Hostname: page-component-586b7cd67f-g8jcs Total loading time: 0 Render date: 2024-11-30T20:11:43.709Z Has data issue: false hasContentIssue false

Staphylococcus aureus Nasal Carriage in a Student Community Prevalence, Clonal Relationships, and Risk Factors

Published online by Cambridge University Press:  02 January 2015

Werner E. Bischoff*
Affiliation:
Department of Internal Medicine, Section on Infectious Diseases, Winston-Salem, North Carolina
Michelle L. Wallis
Affiliation:
Department of Internal Medicine, Section on Infectious Diseases, Winston-Salem, North Carolina
Keith B. Tucker
Affiliation:
Department of Internal Medicine, Section on Infectious Diseases, Winston-Salem, North Carolina
Beth A. Reboussin
Affiliation:
Section on Biostatistics, Wake Forest University School of Medicine, Winston-Salem, North Carolina
Robert J. Sherertz
Affiliation:
Department of Internal Medicine, Section on Infectious Diseases, Winston-Salem, North Carolina
*
Wake Forest University School of Medicine, Department of Internal Medicine, Section on Infectious Diseases, Medical Center Boulevard, Winston-Salem, NC 27157-1042

Abstract

Objective:

To evaluate the prevalence and risk factors of nasal Staphylococcus aureus (SA) in the community.

Design:

Cross-sectional study.

Setting:

Wake Forest University, Winston-Salem, North Carolina.

Participants:

Four hundred fifty students were screened for nasal SA carriage during the fall of 2000, 2001, and 2002.

Methods:

Students were screened by nose swabs. A self-administered questionnaire collected information on demographics and medical history. Antibiotic testing and PFGE were performed on isolates. Risk factors were determined by logistic regression analysis.

Results:

Of 450 volunteers, 131 (29%) were SA carriers. Antibiotic resistance was high for azithromycin (26%) and low for ciprofloxacin (1%), tetracycline (5%), mupirocin (1%), and methicillin (2%). PFGE patterns were not associated with carriage. Age, male gender, white race, medical student, allergen injection therapy, chronic sinusitis, rheumatoid arthritis, hospitalization for 6 months or less, and use of antibiotics were associated with carrier status by univariate analysis. Stepwise multivariate logistic regression led to a best fitting model with older age (OR, 1.04; CI95, 1.005-1.079), male gender (OR, 1.50; CI95, 0.982-2.296), and chronic sinusitis (OR, 2.71; CI95, 0.897-8.195) as risk factors. Antibiotic use (< 4 weeks) (OR, 0.41; CI95, 0.152-1.095) and allergen injection therapy (OR 0.41; CI95, 0.133-1.238) were protective. Analyses of carriers revealed candidate factors for persistent carriage to be nasal SA colonization rate and male gender. Factors for azithromycin resistance were non-medical students and antibiotic use in the past 6 months.

Conclusion:

Older male volunteers suffering from chronic sinusitis and not taking antibiotics were at higher risk for carrying SA.

Type
Original Articles
Copyright
Copyright © The Society for Healthcare Epidemiology of America 2004

