Original Article
Staphylococcus aureus Nasal Carriage and Infection in Patients on Continuous Ambulatory Peritoneal Dialysis
N Engl J Med 1990; 322:505-509February 22, 1990
- Abstract
- Abstract
We studied 140 consecutive patients beginning continuous ambulatory peritoneal dialysis (CAPD) at one of seven hospitals to assess the relation of the nasal carriage of Staphylococcus aureus to subsequent catheter-exit-site infection or peritonitis. Shortly before the implantation of the catheters, the patients' anterior nares were cultured for the presence of S. aureus. Antibiotics were not prescribed for the S. aureus carriers, but all the patients were monitored for signs of catheter infection (median follow-up, 10.4 months).
At the initiation of CAPD, 63 patients (45 percent) carried S. aureus in the nares. Nasal carriage was more frequent among the 30 patients with diabetes (77 percent) than among the 110 without the disease (36 percent). The carriers of S. aureus had a significantly higher rate of exit-site infection than the noncarriers (0.40 vs. 0.10 episode per year; P = 0.012). Of these episodes, 24 of 34 were caused by S. aureus. The rates of peritonitis of all bacterial types did not differ significantly between the groups, but all 11 episodes of peritonitis caused by S. aureus occurred among the carriers. In 85 percent of the patients with clinical S. aureus infections, the strain from the nares and the strain causing the infection were similar in phage type and antibiotic profile.
We conclude that in patients beginning ambulatory peritoneal dialysis, the nasal carriage of S. aureus is associated with an increased risk of catheter-exit-site infection and that the performance of nasal cultures before the implantation of the catheter can identify patients at high risk of subsequent morbidity. (N Engl J Med 1990; 322:505–9.)
Media in This Article
Table 1
Patients' Characteristics and Causes of End-Stage Renal Disease in Carriers and Noncarriers of S. aureus.*Table 2
Rates of Exit-Site Infection and Peritonitis among Carriers and Noncarriers of S. aureus.Article Activity
- Article
THE importance of Staphylococcus aureus as an etiologic agent of exit-site infection in continuous ambulatory peritoneal dialysis (CAPD) has been well established.1 2 3 4 Recent studies have shown that pericatheter infections are a major cause of the failure of CAPD catheters. Piraino et al. reported that exit-site infection, independently of peritonitis, was responsible for 57 percent of the cannulas removed during a five-year period.5 Zimmerman et al. identified S. aureus as the chief etiologic agent associated with the removal of catheters due to infection.1 Davies et al. demonstrated that the late removal of cannulas was due primarily to recurrent peritonitis caused by S. aureus. 6 The high rate of recurrence associated with S. aureus infection and the serious consequences of disease caused by this pathogen indicate that more information is needed about the predisposition to S. aureus invasion in patients undergoing CAPD.1 , 4
In a five-year prospective, controlled study of patients on hemodialysis, Yu et al. established that S. aureus infection occurred significantly more frequently in nasal carriers of the organism than in noncarriers.7 Previous investigations among patients undergoing CAPD6 , 8 9 10 have suggested a possible link between the nasal carriage of this organism and exit-site infection, peritonitis, or both. However, the numbers of patients studied were relatively small, and most were studied after CAPD was started.
In May 1987 we began monitoring new patients undergoing CAPD at seven European hospitals to investigate any association between the nasal carriage of S. aureus before dialysis and infection during CAPD. By identifying the initial strain before the creation of an abdominal-catheter exit site, we were able to follow the evolution of colonization with that organism and its effect on the infection rate.
Methods
Patient Selection and Study Design
The study population consisted of consecutive patients starting CAPD in seven hospitals. There were no enrollment restrictions based on age, sex, race, end-stage renal disease, or previous dialysis therapy. During the 48 hours preceding the implantation of the catheter, the anterior nares of each patient were cultured for the carriage of S. aureus. The patients from whom the organism was isolated were designated the carrier group; those who did not harbor S. aureus in the anterior nares before the implantation of the catheter were designated noncarriers. After the patients had been discharged on CAPD, nasal and catheter-exit-site cultures were obtained from those in the carrier group at each clinic visit (monthly or bimonthly, depending on the hospital). Cultures were obtained from two thirds of the noncarriers on a similar schedule, and from the remainder every two to three months. All the strains of S. aureus isolated at clinic visits were sent to the coordinating laboratory. During each clinic visit, the physician inspected the exit site and reported the patient's status to the coordinating laboratory. All episodes of infection and their causes were documented by one of us at the time of presentation. When a hospital laboratory isolated S. aureus, the strain was sent to the coordinating laboratory for comparison with the surveillance strains from the nares of the patient. When strains colonizing the exit site were isolated, they were also compared with the surveillance strains. The strains isolated at different visits and from different sites in the same patient were compared according to phage type, antibiotic profile, and biotype.
