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Year : 2021  |  Volume : 10  |  Issue : 1  |  Page : 2-8

Nasal carriage of antibiotic-resistant staphylococci among undergraduate medical students, with special reference to methicillin-resistant Staphylococcus aureus

Department of Microbiology, Sri Venkateswara Institute of Medical Sciences, Tirupati, Andhra Pradesh, India

Date of Submission09-Jul-2019
Date of Decision21-May-2020
Date of Acceptance09-Jul-2020
Date of Web Publication4-Mar-2021

Correspondence Address:
Abhijit Chaudhury
Professor, Department of Microbiology, Sri Venkateswara Institute of Medical Sciences, Tirupati 517 507, Andhra Pradesh
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/JCSR.JCSR_88_19

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Background: Staphylococcus aureus and other staphylococci are the commensals of the human body, the anterior nares being an important niche for colonisation. The medical students constitute an important component of the hospital population. Studies of staphylococcal carriage among the medical students are almost non-existent from India. This study was conducted with the primary aim of finding out the nasal carriage of antibiotic-resistant staphylococci among the medical students in our institution.
Methods: A total of 162 medical students equally divided between the preclinical and clinical batches were the study participants. A nasal swab was collected from the participants and cultured. Suspected colonies were identified as S. aureus and antimicrobial susceptibility done by standard methods. The students were also asked to fill up a questionnaire to identify any risk factor associated with staphylococcal carriage.
Results: The overall colonisation rate was 48.8% for S. aureus with 45.7% in the non-exposed pre-clinical students' group to 51.8% in the exposed clinical students' group which was not significant. The carriage rate for methicillin-resistant S. aureus was 6.3% among the S. aureus isolates. A survey of the risk factors revealed no significant association of hostel stay, family size, previous hospital admission, skin or soft-tissue infection with increased carriage rate. However, a history of previous antibiotic therapy had a significant association with nasal carriage.
Conclusions: High rates of colonisation with S. aureus calls for further detailed multicentric studies with application of moecular methods from India.

Keywords: Carriers, medical, methicillin-resistant Staphylococcus aureus, Staphylococcus, students

How to cite this article:
V. Manyala PV, Chaudhury M, Anagoni S, Pulicherla B, Chaudhury A. Nasal carriage of antibiotic-resistant staphylococci among undergraduate medical students, with special reference to methicillin-resistant Staphylococcus aureus. J Clin Sci Res 2021;10:2-8

How to cite this URL:
V. Manyala PV, Chaudhury M, Anagoni S, Pulicherla B, Chaudhury A. Nasal carriage of antibiotic-resistant staphylococci among undergraduate medical students, with special reference to methicillin-resistant Staphylococcus aureus. J Clin Sci Res [serial online] 2021 [cited 2021 Aug 3];10:2-8. Available from: https://www.jcsr.co.in/text.asp?2021/10/1/2/310771

  Introduction Top

Staphylococcus aureus and certain other members of the genus Staphylococcus are the important pathogens which can cause a wide variety of infections both in the community and hospital settings. The importance of these organisms, particularly S. aureus has increased because of the emergence of multiple drug resistance which include methicillin resistance. Staphylococci form part of the normal commensal flora of skin, and it can be cultured from the multiple sites of the skin and mucosal surfaces.[1] However, the primary reservoir of staphylococci is thought to be the vestibulum nasi (anterior nares), and the organism can consistently be cultured from this area.[2] These carrier individuals are the potential sources of spread of infection not only in the health-care settings, but also in the community, in addition to posing a risk for endogenous infection for them.[3]

The prevalence of S. aureus nasal carriage varies according to the population studied. In the general population, the prevalence rate has been found to range from 19.0% to 55.1%.[1] In one recent Indian study done in the community setting, S. aureus colonisation was found in 12% of participants and methicillin-resistant S. aureus (MRSA) was identified in 5% of the study subjects.[4] However, apart from this recent study and a few older studies, data from the general Indian population are lacking. One set of population in which there is a relative paucity of information regarding S. aureus and MRSA carriage are the medical undergraduate students. A PubMed search revealed no study on this subject from the medical student communities from India, who are regularly coming in contact with the hospital patient population during their clinical postings. This study was conducted to look into this unexplored area wherein the medical students were screened for nasal carriage of staphylococci, and in particular S. aureus and MRSA. This is because the chances of transfer of MRSA from the student carriers to the patients as well as the acquisition of MRSA strains from the patient population and further dissemination in the community by the medical students is a real threat.

