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 Table of Contents  
ORIGINAL ARTICLE
Year : 2018  |  Volume : 13  |  Issue : 2  |  Page : 91-94

Nasal carriage of Staphylococcus aureus among undergraduate medical students: Prevalence and antibiogram including methicillin resistance, inducible clindamycin resistance, and high-level mupirocin resistance


Department of Microbiology, Jawaharlal Nehru Medical College, Wardha, Maharashtra, India

Date of Web Publication23-Nov-2018

Correspondence Address:
Dr. Gargi Mudey
Department of Microbiology, Jawaharlal Nehru Medical College, Sawangi (M), Wardha, Maharashtra
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/jdmimsu.jdmimsu_10_18

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  Abstract 


Background: Treatment of infections caused by Staphylococcus aureus has become more problematic since the development of methicillin-resistant S. aureus (MRSA). Medical students carrying S. aureus can be a potential source of infection to the patients. The anterior nares have been shown to be the main reservoir of S. aureus in both children and adults. Hence, the study was carried out to find out the prevalence of nasal carriage of S. aureus and its antimicrobial resistance pattern in undergraduate medical students. Materials and Methods: Nasal swabs of undergraduate medical students were collected aseptically and cultured using standard microbiological methods. Antibiotic susceptibility was done by disc diffusion method as per the CLSI guidelines. Results: The prevalence of S. aureus nasal carriage was 16%. The prevalence of MRSA and inducible clindamycin resistance was 5% and 3.5%, respectively. No isolate showed high-level mupirocin resistance. Interpretation and Conclusions: Nasal carriage of S. aureus is a major threat for public health and required surveillance.

Keywords: Antibiotic susceptibility, methicillin-resistant Staphylococcus aureus, methicillin-sensitive Staphylococcus aureus, nasal carriage, Staphylococcus aureus


How to cite this article:
Munjal R, Mudey G. Nasal carriage of Staphylococcus aureus among undergraduate medical students: Prevalence and antibiogram including methicillin resistance, inducible clindamycin resistance, and high-level mupirocin resistance. J Datta Meghe Inst Med Sci Univ 2018;13:91-4

How to cite this URL:
Munjal R, Mudey G. Nasal carriage of Staphylococcus aureus among undergraduate medical students: Prevalence and antibiogram including methicillin resistance, inducible clindamycin resistance, and high-level mupirocin resistance. J Datta Meghe Inst Med Sci Univ [serial online] 2018 [cited 2018 Dec 16];13:91-4. Available from: http://www.journaldmims.com/text.asp?2018/13/2/91/246006




  Introduction Top


Staphylococcus aureus is a common pathogen responsible for community- as well as hospital-associated infections. The infections caused by S. aureus range from minor skin infections to severe life-threatening infections.[1] Within the hospital, colonized health-care workers act as a reservoir for the spread of S. aureus to uncolonized susceptible patients. The anterior nares have been shown to be the main reservoir of S. aureus in both children and adults. S. aureus can colonize healthy individuals. Nasal carriage of S. aureus acts not only as an endogenous reservoir for clinical infections in the colonized individual but also as a source of cross-colonization for community spread.[2]

Treatment of infections caused by S. aureus has become more problematic since the development of methicillin-resistant S. aureus (MRSA).

MRSA are those strains of S. aureus that express mecA or another mechanism of methicillin resistance, such as changes in affinity of penicillin-binding proteins for oxacillin. For MRSA, other β-lactam/β-lactamase inhibitor combinations, cephems (with exception of the cephalosporins with anti-MRSA activity) and carbapenems, may appear active in vivo but are not effective clinically. MRSA strains also show multidrug resistance. The incidence of nosocomial infection caused by MRSA continues to increase worldwide.[3],[4]

In view of the above facts and observations, it was felt necessary to study the prevalence of nasal carriage of S. aureus and its antimicrobial resistance pattern in undergraduate medical students.


  Materials and Methods Top


The study was conducted in the Department of Microbiology, Jawaharlal Nehru Medical College (JNMC), and Acharya Vinoba Bhave Rural Hospital, Sawangi (M), Wardha, for 2 months from June 1, 2014, to July 31, 2014.