The follow-up period was from the implantation of the catheter until January 1989, or until the patient discontinued CAPD, if earlier.
Culture Methods and Mediums
To obtain the cultures, a dual rayon swab (Culturette, Marion Scientific) was rotated in each anterior naris and streaked onto a medium routinely used by the hospital laboratory for the isolation of S. aureus, which was then incubated at 37°C. Gram-positive, coagulase-positive cocci were tested for antibiotic sensitivity according to the routine methods of each hospital. The pure culture was sent on slants of brain—heart infusion agar (Diagnostics Pasteur) to the coordinating laboratory, along with the accompanying antibiotic profile and the appropriate patient form completed by the physician. The pure culture was transferred to mannitol salt agar (BBL Microbiology Systems) and incubated at 37°C for 24 hours, then transferred to trypticase soy agar (Oxoid) and incubated for 24 hours at 37°C. The results of catalase and coagulase tests were confirmed, and the culture was prepared for phage typing and the determination of antibiotic profile and biotype.
S. aureus strains isolated from clinically normal exit sites and from cases of exit-site infection, tunnel infection, and peritonitis were obtained and treated in the same manner. The culture collection was maintained in long-term storage in trypticase soy broth and glycerol (15 percent vol/vol) at −70°C.
Bacteriophage Typing
All the S. aureus strains isolated from patients in the study were phage typed with the standard bacteriophages of the International Typing Set.11 , 12 All the cultures were typed in a blind manner at the Belgian national reference laboratory for phage typing, the Institut Pasteur Brabant. Cultures that did not react with the phages at the routine test dilution were typed with phages at 100 times that dilution. Eighty-five percent of the cultures could be typed with one of these dilutions.
Antibiotic Profile and Biotype
Preliminary antibiotic profiles of the cultures were obtained at the hospitals with the use of each laboratory's standard antibiotic selections. At the coordinating laboratory, we standardized antibiotic profiles and obtained biotypes using the autoScan-4 automated scanning system (Baxter Healthcare, Microscan Division) in conjunction with positive combo 2I panels containing biochemicals and dilutions of antimicrobial agents in dehydrated form. Positive identification (probability >85 percent) of the strain was used as the criterion for inclusion in the study.13 By January 1989, 525 S. aureus strains had been collected from patients in all the participating hospitals. We identified 95 percent of these strains as S. aureus using the autoScan-4 (identification probability, 99 percent).
Definitions
The diagnosis of exit-site infection was based on pericatheter redness or exudate, with or without a positive culture.5 , 14 The formation of a crust around the exit site was not considered an indication of infection. The diagnosis of tunnel infection was made if erythema, edema, or tenderness of the subcutaneous tunnel was present, with or without discharge and a positive culture. A cell count was performed in the dialysate when fever, tenderness, abdominal pain, or a turbid dialysate was present. Peritonitis was defined as a dialysate leukocyte count of more than 100 cells per cubic millimeter, with more than 50 percent of these cells being polymorphonuclear leukocytes. Patients were considered to have new episodes of infection by the same organism if they had been free of symptoms at the end of antibiotic therapy and if signs of the infection recurred more than four weeks after the onset of the preceding infection.
Treatment of Exit-Site Infection, Tunnel Infection, and Peritonitis
Infections were treated according to the routine protocols established by each hospital. Exit-site infection was generally treated with oral antibiotics for 10 days. Peritonitis was treated with intraperitoneal antibiotics for 4 to 10 days. S. aureus infections were generally treated with vancomycin or floxacillin for 10 days; however, the choice of antibiotic and the duration of treatment were modified according to the culture reports, clinical response to treatment, and condition of the patient. The nasal carriage of S. aureus was not treated. No antibiotic therapy was administered when S. aureus was present at the exit site but there were no clinical signs of infection.
Statistical Analysis
For the purposes of statistical analysis and in order to ascertain whether a nasal culture before CAPD was predictive of subsequent S. aureus exit-site infection or peritonitis, the patients were considered either pre-CAPD carriers or noncarriers for the entire follow-up period. The negative binomial model15 was used to compare exit-site infections and peritonitis and to calculate the probability of remaining free of exit-site infection. The occurrence of tunnel infection in patients with diabetes and those without diabetes was analyzed with Fisher's exact test. All P values are two-tailed.