  Material and Methods Top

It was a prospective study conducted in a two months' period of May–June, 2018 at Sri Venkateswara Institute of Medical Sciences, Sri Padmavathi Medical College for Women, Tirupati, India. Ethical clearance was taken from the Institutional Ethical Committee before the commencement of the study and informed consent was obtained from the study participants. They were also required to fill up a questionnaire to find out any risk factor present.

Undergraduate medical students of the 2nd and 4th semester acted as volunteers for the study. The 2nd semester students comprised the group who have not come into hospital patient contact as they have not started the clinical rotations. The 4th semester students have started coming in contact with the hospital patients as they have already started the clinical rotations. Considering the prevalence of the disease to be 12%,[4] margin of error 5%, 95% confidence interval, the sample size was calculated to be 162 which was equally divided between the two groups (81 in each group). This was done since testing for 162 samples in each group was not possible because of logistic reasons.

A sterile cotton swab moistened with sterile normal saline was used to collect the samples. Sample collection was done at the microbiology department under the supervision of the guide. For each participant, the swab was rolled inside both the nostrils and was immediately processed.

The swabs were inoculated in blood agar and Mannitol salt agar. The plates were incubated at 37°C for 18 h. Identification of Staphylococcus and S. aureus was done on the basis of the following characteristics as described earlier:[5] colony character, Gram stain morphology, catalase test, slide coagulase test and tube coagulase test.

Antibiogram of all the isolates was determined by Kirby–Bauer's disk diffusion technique on Mueller-Hinton agar as per the CLSI guidelines.[6] The antibiotic panel included: penicillin (10 U), ampicillin (10 μg), amoxycillin-clavulanic acid (30 μg), Co-trimoxazole (25 μg), erythromycin (15 μg), tetracycline (30 μg), ciprofloxacin (5 μg), gentamicin (10 μg), vancomycin (30 μg) and linezolid (30 μg). S. aureus ATCC 25923 was used as the sensitive control strain. For vancomycin susceptibility where CLSI guideline for interpretation is not available, the British Society for Antimicrobial Chemotherapy guidelines was followed.[7]

Cefoxitin (30 μg) disc was used as a surrogate marker for methicillin susceptibility testing.[6]

Statistical analysis

Data were entered in Microsoft Excel (Microsoft Corporation, Richmond), and the results expressed as simple counts and percentages. The risk factor association with Staphylococcal colonisation as well as the association between MRSA isolated from hospital exposed and non-exposed participants was carried out using Chi-square test. A P-value < 0.05 wa considered to be statistically significant.

  Results Top

A total of 162 students were enrolled into the study during the 2-month study period. All the study participants were females and in the age range of 18–20 years.

S. aureus colonisation was found in 79 (48.8%) of participants. Coagulase-negative Staphylococcus spp (CONS) colonisation was found in 77/162 (47.5%) of members and in remaining 6/162 (3.7%) of members no growth of any Staphylococcus spp was observed [Table 1]. The study population consisted of two groups each comprising of 81 students. One group belonged to the II Semester MBBS students in their pre-clinical year who have not started the clinical rotation (not regularly exposed to hospital environment). The other group was the IV semester students who have started clinical rotation about 1 year back (regularly exposed to hospital environment). The comparison of the two groups [Table 1] showed that 42 (51.8%) of the exposed 4th semester students carried S. aureus compared to 37 (45.7%) of the II semester non-exposed group which was not significant (P > 0.05).
Table 1: Distribution of Staphylococcus aureus and coagulase-negative Staphylococcus spp

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[Table 2] shows the resistance patterns of the isolates belonging to the two groups against 11 common antibacterial agents. Among the non-exposed population, all the isolates of S. aureus and CONS were uniformly resistant to penicillin, ampicillin and amoxycillin-clavulanate combination, though cefoxitin (methicillin) resistance was shown by only 3 and 1 isolates of S. aureus and CONS, respectively. The resistance frequency for erythromycin was quite high (>60%) followed by co-trimoxazole and tetracycline. Good activity was shown by gentamicin, linezolid and vancomycin. Among the exposed group, examination of the antibiotic resistance pattern revealed almost a parallel trend, with some minor variation when compared to the non-exposed group.
Table 2: Antimicrobial resistance pattern of the isolates in the two groups

