Skip to main content
Log in

Prevalence of multidrug-resistant, coagulase-positive Staphylococcus aureus in nasal carriage, food, wastewater and paper currency in Jalandhar city (north-western), an Indian state of Punjab

  • Published:
Environmental Monitoring and Assessment Aims and scope Submit manuscript

Abstract

Development of multidrug-resistant pattern in the bacterial community is a major threat to the society. Staphylococcus aureus is perhaps the pathogen of the greatest concern because of its inherent virulence, its ability to cause a diverse array of life-threatening situations and capacity to adapt to different environmental conditions. The aims of this study is to investigate the multidrug-resistant pattern of the coagulase-positive S. aureus isolated from nasal carriage, food, paper currency and wastewater samples. We had also studied the multiple antibiotic resistance index and in vitro production of β-lactamase. The study had found out 130 coagulase-positive S. aureus strains isolated from total of 595 samples such as anterior nares of preschool children (195), hospital nurses (100), drivers (76), food (86), wastewater (3) and paper currency (135) (Indian rupee). The biotypes pattern were as follows; A > D > B > C> UT. Multiple antibiotic resistance (MAR) value clearly defines the multidrug-resistant pattern of the S. aureus among different sources. Statistical analysis (one-way ANOVA) of results obtained indicated that the difference in the antibiotic resistance observed in the 130 bacterial isolates against the 23 different antibiotics used in this study was statically significant (p < 0.01).

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Abd, A. A.-H. (2010). Prevalence of microflora in Lamb meat and Offal at Baghdad abattoir. Basrah Journal of Veterinary Research, 9, 28–34.

    Google Scholar 

  • Abulreesh, H. H. (2011). Multidrug-resistant staphylococci in the environment. International Conference on Biotechnology and Environment Management, 18, 1–6.

    Google Scholar 

  • Abulreesh, H. H., & Organji, S. R. (2011). The prevalence of multidrug-resistant staphylococci in food and environment of Makkah, Saudi Arabia. Research Journal of Microbiology, 6(6):510–523. doi:10.3923/jm.2011.510.523

  • Adegoke, A. A., & Okoh, A. I. (2011). The in vitro effect of vancomycin on multidrug resistant Staphylococcus aureus from hospital currency notes. African Journal of Microbiology Research, 5(14), 1881–1887.

    CAS  Google Scholar 

  • Ahmed, U. S. M., Parveen, S., Nasreen, T., & Feroza, B. (2010). Evaluation of the microbial contamination of Bangladesh paper currency notes (Taka) in circulation. Advances in Biological Research, 4(5), 266–271.

    Google Scholar 

  • Al-Sheddy, I. A., Fung, D. Y., & Kastner, C. L. (1995). Microbiology of fresh and restructured lab meat: a review. Critical Reviews in Microbiology, 21(1), 31–52.

    Article  Google Scholar 

  • Artan, O. M., Baykam, Z., & Artan, C. (2008). Nasal carriage of Staphylococcus aureus in healthy preschool children. Japanese Journal of Infectious Diseases, 61, 70–72.

    Google Scholar 

  • Bauer, A. W., Kirby, W. M. M., Sherris, J. C., & Turck, M. (1966). Antibiotics susceptibility testing by a standardized single disk method. American Journal of Clinical Pathology, 45(4), 493–496.

    CAS  Google Scholar 

  • Borjesson, S., Matussek, A., Melin, S., Lofgren, S., & Lindgren, P. E. (2010). Methicillin-resistant Staphylococcus aureus (MRSA) in municipal wastewater: an uncharted threat? Applied Microbiology, 108, 1244–1251.

    Article  CAS  Google Scholar 

  • Chatterjee, S. S., Ray, P., Aggarwal, A., Das, A., & Sharma, M. (2009). A community-based study on nasal carriage of Staphylococcus aureus. Indian Journal of Medical Research, 130(12), 742–748.

    CAS  Google Scholar 

  • Chitnis, V., Chitnis, D., Patil, S., & Kant, R. (2000). Hospital effluent: a source of multiple drug-resistant bacteria. Current Science, 79(7), 989–991.