The study was conducted after obtaining approval from the Institutional Ethical Committee. A total of 200 medical students (final-year MBBS) not suffering from any upper respiratory tract infection and who have not received any antibiotics for the past 30 days were selected for the present study.

After explaining the details of the proposed project, letter of informed consent signed by each volunteer was obtained. Details such as age, sex, health status, and relevant data were collected from each volunteer. Nasal swabs were obtained from each volunteer and were subjected to drug-sensitivity tests.

Collection of the nasal swab

Cotton swabs sterilized by hot air oven at 160°C for 1 h were used for nasal swabbing of the anterior nares of the healthy volunteers. The swabs moistened with sterile saline were rubbed very well by rotating 5 times over the inner wall of the ala and nasal septum of both nostrils.

Culture of nasal swabs for identification of Staphylococcus aureus

The nasal swabs were cultured on mannitol salt agar (selective medium for S. aureus) within 1 h after collection by streaking as per the conventional technique [Figure 1]. The culture plates were incubated at 37°C for 24–48 h. The study participants whose swabs showed suspected S. aureus colonies (yellow colonies surrounded by yellow medium due to mannitol fermentation) were called again to collect second swab. This time swabs were inoculated on nutrient agar, blood agar, and mannitol salt agar. The culture plates were incubated at 37°C for 24–48 h. Identification was performed on the basis of colony characteristics, Gram staining, catalase test, and coagulase test (slide and tube) as per the standard microbiological methods.[5]
Figure 1: Culture of nasal swabs on mannitol salt agar

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S. aureus isolates were identified by β-hemolysis on blood agar, golden yellow pigment on nutrient agar, Gram-positive cocci in clusters on Gram staining, fermenting mannitol, catalase test positive, and coagulase test positive.

Antibiotic susceptibility testing

All the S. aureus isolates were subjected to in vitro antibiotic susceptibility testing by disc diffusion test on Muller-Hinton agar as per the CLSI guidelines, 2012.[4]

Antibiotic discs from HiMedia Ltd, Mumbai, were used. Interpretation of antibiotic susceptibility was done using HiMedia interpretation chart and following the CLSI guidelines 2012.

Methicillin-resistant Staphylococcus aureus

For screening, cefoxitin disc method was used. All the S. aureus isolates were subjected to in vitro antibiotic susceptibility testing for cefoxitin (30 μg) by disc diffusion test on Muller-Hinton agar. Isolates giving inhibition zone diameter of ≤21 mm for cefoxitin (30 μg) disc were labeled as methicillin resistant and a zone diameter of ≥22 mm as methicillin sensitive. For confirmation, oxacillin Methicillin Inducible Clindamycin (MIC) testing using Ezy MIC strips was done. Isolates with MIC for oxacillin ≥4 were labeled methicillin resistant and those with MIC for oxacillin ≤2 as methicillin sensitive.

Inducible clindamycin resistance

Erythromycin (15 μg) disc was placed at a distance of 15 mm (edge to edge) from clindamycin (2 μg). Staphylococcal isolate showing resistance to erythromycin (zone size ≤13 mm) while being sensitive to clindamycin (zone size ≥21 mm) and giving D-shaped zone of inhibition around clindamycin with flattening toward erythromycin disc was labeled as having inducible clindamycin resistance (iMLSB). Hazy growth within the zone of inhibition around clindamycin even if no D-zone is apparent was taken as clindamycin resistant.

High-level mupirocin resistance

Mupirocin discs 200 μg from Oxoid, India, were used. All the S. aureus isolates were subjected to in vitro antibiotic susceptibility testing of mupirocin (200 μg) by disc diffusion test on Muller-Hinton agar. No zone for mupirocin (200 μg) was labeled high-level mupirocin resistance.

Control strains used were S. aureus ATCC25293 and confirmed strains of MRSA and iMLSB from Microbiology Laboratory, JNMC.