Results
Patient Characteristics and Nasal Carriage of S. aureus
One hundred forty patients were enrolled in the study between May 1987 and September 1988. The cumulative follow-up time as of January 1989 was 122 patient-years. The median duration of follow-up was 10.4 months. CAPD was the initial mode of dialysis therapy in 82 percent of the patients. Fourteen percent of both the carrier and noncarrier groups had previously undergone hemodialysis, and approximately 4 percent of the patients in each group received transplants before entering the study. On the basis of pre-CAPD cultures by nasal swab, 63 patients (45 percent) entered the study as carriers of S. aureus, and 77 patients (55 percent) entered as noncarriers. The characteristics of the two groups are shown in Table 1Table 1
Patients' Characteristics and Causes of End-Stage Renal Disease in Carriers and Noncarriers of S. aureus.*. Of the 30 patients with diabetes enrolled in the trial, 23 (77 percent) were nasal carriers; of the 110 patients who did not have diabetes, only 40 (36 percent) were carriers of S. aureus. Diabetes was the most common cause of end-stage renal disease among the carriers. There were more than 12 causes of end-stage renal disease reported in both groups, and no single form of the disease dominated among the noncarriers. The mean age of the carriers was 53.3 years, 5 years less than that of the noncarriers (P not significant).There was no important difference between the two groups in the type of catheter implanted. Tenckhoff double-cuffed catheters were implanted (primarily by midline insertion) in 79 percent of the carriers and 81 percent of the noncarriers. Eight patients received the Missouri Swan Neck catheter, and 20 patients had Toronto Western Hospital Type II catheters implanted surgically through the rectus muscle. Long-term care of the exit site was also similar in the two groups. Seventy-four percent of the noncarrier group and 80 percent of the carrier group used nonocclusive, sterile gauze dressings and povidone—iodine. Thirty-six percent of the patients employed either single-use or reusable disconnecting systems for dialysis. No significant difference in the choice of system existed between the two groups.
There were 11 deaths in the carrier group and 9 in the noncarrier group. Patients in the carrier group left the study because of transplantation (7 patients), transfer to hemodialysis (1), and other medical reasons (1). Noncarriers left the study because of transplantation (11 patients), the recovery of renal function (3), and transfer to hemodialysis (2).
Causes and Rates of Exit-Site Infection and Peritonitis
The analysis of infection rates is shown in Table 2Table 2
Rates of Exit-Site Infection and Peritonitis among Carriers and Noncarriers of S. aureus.. There was a significant difference in the rate of exit-site infection between the S. aureus carriers and the noncarriers. Whereas the probability of remaining free of exit-site infection after 18 months on CAPD was 92 percent among the patients whose nares were not colonized by S. aureus before dialysis, it was only 54 percent among those whose nares were colonized (P = 0.012). Catheters were replaced because of infection in three patients in the carrier group; none of the noncarriers had catheter replacements.The etiologic agents of exit-site infection and peritonitis are shown in Table 3Table 3
Etiologic Agents and Number of Episodes of Exit-Site Infection and Peritonitis in Carriers and Noncarriers of S. aureus.. In the carrier group, S. aureus was responsible for 85 percent of the exit-site infections and 35 percent of the episodes of peritonitis. Three episodes of S. aureus peritonitis occurred in carriers at the same time as an exit-site infection caused by the organism. Six noncarriers acquired S. aureus in the nares during the follow-up period. Among the noncarriers there were eight episodes of exit-site infection, only two of which were caused by S. aureus. There was no peritonitis due to S. aureus in the noncarrier group. Six of the 23 patients with diabetes who were S. aureus carriers (26 percent) had S. aureus infections at the catheter exit site, and 5 (22 percent) had S. aureus peritonitis. Of the 40 S. aureus carriers without diabetes, 14 (35 percent) had S. aureus exit-site infections and 1 had S. aureus peritonitis. In contrast, the seven noncarriers with diabetes had no exit-site infection and no peritonitis due to S. aureus. Two of the 70 noncarriers who did not have diabetes (3 percent) had S. aureus exit-site infections, but none had peritonitis caused by S. aureus.Tunnel Infections
Although infrequent, all seven episodes of infection of the subcutaneous-catheter tunnel were caused by S. aureus. Five of the seven occurred in the carrier group. All five patients had diabetes. The incidence of tunnel infection was higher in the carriers than the noncarriers (0.09 vs. 0.02 episode per year). There was a significant association between diabetes and tunnel infection. Six of the 30 patients with diabetes had an episode of tunnel infection, as compared with only 1 patient without diabetes (P = 0.0003 by Fisher's exact test).