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The isolation rate of MRSA was low in this study population. MRSA could be isolated in a total of 5 out of the total 79 S. aureus (6.3%), while overall, the carriage rate was 5/162 (3.1%). Of these 5 MRSA, 3 belonged to the exposed group. Interestingly, we could also isolate four strains of methicillin-resistant CONS in our study population. Encompassing the CONS, the overall prevalence of methicillin-resistant staphylococci isolates in this study amounts to 9/162 (5.5%). Sensitivity profile revealed a mixed pattern of sensitivity, with all the five strains being sensitive to gentamicin and ciprofloxacin; apart from linezolid and vancomycin.

In this study, certain putative risk factors which have been associated with nasal carriage of S. aureus were looked into by providing a questionnaire to the study participants. [Table 3] shows the result of the survey among the two groups of students. [Table 4] and [Table 5] show the results of this survey among the two groups of students. It was observed that almost all of these factors were not significantly associated with S. aureus carriage. The one exception was the association of recent consumption of antibiotics in the exposed group of students, where a level of significance of 0.033 (P < 0.05) was noted.
Table 3: Assessment of presence of putative risk factors among participants

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Table 4: Association of students' Staphylococcus aureus carriage with risk factors (not-exposed group)

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Table 5: Association of students' Staphylococcus aureus carriage with risk factors (exposed group)

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  Discussion Top

The principal aim of the present study was to investigate the nasal carriage rate among two groups of medical students. One group comprised pre-clinical first year students who have not started clinical rotation (the non-exposed group), while the other group had started clinical rotation with daily hospital visit (the exposed group).

The overall colonisation rate for S. aureus was 48.8%, whereas 47.5% harboured CONS. This carriage rate was found to be comparable to a study from USA where an almost similar sample size (n = 132) showed 47% carriage rate for S. aureus.[8] A larger study from China with 1149 samples also showed a carriage rate of 45%.[9] On the other hand, a study from Nepal found only 15% overall carriage rate.[10] In our study, we found 3.7% of the participants showing no growth of any staphylococci. This set of individuals can either be intermittent carriers or non-carriers which could have only been differentiated if two culture swabs had been obtained and the 'culture rule' had been applied.[11]

We found an increase in S. aureus carriage rate from 45.7% in the non-exposed group to 51.8% in the exposed group, whereas the carriage rate of CONS decreased proportionately. However, this increase was not statistically significant (P > 0.05). A few other studies have looked into the actual difference in the prevalence of nasal carriage of S. aureus among the clinical and non-clinical group of students. A Tanzanian study[12] also found almost similar rates of carriage among the clinical and pre-clinical groups of students (22% vs. 20%). Similar findings were also reported from an earlier study from Australia[13] where 40% of the clinical students and 35% of the pre-clinical students were S. aureus carriers. On the other hand, an US study found the carrier rate among clinical students to be 23% compared to only 7% in the pre-clinical group.[14] These findings show that carriage rates are variable across the globe and these variations may be multi-factorial where both the host and the environmental factors play a crucial role in determining the carrier state. However, it can be inferred that the exposure to clinics does not influence the carriage of S. aureus among the medical students since in both the groups the prevalence is almost similar.

In our study, the carriage rate for MRSA was 6.3% among the S. aureus isolates (n = 79), while overall, it was 3.1% (n = 162). MR-CONS could be isolated from four samples. In the US study mentioned earlier,[8] the MRSA carriage was 5% similar to our finding. Similar carriage of 4% was noted in the Nepalese study.[10] A recent study conducted among undergraduate medical students by Royal College of Surgeons, Ireland, with 444 participants found MRSA carriage rate of 6.6% and MR-CONS rate of 13.1%.[15] In a study from India as well, MRSA carriage rate was 6.8%.[16] However, in the Chinese[9] and Tanzanian[12] studies, much lower carriage rates were found of the Figures 1% and 0.3%, respectively. In contrast, an unusually higher MRSA carriage was found in an earlier Indian study[16] where a comparatively lower sample size of 50 yielded 24% MRSA. Similarly, a Canadian study with sample size 61 found 21% MRSA carriage.[17] Similar carriage rates of MRSA (4%–6%) in diverse geographic locations of USA, Ireland and India substantiate that the MRSA carriage is almost constant, with some minor exceptions.