  Results Top


Nasal swabs of 200 undergraduate medical students (final-year MBBS) were screened for the presence of S. aureus. From 200 nasal swabs, S. aureus was isolated in 32 (16%). Among these, 3 (1.5%) were MRSA and 29 (14.5%) were methicillin-sensitive S. aureus.

Antibiotic susceptibility testing of all the isolates was done. [Table 1] and [Table 2] depict the sensitivity and resistance pattern in nasal isolates of S. aureus.
Table 1: Sensitivity pattern of methicillin -resistant and methicillin -sensitive Staphylococcus aureus isolated from nasal swabs of medical undergraduate students

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Table 2: Resistance pattern of nasal isolates

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All MRSA isolates were erythromycin and clindamycin resistant, one inducible clindamycin resistant, and two constitutive clindamycin resistant. One constitutive clindamycin-resistant isolate was low-level mupirocin resistant; others were mupirocin sensitive.


  Discussion Top


The present study showed an overall prevalence of 16% S. aureus in the nostrils of the healthy undergraduate medical students. The prevalence of S. aureus nasal carriage was found to be higher in different studies from India, i.e., 62.14% in Karnataka,[6] 52.35% in Haryana,[7] 47.62% in Aligarh,[3] and 39.25% in Bangalore.[8] The findings in our study correlate with the findings of studies conducted in other countries of the world such as 18.48% among patients with surgical site infection in the Netherlands,[9] 17.03% among midwifery students in Turkey,[10] and 15.4% among healthcare workers in China.[11]

Higher prevalence in India may be due to poor socioeconomic conditions and overcrowding in India. Among medical students, difference in prevalence may be due to factors such as number of years of service in the hospital, aseptic precautions, and protective measures they are using.

However, the prevalence of nasal MRSA carriage in our study 1.5% was significantly lower than previously reported from different cities in India, including Aligarh (21.43%), Bangalore (14.52%), and Bagalkot, Karnataka (40.28%).[3],[6],[8] Our results are comparable with that of other countries such as Turkey (2.96%), China (3%), and Serbia (0.16%).[2],[10],[11]

The overall susceptibility test result showed penicillin to be the least effective drug against S. aureus (3.13%), which is in agreement to other studies such as 3.22% in Serbia[2] and 3.5% in China.[11] In contrast, penicillin was found effective antibiotic in the study at Srinagar.[12] Susceptibility to rifampicin, doxycycline, and vancomycin was found to be 100%. Thus, these antibiotics emerge as the best alternatives for the treatment of S. aureus infections. This result is in agreement with many other studies conducted across India.[1],[7],[12] Mupirocin was highly sensitive as in many other studies.[8],[11]

Our study revealed 34.38% sensitive to erythromycin and 53.13% to clindamycin. These data contradict several studies reporting high rates of sensitivity to erythromycin and clindamycin for S. aureus isolates recovered from the nares.[1],[7],[12]

Low sensitivity to these antibiotics in our area may be a result of antibiotic abuse in the community. This observation implies that these antibiotics cannot longer be effectively used for empirical therapy in the study area.

In our study, iMLSB in S. aureus was found to be 3.5%. This is less when compared with data from other studies. It was 16.7% among nursing students[13] and 16.40% among health-care workers.[6]

In this study, no isolate was high-level mupirocin resistant which is comparable to other studies on nasal isolates.[8],[11],[14] However, higher prevalence of high-level mupirocin resistance was seen in clinical isolates. It was 2% in study at Lucknow and 16.66% in study at Rochester.[5],[15]


  Interpretation and Conclusions Top


Nasal carriage of S. aureus is a major threat for public health as they can disseminate the same to the patients as well as to their colleagues. To reduce the prevalence and antimicrobial resistance, emphasis should be given to aseptic precaution, protective measures, and proper protocol for eradication of nasal carriage.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
  References Top

1.
Pathak A, Marothi Y, Iyer RV, Singh B, Sharma M, Eriksson B, et al. Nasal carriage and antimicrobial susceptibility of Staphylococcus aureus in healthy preschool children in Ujjain, India. BMC Pediatr 2010;10:100.  Back to cited text no. 1
    
