospital settings especially due to an upsurge in the resistance to methicillin and other classes of antibiotics. Although S. aureus is a frank pathogen, however, due to its wide array of virulence factors, it can cause invasive diseases that increase their likelihood of gaining access to normally sterile sites. The MRSA strains, being resistant to all β-lactam groups of antibiotics, pose a challenge to treating physicians with restricted antibiotic options. In such cases, glycopeptide antibiotics such as vancomycin become the drug of choice, against whom increased MIC/resistance has also been reported from different parts of the world.[12],[13]

This bacterium is a commensal of skin and mucosa of human beings, especially residing in the anterior nares, axilla and perineum. The anterior nares (vestibulum nasi) are the most frequently colonised sites of health care workers, patients and the general population. From them, it is transmitted to the other patients by different modes, contact being the most common route.[4] Anterior nares colonisation plays an important role in the pathogenesis of S. aureus infections, especially in patients undergoing surgery, dialysis and in intensive care units.[14],[15],[16]

Medical students are an important but forgotten group of health care workers who usually do not have sufficient knowledge of appropriate infection control policies. The medical students pursuing their MBBS course come in contact with the patients during their clinical postings in the hospital. These MBBS students colonised with S. aureus may be the source of transmission as shown in our study. A total of 12% of the medical students were colonised by S. aureus amongst which 5.33% were MRSA carriers. These MBBS students had varied duration of exposure to the hospital as the 1st-semester students usually do not have any exposure to the hospital environment, whereas the 5th- and 9th-semester students have exposure of 1.5 and 3.5 years, respectively. In our study, S. aureus nasal colonisation was observed in 10 students of 5th semester, whereas 3 and 5 students belonged to the 1st and 9th semesters, respectively. A similar study conducted in Jeddah, Saudi Arabia, reported a nasal colonisation in 25.33% of enrolled medical students (38/150) with MRSA nasal carriage of 6.7%.[17] Worldwide, S. aureus anterior nares colonisation amongst health care personnel varies from 1.1% to 34.6%.[5],[18],[19],[20],[21] These colonised medical personnel may be the source of S. aureus infections. Interestingly, the report by Carmona et al. documents only 1·9% MRSA prevalence amongst 1st-year medical undergraduate, while in all students, the prevalence was found to be only 0.6%.[5]

The anterior nares colonisation of methicillin-sensitive or resistant S. aureus strains is either community- or hospital-acquired. S. aureus strains isolated from the 1st-semester medical undergraduate, with no hospital exposure, are considered community-acquired whereas the strains isolated from 5th- and 9th-semester students (as they are exposed to the hospital environments) are usually considered hospital-acquired. However, in general, the strains isolated from the patients with hospital admission for >48 h are considered hospital-acquired, but it is very difficult to categorise the isolates as community- or hospital-acquired strains.

The MRSA isolates are resistant to all β-lactam antibiotics due to mutated penicillin-binding protein 2a that is encoded by the mecA gene. Similarly, amongst multiple virulence factors, exhibited by some strains of S. aureus is the Panton–Valentine leucocidin (pvl), encoded by two genes, lukS-PV and lukF-PV. It belongs to the synergohymenotropic toxin family that engenders pores in the cell membranes. In general, the pvl-positive MRSA isolates cause mild skin or soft-tissue infections; however, in severe cases, they may cause necrotising pneumonia and sepsis. Epidemiological data suggest that pvl is present in the majority of community-associated MRSA isolates but seldom present in hospital isolates, therefore, it is recognised as the marker of community-acquired strains. A plethora of literature establishes the association of high virulence of community-acquired MRSA with pvl genes, but in our study, we did not get pvl genes in any of the isolates. Our work has similar findings as Karmakar et al. where they reported the presence of pvl gene in only 9% of the isolated CA-MRSA strains in West Bengal, India.[22]

Amongst the colonised 18 MBBS students 3, 10 and 5 belonged to 1st, 5th and 9th semesters respectively. Amongst them, 2, 3 and 3 medical undergraduate students having nasal MRSA colonisation belong to 1st, 5th and 9th semesters, respectively. The higher nares colonisation rate amongst the 5th-semester medical undergraduate students may be attributed to the little knowledge of infection control practices. The 9th-semester students also have S. aureus nasal colonisation but the reduced number may be attributed to the transient nature of colonisation, which may have occurred in their previous semester.

Colonisation of S. aureus strains in the anterior nares precedes the transmission through nose picking, hands, sneezing and coughing. Anterior nares colonisation increases the risk by 2–10 times for patients undergoing surgery and haemodialysis.[23] Recently, a Bengal Bay clone ST772-MRSA-V outbreak has been reported from Akershus University Hospital, Lørenskog, Norway, where amongst the 25 strains of S. aureus isolated, 7 strains were from patients who were carriers, whereas 18 similar strains causing infections were isolated from the patients.[24]

These commensal S. aureus strains have varied antimicrobial sensitivity as in our study, all the isolates were resistant to one or more tested drugs. MAR index, the percentage of the resistant drugs in comparison to the tested drugs, also varied for the isolates. For instance, only one isolate exhibited a MAR index of 0.58 whereas four isolates had a MAR index of 0.5. This mid-way distribution of high MAR indices shows the difficult eradication of these pathogens in a clinical setup. This higher MAR index may be attributed to the frequent use of antibiotics, which facilitates the survival of only drug-resistant pathogens or promotes the presence of multiple-resistant genes in their genome.

These MRSA strains, being resistant to all β-lactam groups of antibiotics, usually are resistant to other frequently used antibiotics such as fluoroquinolones, sulpha drugs, macrolides and aminoglycosides. Topical mupirocin is considered the drug of choice for the eradication of this commensal S. aureus including MRSA as it significantly reduces the carrier stage.[24] An upsurge in the resistance against topical mupirocin and postmupirocin its recolonisation has also been reported which implies the importance of exploration of other effective drugs.[25] In our present study, two isolated strains exhibited a high-level mupirocin resistance. In such conditions, other drugs such as cotrimoxazole, clindamycin, ciprofloxacin and erythromycin are widely used, however, in our present study, 7, 8, 4 and 11 strains, respectively, were found resistant to these antibiotics as well. Results supporting our findings are also reported earlier.[26],[27],[28] Ramana et al. reported 25% erythromycin and 14.3% cotrimoxazole resistance amongst the isolated S. aureus from the anterior nares of school-going children.[29] Even Singh et al. have reported 7.55% MRSA anterior nares colonisation amongst health care workers with cotrimoxazole (93.3%), ciprofloxacin (80%) and erythromycin (66.66%) resistance.[30]

Isolation of eight MRSA from medical undergraduate students strongly endorses the implementation of the strict guidelines of hospital infection control. Strict handwashing must be strictly followed. In addition, random nasal screenings to detect nasal colonisation must be done so that preventive decolonisation action can be taken.

  Conclusion Top

There is a need of education regarding infection control practices in medical schools, before starting ward postings to stress the importance of handwashing and wearing masks properly.

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Conflicts of interest

There are no conflicts of interest.

  References Top

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