    Google Scholar 

  • CLSI. (2011). Performance standards for antimicrobial susceptibility testing; 21st Information Supplement. Pa: Wayne.

    Google Scholar 

  • Coia, J. E., Carter, F. T., Baird, D., & Platt, D. J. (1990). Characterisation of methicillin-resistant Staphylococcus aureus by biotyping, immunoblotting and restriction enzyme fragmentation patterns. Medical Microbiology, 31, 125–132.

    Article  CAS  Google Scholar 

  • CPCB (2011). Guide manual: water and wastewater analysis. Online at <http://www.cpcb.nic.in/upload/NewItems/NewItem_171_guidemanualw%26wwanalysis.pdf>. Accessed 19 December 2011.

  • Cunha, M. L. R. S., Sinzato, Y. K., & Silveira, L. V. A. (2004). Comparison of methods for the identification of coagulase-negative staphylococci. Memórias do Instituto Oswaldo Cruz, 99, 855–860.

    Article  Google Scholar 

  • Datta, S., Akter, A., Shah, I. G., Fatema, K., Islam, T. H., Bandyopadhyay, B., Khan, Z. U. M., & Biswas, D. (2012). Microbiological quality assessment of raw meat and meat products, and antibiotic susceptibility of isolated Staphylococcus aureus. Agriculture, Food and Analytical Bacteriology, 2(3), 187–194.

    Google Scholar 

  • Dubey, D., Rath, S., Sahu, M. C., Pattnaik, L., Debata, N. K., & Padhy, R. N. (2013). Surveillance of infection status of drug resistant Staphylococcus aureus in an Indian teaching hospital. Asian Pacific Journal of Tropical Disease, 3(2), 133–142.

    Article  Google Scholar 

  • Elmund, G. K., Morrison, S. M., Grant, D. W., & Nevins, M. P. (1971). Role of excreted chlortetracycline in modifying the decomposition process in feedlot waste. Bulletin of Environmental Contamination and Toxicology, 6, 129–135.

    Article  CAS  Google Scholar 

  • Elumalai, E. K., David, E., & Hemachandran, J. (2012). Bacterial contamination of Indian currency notes (Rupee). International Journal of Occupational and Environmental Medicine, 3(4), 204–205.

    CAS  Google Scholar 

  • Eze, V. C., & Ivuoma, N. (2012). Evaluation of microbiological quality of fresh goat meat sold in Umuahi market, Abia State, Nigeria. Pakistan Journal of Nutrition, 11(9), 782–786.

    Article  Google Scholar 

  • Feinman, S. E., & Matheson, J. C. (1978). Draft environmental impact statement: Subtherapeutic antibacterial agents in animal feeds. Food and drug administration department of health, education and welfare report. Food and drug administration, p. 372, Washington.

  • Ghamdi, A. A., Abdelmalek, S. M. A., Azhar, E. I., Wakidi, M. H., & Alsaied, Z. (2011). Bacterial contamination of Saudi “one” riyal paper notes. Southeast Asian Journal of Tropical Medicine and Public Health, 42(3), 711–716.

    Google Scholar 

  • Goktas, P., & Oktay, G. (1992). Bacteriological examination of the currency notes. Microbiology Bulletin, 26, 344–348.

    CAS  Google Scholar 

  • Goud, R., Gupta, S., Neogi, U., Agarwal, D., Naidu, K., Chalannavar, R., & Subhaschandra, G. (2011). Community prevalence of methicillin and vancomycin resistant Staphylococcus aureus in and around Bangalore, southern India. Revista da Sociedade Brasileira de Medicina Tropical, 44(3), 309–312.

    Article  Google Scholar 

  • Greeson, K., Suliman, G. M., Sami, A., Alowaimer, A., & Koohmaraie, M. (2013). Frequency of antibiotic resistant Salmonella, Escherichia coli, Enterococcus, and Staphylococcus aureus in meat in Saudi Arabia. African Journal of Microbiology Research, 7(4), 309–316.

    CAS  Google Scholar 

  • Gundogan, N., Citak, S., Yucel, N., & Devren, A. (2005). A note on the incidence and antibiotic resistance of Staphylococcus aureus isolated from meat and chicken samples. Meat Science, 69(4), 807–810.

