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Staphylococcal nasal carriage in medical students with varying clinical exposure
Journal of Hospital Infection (1983) 4, 75-79
SHORT REPORT
Staphylococcal nasal carriage in medical students with varying clinical exposure J. C. P. Kingdom, Susan M. Joyce, Fiona L. Bradley, W. Jauch, F. R. Falkiner and C. T. Keane
Department of Clinical Microbiology, Trinity College, St. James’s Hospital, James’s Street, Dublin 8, Eke Summary: Nasal carriage and antibiotic sensitivities of coagulase-positive and coagulase-negative staphylococci were assessed among medical students of three different years. Although carriage rates did not change, there was a trend towards multiple resistance with increasing hospital exposure. Gentamicin resistance in Staphylococcus aZbu.sshowed a similar trend. The relevance of these findings to current views on the origin of gentamicin resistance is discussed. Introduction
Staphylococcus aureus and Staphylococcus albus are both recognized causes of hospital-acquired infection and antibiotic-resistant strains are a particular problem in Dublin Hospitals (Marples et al., 1978; Cafferkey, Hone and Keane, 1982). Staph. aureus nasal carriage can reflect skin carriage in an individual and, in turn, this may result in transmission to susceptible patients. In a recent outbreak due to antibiotic-resistant Staph. aureus, a medical student was shown to be a carrier (Reynolds et al., 1978). This study was undertaken to evaluate the nasal carriage rates of antibiotic-resistant staphylococci, amongst medical students with differing periods of hospital exposure. Subjects and methods
First (Group A), third (Group B) and fifth (Group C) year medical students of Trinity College, Dublin, were studied, and at the time of sampling they had 0, 12, and 36 months clinical experience respectively. Antibiotic treatment of students during the previous two months was noted. This was usually for respiratory tract infection or acne. All 75 students in Group A, 75 of 76 in Group B and only 69 of 84 in Group C took part in the study (Table I). Sterile cotton swabs with transport medium (‘Transwabs’, Medical Wire and Equipment Co. Ltd, Wiltshire) were used to sample the distal 2 cm of both nares of the students. The swabs were inoculated on blood agar and mannitol salt agar (BBL, Cockeysville, USA), and incubated overnight and for 36 h respectively. Before incubation a gentamicin disc (10 pg) was placed on the ‘well 0195-6701/83/010075
6 1983 The Hospital Infection Society
+ 05 SO2.00/0
75
12 months
36 months
13 73*
C 65*
Staph. Staph. Staph. Staph. Staph. Staph.
aureus albus aureus albus aureus albus
Organism
;22 109
;:
22
Number of isolates
:: 3:
2;
R
Tet.
2 30 16
3
M
8
1 2 i
R
Ev.
4
ii 16 07
M
1s
1:
i
R
Trim.
;
E
111
M
10
10 ::
:
17
8
2
Sulph. R M
of resistant strains Gent.
1:
00 0 5
R
;1
00 0
M
staphylocci were isolated. (One student yielded two strains of Staph. aweus.) Trim., trimethoprim; Sulph., sulphonamide; Gent., gentamicin; Meth., methicillin
21 51 ifi
ii
Pen. R
Number
resistance of strains of Staph. aureus and Staph. albus from students
* Number of students from whom coagulase-negative Pen., penicillin; Tet., tetracycline; Ery., erythromycin; R, resistant M, moderately sensitive
Nil
Clinical experience
A 59*
Student group
Table I. Antibiotic
;3
: 0
Meth. R
Staphylococci
in medical
students
77
inoculum’ of the blood agar plate. Staphylococci were identified by their morphology on both media, Gram stain and catalase production. Staph. aweus was distinguished from Staph. albus by the coagulase test (Facklam & Smith, 1976). Susceptibility to a range of antibiotics was determined using Diagnostic Sensitivity Test agar (Oxoid Ltd, Basingstoke) by a modification of the method of Stokes and Waterworth (1972). Th e antibiotics tested were penicillin (two units), tetracycline (10 pg), erythromycin (15 pg), trimethoprim (1.25 pg), sulphonamide (100 pg) and gentamicin (10 pg). Methicillin sensitivities were determined after overnight incubation at 30°C (Hewitt, Coe and Parker, 1969). Organisms found to be resistant to gentamicin were further tested for sensitivity to rifampicin (30 pg), chloramphenicol (30 pg), amikacin (30 pg) and vancomycin (30 pg). Sensitivity was defined as having a zone greater than, equal to, or reduced by not more than 3 mm when compared with the control. Moderate sensitivity was defined by a zone of at least 3 mm radius but reduced by more than 3 mm compared with control. Resistance was defined by a zone of less than 3 mm radius. Coagulase positive staphylococci were phage typed (Blair and Williams, 1961). These typing results were compared with those of Staph. aweus isolated from 14 patients in the hospital group during the first quarter of 1982 when the study was carried out. The strains of Staph. albus were distinguished from one another on the basis of colonial appearance and antibiotic sensitivity patterns. Results
