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 Table of Contents  
ORIGINAL ARTICLE
Year : 2018  |  Volume : 11  |  Issue : 3  |  Page : 279-282

A community-based study on nasal carriage of Staphylococcus aureus among healthy schoolchildren and its antimicrobial susceptibility pattern


Department of Microbiology, JNMC, KLE University, Belagavi, Karnataka, India

Date of Web Publication25-Sep-2018

Correspondence Address:
Dr. Sumati A Hogade
Department of Microbiology, JNMC, KLE University, Belagavi, Karnataka
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/kleuhsj.kleuhsj_298_17

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  Abstract 


BACKGROUND: Invasive infections from Staphylococcus aureus are increasingly being encountered in healthy children. Nasal colonization of S. aureus is associated with increased risk for acquiring invasive disease. The objective of this study was to determine the prevalence and risk factors for S. aureus nasal colonization among a healthy pediatric population and to determine antibiotic susceptibilities of the S. aureus isolates.
MATERIALS AND METHODS: Using a cross-sectional study design, a total of 468 children of age group 5–16 years from 15 different schools of urban Belgaum (Belagavi) located under Ramnagar Urban Health Centre of KLE University's Jawaharlal Nehru Medical College, India, were screened for S. aureus colonization. Information on selected risk factors for nasal colonization of S. aureus was obtained through a questionnaire. Samples were obtained from the anterior nares and processed. S. aureus isolates were confirmed by growth on selective media and coagulase testing. Disc diffusion antibiotic susceptibility tests were performed according to the Clinical and Laboratory Standard Institute guidelines.
RESULTS: Of the 468 children included in the study, S. aureus was isolated from the anterior nares in 142 (30.3%) children. S. aureus isolates exhibited resistance to multiple classes of antibiotics including co-trimoxazole resistance (19.7%), ciprofloxacin (47.9%), erythromycin resistance (33.1%), clindamycin resistance (4.9%), amoxiclav (1.4%), and linezolid (4.9%).
CONCLUSION: Children in India have a high rate of nasal colonization of S. aureus. The high rate of resistance to many classes of antibiotics among S. aureus strains is of great concern warranting continued surveillance and antimicrobial stewardship.

Keywords: Children, disc diffusion test, nasal carriage


How to cite this article:
Ranjeeta, Hogade SA. A community-based study on nasal carriage of Staphylococcus aureus among healthy schoolchildren and its antimicrobial susceptibility pattern. Indian J Health Sci Biomed Res 2018;11:279-82

How to cite this URL:
Ranjeeta, Hogade SA. A community-based study on nasal carriage of Staphylococcus aureus among healthy schoolchildren and its antimicrobial susceptibility pattern. Indian J Health Sci Biomed Res [serial online] 2018 [cited 2018 Dec 15];11:279-82. Available from: http://www.ijournalhs.org/text.asp?2018/11/3/279/242042




  Introduction Top


Staphylococcus aureus (S. aureus) is one of the most prevalent and clinically significant pathogens which causes wide variety of infections, ranging from mild skin and soft-tissue infections to life-threatening infections.[1]

S. aureus readily colonizes the anterior nares as a commensal microflora. Nasal colonization of S. aureus act as an endogenous reservoir for clinical infections in the colonized individuals as well as a source of cross-colonization for others in the community.[1] Nasal colonization by S. aureus has been considered an important risk factor for infections that could threaten its carrier's life.[1]

Due to the indiscriminate use of antibiotics, there is an increase in emergence of strains, which are resistant to the most commonly used antibiotics.[2] With a human population of over 1 billion and growing, the microbial milieu within India should be closely monitored, especially with recent reports of the global spread of antimicrobial resistance.[3] Few studies from India have reported the prevalence of nasal carriage of S. aureus among the healthy preschool children. However, since the prevalence of S. aureus colonization and its antimicrobial susceptibility pattern differs dramatically in different geographical areas, this study was carried out to estimate the same from this part of India.


  Materials and Methods Top


The study was carried out for the period of 1 year from January 2016 to December 2016.