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

1.Gerberding, JL, McGowan, JE Jr, Tenover, FC. Emerging nosocomial infections and antimicrobial resistance. Curr Clin Top Infect Dis 1999;19:8398.Google ScholarPubMed
2.Chambers, HF. The changing epidemiology of Staphylococcus aureus? Emerg Infect Dis 2001;7:178182.Google Scholar
3.National Nosocomial Infections Surveillance (NNIS) System. National Nosocomial Infections Surveillance (NNIS) System report: data summary from January 1992-June 2001, issued August 2001. Am J Infect Control 2001;29:404421.Google Scholar
4.Hartstein, AI, Mulligan, ME. Methicillin-resistant Staphylococcus aureus. In: Mayhall, CG, ed. Hospital Epidemiology and Infection Control. Baltimore: Williams & Wilkins; 1996:290306.Google Scholar
5.John, JF Jr, Barg, NL. Staphylococcus aureus. In: Mayhall, CG, ed. Hospital Epidemiology and Infection Control. Baltimore: Williams & Wilkins; 1996:271290.Google Scholar
6.Austin, TW, Austin, MA, Coleman, B. Methicillin-resistant/methicillin-sensitive Staphylococcus aureus bacteremia. Saudi Med J 2003;24:256260.Google ScholarPubMed
7.Talon, D, Woronoff-Lemsi, MC, Limat, S, et al.The impact of resistance to methicillin in Staphylococcus aureus bacteremia on mortality. European Journal of Internal Medicine 2002;13:3136.Google Scholar
8.Hiramatsu, K. Vancomycin-resistant Staphylococcus aureus: a new model of antibiotic resistance. Lancet Infect Dis 2001;1:147155.CrossRefGoogle ScholarPubMed
9.Tenover, FC, Weigel, LM, Appelbaum, PC, et al.Vancomycin-resistant Staphylococcus aureus isolate from a patient in Pennsylvania. Antimicrob Agents Chemother 2004;48:275280.Google Scholar
10.Stubbs, E, Pegler, M, Vickery, A, Harbour, C. Nasal carriage of Staphylococcus aureus in Australian (pre-clinical and clinical) medical students. J Hosp Infect 1994;27:127134.CrossRefGoogle ScholarPubMed
11.Kingdom, JC, Joyce, SM, Bradley, FL, Jauch, W, Falkiner, FR, Keane, CT. Staphylococcal nasal carriage in medical students with varying clinical exposure. J Hosp Infect 1983;4:7579.CrossRefGoogle ScholarPubMed
12.Dunkelberg, H. On the incidence of Staphylococcus aureus in the throat of medical students. Zentralbl Bakteriol 1976;163:530535.Google ScholarPubMed
13.Kunz, B. Demonstration of nosocomial pathogens in the nasal swabs of medical students. Zentralblatt Hygiene und Umweltmedizin 1993;194:571577.Google Scholar
14.Bryl, M, Lojko, D, Giersz, R, Andrzejewska, E. Carrier status of Staphylococcus aureus among students of different courses. Przegl Epidemiol 1995;49:1721.Google ScholarPubMed
15.National Committee for Clinical Laboratory Standards. Performance Standards for Antimicrobial Susceptibility Testing: Twelfth Informational Supplement. Wayne, PA: National Committee for Clinical Laboratory Standards; 2002:22.Google Scholar
16.Finlay, JE, Millere, LA, Poupard, JA. Interpretive criteria for testing susceptibility of staphylococci to mupirocin. Antimicrob Agents Chemother 1997;41:11371139.Google Scholar
17.Bannerman, TL, Hancock, GA, Tenover, FC, Miller, JM. Pulsed-field gel electrophoresis as a replacement for bacteriophage typing of Staphylococcus aureus. J Clin Microbiol 1995;33:551555.CrossRefGoogle ScholarPubMed
18.Goering, RV, Winters, MA. Rapid method for epidemiological evaluation of gram-positive cocci by field inversion gel electrophoresis. J Clin Microbiol 1992;30:577580.Google Scholar
19.Tenover, FC, Arbeit, R, Goering, RV, et al.Interpreting chromosomal DNA restriction patterns produced by pulsed-field gel electrophoresis: criteria for bacterial strain typing. J Clin Microbiol 1995;33:22332239.Google Scholar
20.Bendel, RB, Afifi, AA. Comparison of stopping rules in forward regression. Journal of the American Statistical Association 1977;72:4653.Google Scholar
21.Gould, JC, McKillop, EJ. The carriage of Staphylococcus pyogenes var. aureus in the human nose. Journal of Hygiene 1954;52:304310.Google Scholar
22.Hallman, FA. Pathogenic staphylococci in the anterior nares: their incidence and differentiation. Proceedings of the Society of Experimental Biology and Medicine 1937;36:789794.CrossRefGoogle Scholar
23.Hu, L, Umeda, A, Kondo, S, Amako, K. Typing of Staphylococcus aureus colonising human nasal carriers by pulsed-field gel electrophoresis. J Med Microbiol 1995;42:127132.CrossRefGoogle ScholarPubMed
24.Wilson, SZ, Martin, RR, Putman, M. In vivo effects of josamycin, erythromycin, and placebo therapy on nasal carriage of Staphylococcus aureus. Antimicrob Agents Chemother 1977;11:407410.Google Scholar
25.Williams, REO. Healthy carriage of Staphylococcus aureus: its prevalence and importance. Bacteriol Rev 1963;27:5671.Google Scholar