The antimicrobial susceptibility of the S. aureus and CONS isolates was also examined in this study. In the pre-clinical non-exposed group, all the strains of both S. aureus and CONS were found to be resistant to the penicillin group of antibacterial agents including clavulanic acid combination. On the other hand, a few isolate showed sensitivity to these agents among the exposed group. In the Tanzanian study,[12] all the isolates were sensitive to ciprofloxacin, while ampicillin resistance was high (87.9%), comparable to our study, whereas lower resistance was seen for erythromycin (19.7%) and tetracycline (9.1%). In the study from Nepal,[10] ciprofloxacin resistance was higher (36.7%) compared to our study (overall 17.6% resistance). In this same study, 27% of strains were sensitive to penicillin G, which is higher compared to our study where <10% of strains were sensitive to penicillin G. Orlin et al.[18] from Israel found high resistance frequency of 38% for erythromycin and only 2% resistance for ciprofloxacin against the S. aureus strains while overall gentamicin resistance was 10%. In our study, we found gentamicin to be highly active against both S. aureus and CONS with resistance frequency between 2.4% and 7.1% only. This may be explained by the infrequent use of parenteral preparations for the treatment of minor infections and the frequent use of over-the-counter oral preparation such as ciprofloxacin, ampicillin, amoxycillin-clavulanate, tetracylines and erythromycin.

Various workers have tried to link certain modifiable or non-modifiable risk factors to S. aureus or MRSA carriage. In this study, ten risk factors were looked into by providing a questionnaire to the participants. In a study[19] large households (≥5 members) were found to be positively associated with S. aureus nasal carriage. However, in our study, household member size ≥4 was not significantly associated with S. aureus carriage. Similarly, hostel stay was not associated with increased S. aureus carriage rate in our study. Thus, overcrowding or close contact was not found be important risk factors for colonisation in our study, although the contrary has been found in other studies.[19],[20] The exposure to health-care systems has been found to be associated with increased risk of S. aureus and MRSA carriage in various studies.[1],[21],[22] In the present study, no significant differences were found in the carriage rate of pre-clinical and clinical students. The only significant association (P < 0.05) was found with respect to antibiotic use in immediate past in the students who have started clinical rotation (the exposed group). In a study,[23] no significant association was found between antibiotic usage in the past 6 months and MRSA carriage among infants in a day care centre, although more than 80% of the participants had taken antibiotics in the previous 6 months. In a Taiwanese study,[24] medical students who took antibiotics in the past year were significantly less likely to be colonised by S. aureus compared with those who did not.Hence, the significance of our finding remains unclear.

Certain limitations of this study need to be mentioned. The study examined the students in the second group who have started clinical rotation just one year back. The inclusion of final year students who have been in contact with hospital environment for a much longer period could have revealed additional findings, particularly with respect to MRSA. Second, genotypic study with the isolates would have given us more insight into the identification of clonal lineage of the strains and SCCmec types. Third, the presence of Panton-Valentine leucocidin genes (lukF/S-PV) in the isolates would have given us some idea about the acquisition of the strains from community or hospital environment. These genotypic parameters could not be investigated due to the dual constraint of time and financial support.

To conclude, this preliminary study throws some light about the distribution of S. aureus and CONS, including MRSA and MR-CONS in a female medical student community. It is alarming that many of the participants who have not started clinical rotation are already colonised with multidrug-resistant staphylococci, including MRSA. This signifies a large pool of antibiotic-resistant staphylococci in the community who pose significant risk to the patient population when these students start coming in contact with patients once they start clinical rotation. With the increasing influx of CA-MRSA strains into the hospital environment, and emergence of HA-MRSA strains with features similar to CA-MRSA, there will be an increase in the transmission and emergence of these MRSA strains in the hospital environment. The other way round, spread of the hospital strains into the community will result in difficult to treat simple infections. The net result will be an increase in antibiotic pressure leading to the spread of antimicrobial resistance in both settings.


This study was done as part of Short Term Studentship for undergraduate medical students awarded by Indian Council for Medical Research, New Delhi to Preethika V. V. Manyala (STS-2018 Ref No.2018-00331).

Financial support and sponsorship


Conflicts of interest

There are no conflicts of interest.

  References Top

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  [Table 1], [Table 2], [Table 3], [Table 4], [Table 5]


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