Table I shows the number of students in each group from whom coagulasepositive and negative staphylococci were isolated. One student in Group C carried two strains of Staph. aureus. The carriage rates for this organism of 29 per cent, 32 per cent and 32 per cent did not vary significantly among the three groups. Some individuals yielded more than one strain of coagulase-negative staphylococcus, but again the carriage rates of 79 per cent, 97 per cent and 94 per cent were not significantly different. There was a change of distribution of antibiotic resistance patterns (Table I and Figure 1). The numbers of Staph. aUreUSresistant to three or more antibiotics were two (9 per cent) in Group A, nil in Group B and 12 (55 per cent) in Group C. Only two strains were moderately resistant to gentamicin and these were both from fifth-year medical students. While there was no significant increase in the percentage of multi-resistant strains of coagulase-negative staphylococci in the groups, there was a small increase in the total numbers isolated and a more noticeable increase in the numbers of gentamicin-resistant strains (Table I). The numbers of strains resistant to three or more antibiotics were 6 (10 per cent) in Group A, 13 (16 per cent) in Group B, and 16 (15 per cent) in Group C. The organisms resistant to gentamicin were all multi-resistant (Figure 1). Further testing of these showed that two strains from Group B were resistant to chloramphenicol and one to amikacin, two from Group C were resistant to
J. C. P. Kingdom
0
1234
et al.
56
Number of antibiatlcs
Figure 1. Number of antibiotics to which strains of Staphylococcus albus were resistant. Gentamicin-resistant strains.
chloramphenicol and two resistant and one moderately resistant to amikacin. All were sensitive to rifampicin and vancomycin. Table II shows the distribution of phage types of Staph. aureU$from the three groups of students and from 400 specimens from hospital patients taken in the Table II. Phage types of Staph. aureus from patients and students
Type at RTDf’
Numbers of types from hospital patients*
Number of types isolated from student groups A
Non-typable 94, 96
+ 9
B
C
90
;
i
; 0
i 1
:9
12 0
*:,
i
241
22
24
22
161 40 :4
xi 29 Miscellaneous
43 0
t RTD, routine test dilution + Strains isolated from 400 specimens. The remaining 159 strains were of types not found amongst the students
Staphylococci
in medical students
79
first quarter of 1982, during the period of study. There is a trend towards the isolation of ‘hospital’ strains from final year students. Discussion
We were unable to find a similar study of medical students in the literature. In an attempt to assess the effect of the hospital environment on nasal carriage Henning et al. (1979) studied three different groups: office workers outside the hospital, psychiatric staff and surgical staff. They found that carriage rates (32 per cent) did not differ between the three groups. Our findings are similar. While they did not find any variation in antibiotic resistance they noted that the surgical group had a more labile pattern of carriage. It was not possible to demonstrate strain changes in this study, but it was apparent that ‘hospital’ phage types were more likely to be carried by the final year students. Staph. albus is now an established cause of infection (Leading article, 1981). For example, in patients with prosthetic heart valves, it is the most frequent cause of endocarditis; a common cause of infection in patients with a cerebrospinal fluid shunt, and of sepsis after total hip replacement. In spite of this, little work has been reported on the nasal carriage of these staphylococci. Furthermore, plasmid-mediated gentamicin resistance has been shown to be transferable between Staph. albus and Staph. aureus both in vitro and on human skin (Jaffe et al., 1980). It has been suggested that this mechanism might account for the emergence of gentamicin resistance in Staph. aureus (Naidoo and Noble, 1981). Our results indicate that acquisition of multiple resistant strains of Staph. albus increases with duration of hospital exposure. This, coupled with the increasing spectrum of infections caused by Staph. albus indicates the need for further studies on the carriage of these organisms. Acknowledgements We would like to acknowledge the co-operation of the laboratory statI of the Central Microbiology Laboratory and the medical students. We are most grateful to Miss Harriett Pomeroy, for phage typing the strains and to Mrs Mary Foody who typed the manuscript.