26.Noble, WC. Carriage of Staphylococcus aureus in random samples of a normal population. Journal of Hygiene 1967;65:567573.Google Scholar
27.VandenBergh, MFQ, Verbrugh, HA. Carriage of Staphylococcus aureus: epidemiology and clinical relevance. J Lab Clin Med 1999;133:525534.Google Scholar
28.Ayliffe, GAJ, Brightwell, KM, Collins, BJ, Lowbury, EJL, Goonatilake, PCL, Etheridge, RA. Surveys of hospital infection in the Birmingham region: I. Effect of age, sex, length of stay and antibiotic use on nasal carriage of tetracycline-resistant Staphylococcus aureus and on postoperative wound infection. Journal of Hygiene 1977;79:299314.CrossRefGoogle Scholar
29.Lamikanra, A, Paul, BD, Akinwole, OB, Paul, MO. Nasal carriage of Staphylococcus aureus in a population of healthy Nigerian students. J Med Microbiol 1985;19:211216.Google Scholar
30.Riewerts Eriksen, NH, Esperen, F, Thamdrup Rosdahl, V, Jensen, K. Carriage of Staphylococcus aureus among 104 healthy persons during a 19-month period. Epidemiol Infect 1995;115:5160.Google Scholar
31.Kremer, B, Jacobs, JA, Soudijn, ER, Van der Ven, AJAM. Clinical value of bacteriological examinations of nasal and paranasal mucosa in patients with chronic sinusitis. Eur Arch Otorhinolaryngol 2001;258:220225.Google Scholar
32.Boyce, JM, Opal, SM, Potter-Bynoe, G, Medeiros, AA. Spread of methi-cillin-resistant Staphylococcus aureus in a hospital after exposure to a health care worker with chronic sinusitis. Clin Infect Dis 1993;17:496504.Google Scholar
33.Winkler, J, Block, C, Leibovici, L, Faktor, J, Pitlik, SD. Nasal carriage of Staphylococcus aureus: correlation with hormonal status in women. J Infect Dis 1990;162:14001402.CrossRefGoogle ScholarPubMed
34.Bassetti, S, Dunagan, DP, D'Agostino, RB Jr, Sherertz, RJ. Nasal carriage of Staphylococcus aureus among patients receiving allergen-injection immunotherapy: associated factors and quantitative nasal cultures. Infect Control Hosp Epidemiol 2001;22:741745.Google Scholar
35.Kirmani, N, Tuazon, CU, Ailing, D. Carriage rate of Staphylococcus aureus among patients receiving allergy injections. Ann Allergy 1980;45:235237.Google Scholar
36.Shiomori, T, Yoshida, S, Miyamoto, H, Makishima, K. Relationship of nasal carriage of Staphylococcus aureus to pathogenesis of perennial allergic rhinitis. J Allergy Clin Immunol 2000;105:449454.CrossRefGoogle ScholarPubMed
37.White, A. Quantitative studies of nasal carriers of staphylococci among hospitalized patients. J Clin Invest 1961;40:2330.Google Scholar
38.VandenBergh, MFQ, Yzerman, EPF, Van Belkum, A, Boelens, HAM, Sijmons, M, Verbrugh, HA. Follow-up of Staphylococcus aureus nasal carriage after 8 years: redefining the persistent carrier state. J Clin Microbiol 1999;37:31333140.Google Scholar
39.Goslings, WRO, Buechli, K. Nasal carrier rate of antibiotic-resistant staphylococci. Arch Intern Med 1958;102:691715.Google Scholar
40.Jevons, MP. ‘Celbenin’-resistant staphylococci. Br Med J 1961;1:124125.CrossRefGoogle Scholar
41.Panlilio, AL, Culver, DH, Gaynes, RP, et al.Methicillin-resistant Staphylococcus aureus in US hospitals, 1975-1991. Infect Control Hosp Epidemiol 1992;13:582586.Google Scholar
42.Srinivasan, A, Dick, JD, Perl, TM. Vancomycin resistance in staphylococci. Clin Microbiol Rev 2002;15:430438.Google Scholar
43.Steinman, MA, Gonzales, R, Under, JA, Landefeld, CS. Changing use of antibiotics in community-based outpatient practice, 1991-1999. Ann Intern Med 2003;138:525533.Google Scholar
44.Aly, R, Shinefield, HR, Maibach, HI. Staphylococcus aureus adherence to nasal epithelial cells: studies of some parameters. In: Maibach, HI, Aly, R, eds. Skin Microbiology. New York: Springer-Verlag; 1981:171179.Google Scholar
45.Jacobs, SI, Williamson, GM, Willis, AT. Nasal abnormalities and the carrier rate of Staphylococcus aureus. J Clin Pathol 1961;14:519521.CrossRefGoogle ScholarPubMed
46.Noble, WC, Williams, REO, Jevons, MP, Shooter, RA. Some aspects of nasal carriage of staphylococci. J Clin Pathol 1964;17:7983.Google Scholar
47.Aly, R, Shinefield, HI, Strauss, WG, Maibach, HI. Bacterial adherence to nasal mucosal cells. Infect Immun 1977;17:546549.Google Scholar
48.Brien, LM, Walsh, EJ, Massey, RC, Peacock, SJ, Foster, TJ. Staphylococcus aureus clumping factor B (ClfB) promotes adherence to human type I cytokeratin 10: implications for nasal colonization. Cell Microbiol 2002;4:759770.Google Scholar
49.Fainstein, V, Musher, DM, Cate, TR. Bacterial adherence to pharyngeal cells during viral infection. J Infect Dis 1980;141:172176.Google Scholar
50.Shuter, J, Hatcher, VB, Lowy, FD. Staphylococcus aureus binding to human nasal mucin. Infect Immun 1996;64:310318.Google Scholar