A total of 468 children of age group 5–16 years from 15 different schools of urban Belgaum (Belagavi) located under Ramnagar Urban Health Centre of KLE University's Jawaharlal Nehru Medical College (JNMC) were enrolled for the study. Children suffering from skin and soft-tissue infections, consuming or have recently consumed antibiotics for any indications, and having a history of hospitalization within the last 12 months were excluded from the study.

After obtaining informed consent, a questionnaire was administered in the local languages (Kannada, Marathi, and Hindi as applicable) to the guardian of each participant to collect demographic data and obtain information on selected risk factors of nasal colonization with S. aureus. Samples were obtained from the anterior nares of each child participant using a sterile Culturette swab, premoistened with sterile normal saline. The swab was inserted into each nostril, rotated for 5 s, and placed immediately into the Culturette tube containing transport media. The sample was plated on mannitol salt agar (MSA) and 5% sheep blood agar (SBA) simultaneously and incubated at 37°C for 24 h. Mannitol-fermenting colonies appeared yellow on MSA. The characteristic small, golden-yellow, opaque β-hemolytic colonies on SBA signified the presence of S. aureus. The isolates were confirmed as S. aureus based on colony morphology, Gram staining, catalase test, and tube coagulase test.

Antimicrobial susceptibility testing

A single colony was chosen from each coagulase-positive S. aureus isolate and streaked onto a Mueller-Hinton agar plate for susceptibility testing. Kirby–Bauer disc diffusion test on Mueller-Hinton medium was used to determine antimicrobial susceptibility against penicillin G, Amoxiclav, clindamycin, erythromycin, ciprofloxacin, and trimethoprim-sulfamethoxazole or co-trimoxazole. The plates were incubated for 24 h at 37°C and zone diameters were measured, recorded, and classified as sensitive, intermediate, or resistant according to the Clinical and Laboratory Standard Institute (CLSI) interpretation table.[4] Quality control organism S. aureus ATTC 25923 was used according to standard procedures recommended by the CLSI.

Ethical Issues

The study was approved by the Institutional Ethics Committee at JNMC, Belagavi. Written informed consent was obtained from the parents of each participant.

Statistical analysis

Questionnaire data were recorded on the questionnaire forms and entered into a Microsoft Excel spreadsheet. Laboratory results were entered into the spreadsheet along with the corresponding participant's information as they become available. The Statistical software, namely, R 3.4.2 and R-studio were used for the analysis of the data and Microsoft Excel 2010 was used to generate graphs, tables, etc. Descriptive statistics (including means, standard deviations, frequencies, and percentage) were calculated for the sociodemographic variables. Chi-square test has been used to find the significance of study parameters on categorical scale between two or more groups. t-test was used to find significance for quantitative data across two groups.


  Results Top


Of the 468 students selected in age group of 5–16 years studying in the schools of urban Belagavi, majority of the students were aged 12, 13, or 14 years. Highest number of students was aged 13 years, i.e., 14.3% of total). The highest number of participants (41.2%) belonged to 9–12 years age group. Female students (246, 52.6%) were a little more as compared to male students (222, 47.4%).

Of the total 468 children, 142 children were found to be colonized with S. aureus. Hence, the prevalence of the nasal carriage of S. aureus among healthy schoolchildren of urban Belagavi was found to be 30.3% by this study. Among these 142 children, 84 (34.1%) were girls and 58 (26.1%) were boys as depicted in [Table 1].
Table 1: Prevalence of nasal carriage of Staphylococcus aureus (n=468)

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Next, the antibiotic sensitivity pattern of the S. aureus isolates was explored. As evident in [Table 2], majority of the isolates (97.9%) were resistant to penicillin.
Table 2: Antibiotic sensitivity pattern of S. aureus isolated in the study samples (n=142)

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In our study, the S. aureus isolates exhibited resistance to multiple classes of antibiotics including co-trimoxazole (19.7%), ciprofloxacin (47.9%), erythromycin (33.1%), clindamycin (4.9%), amoxiclav (1.4%), and linezolid (4.9%).