    Article  CAS  Google Scholar 

  • Jay, J. (1986). Staphylococcal gastroenteritis. In Modern food microbiology (3rd ed., pp. 437–458). New York: Van Nostrand Reinhold.

    Google Scholar 

  • Jevons, M. P. (1961). “Celbenin”-resistant staphylococci. British Medical Journal, 1, 124–125.

    Article  Google Scholar 

  • Joshi, D. R., Shrestha, S. N., Bomjan, R., & Poudel, K. (2008). Nasal carriage of Staphylococcus aureus among health school children in Kathmandu valley. Nepal Journal of Science and Technology, 9, 139–142.

    Google Scholar 

  • Kakhandki, L. S., & Peerapur, B. V. (2012). Study of nasal carriage of MRSA among the clinical staff and health care workers of a teaching hospital of Karnataka, India. Al Ameen Journal of Medical Sciences, 5(4), 367–370.

    Google Scholar 

  • Kirby, W. M. M. (1944). Extraction of high potent Penicillin inactivator from Penicillin resistant staphylococci. Clinical Investigation, 24(2), 170–174.

    Article  Google Scholar 

  • Kloos, W. E., & Schleifer, K. H. (1975). Simplified scheme for routine identification of human staphylococcus species. Clinical Microbiology, 1(1), 82–88.

    CAS  Google Scholar 

  • Kluytmans, W. J. A. J. (2010). Methicillin-resistant Staphylococcus aureus in food products: cause for concern or case for complacency? Clinical Microbiology and Infection, 16, 11–15.

    Article  CAS  Google Scholar 

  • Krumperman, P. H. (1983). Multiple antibiotic resistance indexing of Escherichia coli to identify high-risk sources of fecal contamination of foods. Applied and Environmental Microbiology, 46(1), 165–170.

    CAS  Google Scholar 

  • Kumar, R., & Prasad, A. (2010). Detection of E. coli and Staphylococcus in milk and milk products in and around Pantnagar. Veterinary World, 3(11), 495–496.

    Google Scholar 

  • Kummerer, K. (2004). Resistance in the environment. Antimicrobial Chemotherapy, 54, 311–320.

    Article  CAS  Google Scholar 

  • Lamichhane, J., Adhikary, S., Gautam, P., Maharjan, R., & Dhakal, B. (2009). Risk of handling paper currency in circulation chances of potential bacterial transmittance. Nepal Journal of Science and Technology, 10, 161–166.

    Google Scholar 

  • Lamprell, H., Villard, L., Chamba, J. F., Beuvier, E., Borges, E., Maurin, F., Mazerolles, G., Noel, Y., & Kodjo, A. (2004). Identification and biotyping of coagulase positive staphylococci (CPS) in ripened French raw milk cheeses and their in vitro ability to produce enterotoxin. Revue de Médecine Vétérinaire, 155(2), 92–96.

    CAS  Google Scholar 

  • Lowy, F. D. (1998). Staphylococcus aureus infections. New England Journal of Medicine, 339, 520–532.

    Article  CAS  Google Scholar 

  • Mims, C., Dockrell, H. M., Goering, H. V., Roitt, I., Wakelin, D., & Zuckerman, M. (2006). A text book of medical microbiology (3rd ed., p. 585). U. K: Mosby press.

    Google Scholar 

  • Morandi, S., Brasca, M., Lodi, R., Cremonesi, P., & Castiglioni, B. (2007). Detection of classical enterotoxin genes in Staphylococcus aureus from milk and dairy products. Veterinary Microbiology, 124, 66–72.

    Article  CAS  Google Scholar 

  • Nazir, K. H. M. N. H., & Islam, T. (2007). Association of bacteria in stored bakery foods of retailers shops in Mymensingh, Bangladesh. Bangladesh Society of Agriculture Science and Technology, 4(1&2), 21–24.

    Google Scholar 

  • Neel, R. (2013). Multidrug resistance of isolates of methicillin resistant Staphylococcus aureus (MRSA) in paper currency notes from restaurants and hotels in Lusaka in Zambia. International Journal of Pharmacy and Pharmaceutical Sciences, 5(1), 363–366.