2.
Jeremic LP. Frequency of methicillin-resistant Staphylococcus aureus (MRSA) in healthy nasal carriers in Pomoravlje district. Acta Med Med 2010;49:33-5.  Back to cited text no. 2
    
3.
Kumar P, Shukla I, Varshney S. Nasal screening of health care workers for nasal carriage if coagulase positive MRSA and prevalence of nasal colonization with Staphylococcus aureus. Biol Med 2011;3:182-6.  Back to cited text no. 3
    
4.
Wayne PA. Clinical and Laboratory Standards Institute (CLSI) Guidelines 2012: Performance Standards for Antimicrobial Susceptibility Testing; Seventeenth Information Supplement; M100-S22. Vol. 32; January, 2012.  Back to cited text no. 4
    
5.
Rotger M, Trampuz A, Piper KE, Steckelberg JM, Patel R. Phenotypic and genotypic mupirocin resistance among staphylococci causing prosthetic joint infection. J Clin Microbiol 2005;43:4266-8.  Back to cited text no. 5
    
6.
Mahesh CB, Ramakant BK, Jagadeesh VS. The prevalence of inducible and constitutive clindamycin resistance among the nasal isolates of staphylococci. J Clin Diagn Res 2013;7:1620-2.  Back to cited text no. 6
    
7.
Chatterjee SS, Ray P, Aggarwal A, Das A, Sharma M. A community-based study on nasal carriage of Staphylococcus aureus. Indian J Med Res 2009;130:742-8.  Back to cited text no. 7
[PUBMED]  [Full text]  
8.
Ravi GC, Shivaprasad A, Shenoy P, Nagaraj BT. Changing pattern of nasal carriage of Staphylococcus aureus in undergraduate medical students. Int J Appl Biol Pharm Technol 2011;2:58-63.  Back to cited text no. 8
    
9.
Yassin NA, Hassan AO. Nasal carriage of methicillin – Resistant/sensitive Staphylococcus aureus among students in faculty of medical sciences, Duhok university. Adv Trop Med Public Health Int 2013;3:65-72.  Back to cited text no. 9
    
10.
Kirecci E, Ozer A, Aral M, Miraloglu M. A research of nasal methicillin resistant/sensitive Staphylococcus aureus and pharyngeal beta-haemolytic Streptococcus carriage in midwifery students in Kahramanmaras, Eastern Mediterranean region of Turkey. Ethiop J Health Dev 2010;24:57-60.  Back to cited text no. 10
    
11.
Du J, Chen C, Ding B, Tu J, Qin Z, Parsons C, et al. Molecular characterization and antimicrobial susceptibility of nasal Staphylococcus aureus isolates from a Chinese medical college campus. PLoS One 2011;6:e27328.  Back to cited text no. 11
    
12.
Fomda BA, Thokar MA, Khan A, Bhat JA, Zahoor D, Bashir G, et al. Nasal carriage of methicillin-resistant Staphylococcus aureus among healthy population of Kashmir, India. Indian J Med Microbiol 2014;32:39-43.  Back to cited text no. 12
[PUBMED]  [Full text]  
13.
Renushri BV, Saha A, Nagaraj ER, Krishnamurthy V. Inducible clindamycin resistance in Staphylococcus aureus isolated from nursing and pharmacy students. J Lab Physicians 2011;3:89-92.  Back to cited text no. 13
    
14.
Bode LG, Kluytmans JA, Wertheim HF, Bogaers D, Vandenbroucke-Grauls CM, Roosendaal R, et al. Preventing surgical-site infections in nasal carriers of Staphylococcus aureus. N Engl J Med 2010;362:9-17.  Back to cited text no. 14
    
15.
Singh Amit K, Vimala V, Mastan S. Mupirocin resistance in clinical isolates of Staphylococcus aureus; in a Tertiary care hospital set up in North India. Int J Med Res Health Sci 2013;2:840-7.  Back to cited text no. 15
    


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    Tables

  [Table 1], [Table 2]



 

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