References Blair, J. E. & Williams, R. E. 0. (1961). Phage typing of staphylococci. Bulletin of the World Health Organisation 24, 771-784. CafIerkey, M. T., Hone, R. & Keane, C. T. (1982). Severe staphylococcal infections treated with vancomycin. Journal of Antimicrobial Chemotherapy 9, 68-74. Facklam, R. & Smith, P. B. (1976). The Gram positive cocci. Human Pathology 17,187-194. Henning, C., Hillborgh, U., Lindvall, K., Marqvardsen, O., Sellers, J., Wahlin, S. & Ransjo, U. (1979). Comparison of Staphylococcus aweus carriage and skin infection rates in hospital and office employees. Journal of Hygiene (Cambridge) 83, 437-444. Hewitt, J. H., Coe, A. W. & Parker, M. T. (1969). The detection of methicillin resistance in Staphylococcus aureus. Journal of Medical Microbiology 2, 443-456. Jaffe, H. W., Sweeney, H. M., Nathan, C., Weinstein, R. A., Kabins, S. A. & Cohen, S. (1980). Identity and interspecific transfer of gentamicin-resistance plasmids in Staphy~OCOCCUS aureus and Staphylococcus epidermidis. Journal of Infectious Diseases 141, 738-746.
80
J. C. P. Kingdom
et al.
Leading article (1981). Coagulase-negative staphylococci. Lancer 1, 139-140. Marples, R. R., Hone, R., Notley, C. M., Richardson, J. F. & Crees-Morris, J. A. (1978). Investigation of Coagulase-negative staphylococci from infections in surgical patients. Zentralblatt fiir Bakteriologie und Hygiene. Abteilung 1. Originale Reihe A 241, 140-l 56. Naidoo, J. 8z Noble, W. C. (1981). Transfer of gentamicin resistance between Coagulase negative and Coagulase-positive staphylococci on skin. Journal of Hygiene (Cambridge) B&183-187. Reynolds, M., Watters, K., Falkiner, F. R., Gargan, P., Lynch, M. & Keane, C. T. (1978). Termination of an outbreak of infection due to a gentamicin and amikacin resistant Staphylococcus aureus by prohibiting the use of gentamicin. Proceedings of the Patho:?;;I Society of Great Britain and Ireland. 54. Journal of Medical Microbiology Stokes,‘E. J. & Waterworth, P. M. (1972). Antibiotic sensitivity Broadsheet No. 55. AssoeMtion of Clinical Pathologists.
tests by diffusion methods.
SHORT REPORT
Staphylococcal nasal carriage in medical students with varying clinical exposure J. C. P. Kingdom, Susan M. Joyce, Fiona L. Bradley, W. Jauch, F. R. Falkiner and C. T. Keane
Department of Clinical Microbiology, Trinity College, St. James’s Hospital, James’s Street, Dublin 8, Eke Summary: Nasal carriage and antibiotic sensitivities of coagulase-positive and coagulase-negative staphylococci were assessed among medical students of three different years. Although carriage rates did not change, there was a trend towards multiple resistance with increasing hospital exposure. Gentamicin resistance in Staphylococcus aZbu.sshowed a similar trend. The relevance of these findings to current views on the origin of gentamicin resistance is discussed. Introduction
Staphylococcus aureus and Staphylococcus albus are both recognized causes of hospital-acquired infection and antibiotic-resistant strains are a particular problem in Dublin Hospitals (Marples et al., 1978; Cafferkey, Hone and Keane, 1982). Staph. aureus nasal carriage can reflect skin carriage in an individual and, in turn, this may result in transmission to susceptible patients. In a recent outbreak due to antibiotic-resistant Staph. aureus, a medical student was shown to be a carrier (Reynolds et al., 1978). This study was undertaken to evaluate the nasal carriage rates of antibiotic-resistant staphylococci, amongst medical students with differing periods of hospital exposure. Subjects and methods
First (Group A), third (Group B) and fifth (Group C) year medical students of Trinity College, Dublin, were studied, and at the time of sampling they had 0, 12, and 36 months clinical experience respectively. Antibiotic treatment of students during the previous two months was noted. This was usually for respiratory tract infection or acne. All 75 students in Group A, 75 of 76 in Group B and only 69 of 84 in Group C took part in the study (Table I). Sterile cotton swabs with transport medium (‘Transwabs’, Medical Wire and Equipment Co. Ltd, Wiltshire) were used to sample the distal 2 cm of both nares of the students. The swabs were inoculated on blood agar and mannitol salt agar (BBL, Cockeysville, USA), and incubated overnight and for 36 h respectively. Before incubation a gentamicin disc (10 pg) was placed on the ‘well 0195-6701/83/010075
6 1983 The Hospital Infection Society
+ 05 SO2.00/0
75
12 months
36 months
13 73*
C 65*
Staph. Staph. Staph. Staph. Staph. Staph.
aureus albus aureus albus aureus albus
Organism
;22 109
;:
22
Number of isolates
:: 3:
2;
R
Tet.