    Google Scholar 

  • Normanno, G., La Salandra, G., Dambrosio, A., Quaglia, N. C., Corrente, M., Parisi, A., Santagad, G., Firinu, A., Crisetti, E., & Celano, G. V. (2007). Occurrence, characterization and antimicrobial resistance of enterotoxigenic Staphylococcus aureus isolated from meat and dairy products. International Journal of Food Microbiology, 115, 290–296.

    Article  CAS  Google Scholar 

  • Oyero, O. G., & Emikpe, B. O. (2007). Preliminary investigation on the microbial contamination of Nigerian currency. International Journal of Tropical Medicine, 2(2), 29–32.

    Google Scholar 

  • Pathak, A., Marothi, Y., Iyer, R. V., Singh, B., Sharma, M., Eriksson, B., Macaden, R., & Lundborg, C. S. (2010). Nasal carriage and antimicrobial susceptibility of Staphylococcus aureus in healthy preschool children in Ujjain, India. BMC Pediatrics, 10, 1–8.

    Article  Google Scholar 

  • Peles, F., Wagner, M., Varga, L., Hein, I., Rieck, P., Gutser, K., Keresturi, P., Kardos, G., Turcsanyi, I., Beri, B., & Szabo, A. (2007). Characterization of Staphylococcus aureus strains isolated from bovine milk in Hungry. International Journal of Food Microbiology, 118, 186–193.

    Article  CAS  Google Scholar 

  • Rachel, E., Golstein, R., Micallef, S. A., Gibbs, S. G., Davis, J. A., He, X., George, A., Kleinfelter, L. M., Schreiber, N. A., Mukherjee, S., Sapkota, A., & Joseph, S. W. (2012). Methicillin-resistant Staphylococcus aureus (MRSA) detected at four U.S. wastewater treatment plants. Environmental Health Perspectives, 120(11), 1551–1558.

    Article  Google Scholar 

  • Rashid, Z., Farzana, K., Sattar, A., & Murtaza, G. (2012). Prevalence of nasal Staphylococcus aureus and methicillin-resistant Staphylococcus aureus in hospital personal and associated risk factors. Acta Poloniae Pharmacutica -Drug Research, 69(5), 985–991.

    Google Scholar 

  • Robert, G. W., & Edmund, F. W. (1970). Activity of penicillinase in Staphylococcus aureus as studied by the iodometric method. Infectious Diseases, 121(4), 433–437.

    Article  Google Scholar 

  • Rongpharpi, S. R., Hazarika, N. K., & Kalita, H. (2013). The prevalence of nasal carriage of Staphylococcus aureus among healthcare workers at tertiary care hospital in Assam with special reference to MRSA. Clinical and Diagnostic Research, 7(2), 257–260.

    Google Scholar 

  • Sawalha, H., & Mowais, M. A. (2012). Bacterial contamination of paper banknotes in circulation; a case study in the Jenin district, Palestine. Science, 1(2), 36–39.

    Google Scholar 

  • Scherrer, D., Corti, S., Muehlherr, J. E., Zweifel, C., & Stephan, R. (2004). Phenotypic and genotypic characteristics of Staphylococcus aureus isolates from raw bulk-tank milk samples of goats and sheep. Veterinary Microbiology, 101, 101–107.

    Article  CAS  Google Scholar 

  • Schwartz, T., Kohnen, W., Jansen, B., & Obst, U. (2003). Detection of antibiotic-resistant bacteria and their resistance genes in wastewater, surface water and drinking water biofilms. FEMS Microbiology Ecology, 43, 325–335.

    Article  CAS  Google Scholar 

  • Selvan, P., Narendra Babu, R., Sureshkumar, S., & Venkataramanujam, V. (2007). Microbial quality of retail meat products available in Chennai city. American Journal of Food Technology, 2(1), 55–59.

    Article  Google Scholar 

  • Shanth, J., Saravanan, T., & Balagurunathan, R. (2012). Isolates of tannery effluent and their antibiogram from effluent plant in south India. Chemical and Pharmaceutical Research, 4(4), 1974–1977.

    Google Scholar 

  • Sharma, A., & Dhanashree, B. (2011). Screening of currency in circulation for bacterial contamination. Current Science, 100(6), 822–825.