  Discussion Top


The present study from South India was conducted among healthy schoolchildren of age 5–16 years in a community setting. A total of 468 children were enrolled to determine the prevalence of nasal carriage of S. aureus.

Our study reports that 30.3% (142/468) of healthy schoolchildren in this geographical area were colonized with S. aureus in their anterior nares asymptomatically. This finding is consistent with reports of various other similar studies conducted in India and worldwide. The prevalence and incidence of S. aureus nasal carriage vary according to the population studied. The results of studies on the nasal carriage as determined in cross-sectional surveys are shown in [Table 3].
Table 3: Comparison of prevalence of nasal carriage of Staphylococcus aureus of the present study with other similar studies conducted in India

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Studies from Taiwan and the US have documented the prevalence of nasal carriage of S. aureus among children ranging from 16% to 23%, respectively.[8],[9] In contrast, Chatterjee et al., studied 489 schoolchildren aged 5–15 years by polymerase chain reaction and found nasal colonization of S. aureus in 256 (52.5%) of children, which is much higher compared to our study and other similar studies.[10] The comparatively higher prevalence rate may be attributed to the characteristics of the study population, although other factors (e.g., sampling and culture techniques) may have played a contributory role.

Since there is regional variation in the colonization of S. aureus, the overall prevalence of S. aureus colonization among healthy population has been estimated ranging from 20% to 40% worldwide. The prevalence of colonization with S. aureus has previously been shown to be age dependent.[11],[12],[13] In our study, the prevalence varied across different age groups. It was lowest among the 5–8 years age group as compared to 9–12 years and 13–16 years age group. However, the difference was not found to be statistically significant (P > 0.05).

In the present study, other sociodemographic factors such as gender, type of house, and family size were also studied for its association with the carriage of S. aureus. None of these were found to be statistically significantly (P > 0.05) associated with nasal colonization. Statistically significant risk factors for colonization included age below 6 years and membership to joint families similar to some other studies.[5] School-going children were shown to have significantly higher prevalence of carriage. The finding is consistent with the fact that large family size with 10 or more members had higher carriage prevalence as compared to families with ≤4 members.[5] This might be due to poor hygiene and overcrowding.

In our study, the S. aureus isolates exhibited resistance to multiple classes of antibiotics including Cotrimoxazole (19.7%), ciprofloxacin (47.9%), erythromycin (33.1%), clindamycin (4.9%), amoxiclav (1.4%), and linezolid (4.9%). Other studies have also found similar results.[14],[15] In a recent study from Ujjain, S. aureus isolates were found to be resistant to many classes of antibiotics including ampicillin (90%), amoxiclav (54%), co-trimoxazole (49%), ciprofloxacin (23%), and erythromycin (11%).[16] A study from Portugal found that among the 36 S. aureus, only 11.5% of isolates were susceptible to all antibiotics tested; a higher nonsusceptibility rate (88.5%) to penicillin was detected, which is similar to our finding of penicillin resistance (97.9%).[17] This may be because penicillin is one of the most commonly prescribed drugs.

Resistance to clindamycin and co-trimoxazole in our setting is a concern since these antibiotics are routinely used to treat common infections due to S. aureus in the outpatient setting and often prescribed to hospitalized patients on discharge to complete a course of outpatient therapy. Judicious antimicrobial use should be implemented by the physicians in this setting given the increasing prevalence of drug-resistant microbes.


  Conclusion Top


Children in this studied area of South India have a high rate of colonization with S. aureus. This study has demonstrated the baseline colonization rate and continued surveillance of this population is necessary to assess the ongoing risk posed by S. aureus to this community. The high rate of antibiotic resistance to frequently used antibiotics such as ciprofloxacin and erythromycin is a major concern warranting continued surveillance and antimicrobial stewardship programs to promote judicious use of antimicrobials in the hospital and ambulatory settings.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
  References Top