2 30 16
3
M
8
1 2 i
R
Ev.
4
ii 16 07
M
1s
1:
i
R
Trim.
;
E
111
M
10
10 ::
:
17
8
2
Sulph. R M
of resistant strains Gent.
1:
00 0 5
R
;1
00 0
M
staphylocci were isolated. (One student yielded two strains of Staph. aweus.) Trim., trimethoprim; Sulph., sulphonamide; Gent., gentamicin; Meth., methicillin
21 51 ifi
ii
Pen. R
Number
resistance of strains of Staph. aureus and Staph. albus from students
* Number of students from whom coagulase-negative Pen., penicillin; Tet., tetracycline; Ery., erythromycin; R, resistant M, moderately sensitive
Nil
Clinical experience
A 59*
Student group
Table I. Antibiotic
;3
: 0
Meth. R
Staphylococci
in medical
students
77
inoculum’ of the blood agar plate. Staphylococci were identified by their morphology on both media, Gram stain and catalase production. Staph. aweus was distinguished from Staph. albus by the coagulase test (Facklam & Smith, 1976). Susceptibility to a range of antibiotics was determined using Diagnostic Sensitivity Test agar (Oxoid Ltd, Basingstoke) by a modification of the method of Stokes and Waterworth (1972). Th e antibiotics tested were penicillin (two units), tetracycline (10 pg), erythromycin (15 pg), trimethoprim (1.25 pg), sulphonamide (100 pg) and gentamicin (10 pg). Methicillin sensitivities were determined after overnight incubation at 30°C (Hewitt, Coe and Parker, 1969). Organisms found to be resistant to gentamicin were further tested for sensitivity to rifampicin (30 pg), chloramphenicol (30 pg), amikacin (30 pg) and vancomycin (30 pg). Sensitivity was defined as having a zone greater than, equal to, or reduced by not more than 3 mm when compared with the control. Moderate sensitivity was defined by a zone of at least 3 mm radius but reduced by more than 3 mm compared with control. Resistance was defined by a zone of less than 3 mm radius. Coagulase positive staphylococci were phage typed (Blair and Williams, 1961). These typing results were compared with those of Staph. aweus isolated from 14 patients in the hospital group during the first quarter of 1982 when the study was carried out. The strains of Staph. albus were distinguished from one another on the basis of colonial appearance and antibiotic sensitivity patterns. Results
Table I shows the number of students in each group from whom coagulasepositive and negative staphylococci were isolated. One student in Group C carried two strains of Staph. aureus. The carriage rates for this organism of 29 per cent, 32 per cent and 32 per cent did not vary significantly among the three groups. Some individuals yielded more than one strain of coagulase-negative staphylococcus, but again the carriage rates of 79 per cent, 97 per cent and 94 per cent were not significantly different. There was a change of distribution of antibiotic resistance patterns (Table I and Figure 1). The numbers of Staph. aUreUSresistant to three or more antibiotics were two (9 per cent) in Group A, nil in Group B and 12 (55 per cent) in Group C. Only two strains were moderately resistant to gentamicin and these were both from fifth-year medical students. While there was no significant increase in the percentage of multi-resistant strains of coagulase-negative staphylococci in the groups, there was a small increase in the total numbers isolated and a more noticeable increase in the numbers of gentamicin-resistant strains (Table I). The numbers of strains resistant to three or more antibiotics were 6 (10 per cent) in Group A, 13 (16 per cent) in Group B, and 16 (15 per cent) in Group C. The organisms resistant to gentamicin were all multi-resistant (Figure 1). Further testing of these showed that two strains from Group B were resistant to chloramphenicol and one to amikacin, two from Group C were resistant to
J. C. P. Kingdom
0
1234
et al.