    Google Scholar 

  • Singh, P., & Prakash, A. (2008). Isolation of Escherichia coli, Staphylococcus aureus and Listeria monocytogenes from milk products sold under market conditions at Agra region. Acta Agriculturae Slovenica, 92(11), 83–88.

    CAS  Google Scholar 

  • Singh, D. V., Thakur, K., Kalpna, & Goel, A. (2002). Microbiological surveillance of currency. Indian Journal of Medical Microbiology, 20(1), 53.

    CAS  Google Scholar 

  • The Tribune (2013a). 45 Hospitals get notice for violating norms. Online at <http://www.tribuneindia.com/2013/20130309/punjab.htm#3>. Accessed 8 March 2013.

  • The Tribune (2013b). Punjab Pollution Control Board team raids PIMS, SGL hospitals finds irregularities in biomedical waste disposal system in both institutes. Online at <http://www.tribuneindia.com/2013/20130104/jaltrib.htm>. Accessed 3 January 2013.

  • The Tribune (2010). Punjab Pollution Control Board directed against erring hospitals. Online at http://www.tribuneindia.com/2010/20101119/punjab.htm#1. Accessed 18 November 2010.

  • The Tribune (2011). Punjab Pollution Control Board orders closures of 3 erring hospitals were found violating biomedical waste disposal norms; several others left off with warning. Online at <http://www.tribuneindia.com/2011/20110717/punjab.htm#1>. Accessed 16 July 2011.

  • Vaishnavi, C., Singh, S., Grover, R., & Singh, K. (2001). Bacteriological study of Indian cheese (paneer) sold in Chandigarh. Indian Journal of Medical Microbiology, 19(4), 224–226.

    CAS  Google Scholar 

  • Vinodhkumaradithyaa, A., Uma, A., Srinivasan, M., Ananthalakshmi, I., Nallasivam, P., & Thirumalaikolundusubramanian, P. (2009). Nasal carriage of methicillin-resistant Staphylococcus aureus among surgical unit staff. Japanese Journal of Infectious Diseases, 62, 228–229.

    CAS  Google Scholar 

  • Waldvogel, F. A. (2000). Staphylococcus aureus (Including staphylococcal toxic shock). In G. L. Mandell, J. E. Bennet, & R. Dolin (Eds.), Principles and practice of infectious diseases (pp. 2069–2092). Philadelphia: Churchill Livingstone.

    Google Scholar 

  • Wertheirn, H. F. L., Melles, D. C., Vos, M. C., Leeuwen, W. V., Belkum, A. V., Verbrugh, H. A., & Nouwen, J. L. (2005). The role of nasal carriage in Staphylococcus aureus infections. The Lancet Infectious Diseases, 5, 751–762.

    Article  Google Scholar 

  • Williams, R. E. O. (1963). Healthy carriage of Staphylococcus aureus: its prevalence and importance. Bacteriological Reviews, 27, 56–71.

    CAS  Google Scholar 

  • Yu-Cheng, C. H., Wan-Wen, L., Chin-Ming, F., Wan-Yu, P., Chien-Shun, C. H., & Hau-Yang, T. (2008). PCR detection of Staphylococcal enterotoxins (SEs) N, O, P, Q, R, U, and survey of SE types in Staphylococcus aureus isolates from food-poisoning cases in Taiwan. International Journal of Food Microbiology, 121, 66–73.

    Article  Google Scholar 

Download references

Acknowledgments

We are thankful to the Super Religare Laboratories, Beas, for providing reference strain of S. aureus ATCC-25923 for this study.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Harsh Kumar.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Table I

(DOC 74 kb)

Table II

(DOC 69 kb)

Table III

(DOC 36 kb)

Table IV

(DOC 41 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kumar, H., Palaha, R., Kaur, N. et al. Prevalence of multidrug-resistant, coagulase-positive Staphylococcus aureus in nasal carriage, food, wastewater and paper currency in Jalandhar city (north-western), an Indian state of Punjab. Environ Monit Assess 187, 4134 (2015). https://doi.org/10.1007/s10661-014-4134-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s10661-014-4134-6

Keywords

Navigation