1.
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. 1
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2.
Bharathi M, Lakshmi N, Kalyani CS, Padmaja IJ. Nasal carriage of multidrug-resistant MSSA and MRSA in children of municipality schools. Indian J Med Microbiol 2014;32:200.  Back to cited text no. 2
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3.
Kumarasamy KK, Toleman MA, Walsh TR, Bagaria J, Butt F, Balakrishnan R, et al. Emergence of a new antibiotic resistance mechanism in India, Pakistan, and the UK: A molecular, biological, and epidemiological study. Lancet Infect Dis 2010;10:597-602.  Back to cited text no. 3
    
4.
Performance Standards for Antimicrobial Susceptibility Testing M100S27. Avaible from: https://www.clsi.org/standards/products/microbiology/documents/m100/. [Last accessed on 2017 Oct 27].  Back to cited text no. 4
    
5.
Shetty V, Trumbull K, Hegde A, Shenoy V, Prabhu R, Sumathi K, et al. Prevalence of community-acquired methicillin-resistant Staphylococcus aureus nasal colonization among children. J Clin Diagn Res 2014;8:DC12-5.  Back to cited text no. 5
    
6.
Govindan S, Maroli AS, Ciraj AM, Bairy I. Molecular epidemiology of methicillin resistant Staphylococcus aureus colonizing the anterior nares of school children of Udupi Taluk. Indian J Med Microbiol 2015;33(5):129-33.  Back to cited text no. 6
    
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Dey S, Rosales-Klintz S, Shouche S, Pathak JP, Pathak A. Prevalence and risk factors for nasal carriage of Staphylococcus aureus in children attending anganwaries (preschools) in Ujjain, India. BMC Res Notes 2013;6:265.  Back to cited text no. 7
    
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Lo WT, Lin WJ, Tseng MH, Lu JJ, Lee SY, Chu ML, et al. Nasal carriage of a single clone of community-acquired methicillin-resistant Staphylococcus aureus among kindergarten attendees in Northern Taiwan. BMC Infect Dis 2007;7:51.  Back to cited text no. 8
    
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Mainous AG 3rd, Hueston WJ, Everett CJ, Diaz VA. Nasal carriage of Staphylococcus aureus and methicillin-resistant S aureus in the United States, 2001-2002. Ann Fam Med 2006;4:132-7.  Back to cited text no. 9
    
10.
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. 10
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Kluytmans J, van Belkum A, Verbrugh H. Nasal carriage of Staphylococcus aureus: Epidemiology, underlying mechanisms, and associated risks. Clin Microbiol Rev 1997;10:505-20.  Back to cited text no. 11
    
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Fritz SA, Garbutt J, Elward A, Shannon W, Storch GA. Prevalence of and risk factors for community-acquired methicillin-resistant and methicillin-sensitive Staphylococcus aureus colonization in children seen in a practice-based research network. Pediatrics 2008;121:1090-8.  Back to cited text no. 12
    
13.
Peacock SJ, Justice A, Griffiths D, de Silva GD, Kantzanou MN, Crook D, et al. Determinants of acquisition and carriage of Staphylococcus aureus in infancy. J Clin Microbiol 2003;41:5718-25.  Back to cited text no. 13
    
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Lee GM, Huang SS, Rifas-Shiman SL, Hinrichsen VL, Pelton SI, Kleinman K, et al. Epidemiology and risk factors for Staphylococcus aureus colonization in children in the post-PCV7 era. BMC Infect Dis 2009;9:110.  Back to cited text no. 14
    
15.
Tavares DA, Sá-Leão R, Miragaia M, de Lencastre H. Large screening of CA-MRSA among Staphylococcus aureus colonizing healthy young children living in two areas (urban and rural) of Portugal. BMC Infect Dis 2010;10:110.  Back to cited text no. 15
    
16.
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. 16
    
17.
Lamaro-Cardoso J, de Lencastre H, Kipnis A, Pimenta FC, Oliveira LS, Oliveira RM, et al. Molecular epidemiology and risk factors for nasal carriage of Staphylococcus aureus and methicillin-resistant S. aureus in infants attending day care centers in Brazil. J Clin Microbiol 2009;47:3991-7.  Back to cited text no. 17
    



 
 
    Tables

  [Table 1], [Table 2], [Table 3]



 

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