56
Number of antibiatlcs
Figure 1. Number of antibiotics to which strains of Staphylococcus albus were resistant. Gentamicin-resistant strains.
chloramphenicol and two resistant and one moderately resistant to amikacin. All were sensitive to rifampicin and vancomycin. Table II shows the distribution of phage types of Staph. aureU$from the three groups of students and from 400 specimens from hospital patients taken in the Table II. Phage types of Staph. aureus from patients and students
Type at RTDf’
Numbers of types from hospital patients*
Number of types isolated from student groups A
Non-typable 94, 96
+ 9
B
C
90
;
i
; 0
i 1
:9
12 0
*:,
i
241
22
24
22
161 40 :4
xi 29 Miscellaneous
43 0
t RTD, routine test dilution + Strains isolated from 400 specimens. The remaining 159 strains were of types not found amongst the students
Staphylococci
in medical students
79
first quarter of 1982, during the period of study. There is a trend towards the isolation of ‘hospital’ strains from final year students. Discussion
We were unable to find a similar study of medical students in the literature. In an attempt to assess the effect of the hospital environment on nasal carriage Henning et al. (1979) studied three different groups: office workers outside the hospital, psychiatric staff and surgical staff. They found that carriage rates (32 per cent) did not differ between the three groups. Our findings are similar. While they did not find any variation in antibiotic resistance they noted that the surgical group had a more labile pattern of carriage. It was not possible to demonstrate strain changes in this study, but it was apparent that ‘hospital’ phage types were more likely to be carried by the final year students. Staph. albus is now an established cause of infection (Leading article, 1981). For example, in patients with prosthetic heart valves, it is the most frequent cause of endocarditis; a common cause of infection in patients with a cerebrospinal fluid shunt, and of sepsis after total hip replacement. In spite of this, little work has been reported on the nasal carriage of these staphylococci. Furthermore, plasmid-mediated gentamicin resistance has been shown to be transferable between Staph. albus and Staph. aureus both in vitro and on human skin (Jaffe et al., 1980). It has been suggested that this mechanism might account for the emergence of gentamicin resistance in Staph. aureus (Naidoo and Noble, 1981). Our results indicate that acquisition of multiple resistant strains of Staph. albus increases with duration of hospital exposure. This, coupled with the increasing spectrum of infections caused by Staph. albus indicates the need for further studies on the carriage of these organisms. Acknowledgements We would like to acknowledge the co-operation of the laboratory statI of the Central Microbiology Laboratory and the medical students. We are most grateful to Miss Harriett Pomeroy, for phage typing the strains and to Mrs Mary Foody who typed the manuscript.
References Blair, J. E. & Williams, R. E. 0. (1961). Phage typing of staphylococci. Bulletin of the World Health Organisation 24, 771-784. CafIerkey, M. T., Hone, R. & Keane, C. T. (1982). Severe staphylococcal infections treated with vancomycin. Journal of Antimicrobial Chemotherapy 9, 68-74. Facklam, R. & Smith, P. B. (1976). The Gram positive cocci. Human Pathology 17,187-194. Henning, C., Hillborgh, U., Lindvall, K., Marqvardsen, O., Sellers, J., Wahlin, S. & Ransjo, U. (1979). Comparison of Staphylococcus aweus carriage and skin infection rates in hospital and office employees. Journal of Hygiene (Cambridge) 83, 437-444. Hewitt, J. H., Coe, A. W. & Parker, M. T. (1969). The detection of methicillin resistance in Staphylococcus aureus. Journal of Medical Microbiology 2, 443-456. Jaffe, H. W., Sweeney, H. M., Nathan, C., Weinstein, R. A., Kabins, S. A. & Cohen, S. (1980). Identity and interspecific transfer of gentamicin-resistance plasmids in Staphy~OCOCCUS aureus and Staphylococcus epidermidis. Journal of Infectious Diseases 141, 738-746.
80
J. C. P. Kingdom
et al.
Leading article (1981). Coagulase-negative staphylococci. Lancer 1, 139-140. Marples, R. R., Hone, R., Notley, C. M., Richardson, J. F. & Crees-Morris, J. A. (1978). Investigation of Coagulase-negative staphylococci from infections in surgical patients. Zentralblatt fiir Bakteriologie und Hygiene. Abteilung 1. Originale Reihe A 241, 140-l 56. Naidoo, J. 8z Noble, W. C. (1981). Transfer of gentamicin resistance between Coagulase negative and Coagulase-positive staphylococci on skin. Journal of Hygiene (Cambridge) B&183-187. Reynolds, M., Watters, K., Falkiner, F. R., Gargan, P., Lynch, M. & Keane, C. T. (1978). Termination of an outbreak of infection due to a gentamicin and amikacin resistant Staphylococcus aureus by prohibiting the use of gentamicin. Proceedings of the Patho:?;;I Society of Great Britain and Ireland. 54. Journal of Medical Microbiology Stokes,‘E. J. & Waterworth, P. M. (1972). Antibiotic sensitivity Broadsheet No. 55. AssoeMtion of Clinical Pathologists.
tests by diffusion methods.