Specificity of the Organism
Unless they had received antibiotics to treat S. aureus infection, the carriers of S. aureus before CAPD tended to have persistent carriage of the same organism, as demonstrated by the phage type. After treatment, the nares culture remained negative for one to four months in half the patients. In most patients, the same organism returned. The results to date of phage typing suggest that a wide variety of phage types are responsible for infection. In 85 percent of the patients with clinical infection, the strain from the nares and the strain causing the infection had a similar phage type and antibiotic profile.
Discussion
This study presents a detailed investigation of the relation between the nasal carriage of S. aureus in patients beginning CAPD and their subsequent risk of infection. The permanent catheters used in CAPD are associated with complications, such as exit-site infections, that may lead to peritonitis and catheter removal.1 , 5 , 6 , 16 , 17 Recent research suggests that the nasal carrier of S. aureus may be at higher risk of exit-site infection during CAPD.6 , 8 9 10 Sewell et al. isolated S. aureus from the nares of 17 patients at least once during their study, and one third of the 30 patients they monitored were chronic and intermittent carriers.8 The nasal carriage of S. aureus has been well documented in patients on hemodialysis.7 , 18 19 20 21 Kirmani et al. reported a carriage rate of 62 percent in patients undergoing hemodialysis, which is higher than the rate of 10 percent to 30 percent reported in the general population.19 , 22
The objective of our study was to establish whether there is a definitive epidemiologic link in CAPD between the nasal carriage of S. aureus before the insertion of the cannula and a subsequent infection. For practical reasons, the patients' nares were cultured only once during the 48 hours preceding the implantation of the catheter. With this technique, we observed that the carriage rate before CAPD was 45 percent, higher than in the general population.6 , 19 , 22 Furthermore, this carrier group had a significantly higher rate of exit-site infection than noncarriers. It remains possible that previous treatment with antibiotics may have transiently abolished the nasal carriage of S. aureus in a few patients at the time of the first sampling. This possibility may explain the two episodes of exit-site infection caused by the organism in patients who were originally classified as noncarriers. In one noncarrier, S. aureus was cultured from the nares two months before the discovery of an exit-site infection by the same organism, as judged by the phage type.
One of our centers obtained pre-CAPD cultures simultaneously from the anterior nares, groin, and abdomen of participating patients. The nasal cultures proved to be the most sensitive (it was possible to culture S. aureus before CAPD from the groin or abdomen of only 10 percent of the carrier patients). In every case in which S. aureus was isolated from another location in the patient before CAPD, the nasal swabs were also positive.
The results of this study indicate that patients undergoing CAPD become infected by endogenously carried strains of S. aureus. It is important to note that 77 percent of the patients with diabetes were carriers and that those with diabetes had significantly more tunnel infections than those without diabetes. This observation deserves further evaluation in view of the increasing number of diabetic patients with end-stage renal disease who now undergo CAPD. It is reported that repeated needle puncture of the skin is a risk factor for the nasal carriage of S. aureus. Patients undergoing hemodialysis,7 intravenous drug abusers,23 otherwise healthy patients who are receiving allergy injections,24 and patients with insulin-dependent diabetes25 , 26 carry S. aureus in the anterior nares at rates up to three times those among control populations. Most of the diabetic patients in our study had insulin-dependent diabetes, which may help explain their high rate of carriage. It should be acknowledged that increased numbers of exit-site infections did not correlate with an increase in episodes of peritonitis; more important, a decrease in the number of exit-site infections (in noncarriers) was not associated with decreased episodes of peritonitis. Although S. aureus did not cause peritonitis in the noncarrier group, peritonitis remains the most serious complication of CAPD.
Persistent nasal carriage did not always lead to exit-site infection during CAPD. One explanation for this may be the erratic shedding of S. aureus from the nose to other parts of the body. Another reason may be that factors in the host, such as nutritional status, predispose some patients to infection, whereas others are only colonized. Finally, some strains of S. aureus may cause infection in patients undergoing CAPD, and other strains may be merely colonizing bacteria. However, we have found no evidence to date that any particular phage type is more likely to be associated with exit-site infection. Whatever the explanation, the majority of clinical events occurred in patients who, in spite of frequent checks, had had no detectable exit-site colonization. S. aureus—positive but clinically normal exit sites were reported in 25 patients, but clinical infection occurred thereafter in only 3. Further monitoring should clarify the importance of exit-site colonization in relation to nasal carriage and infection.
Previous studies have reported an overall incidence of S. aureus peritonitis of approximately 20 percent.6 , 27 , 28 In our experience, all S. aureus peritonitis was confined to the carrier group. In sharp contrast, noncarriers had peritonitis that was predominantly due to S. epidermidis; to date, no S. aureus peritonitis has occurred in this group.
Thus, this study shows that the isolation of S. aureus from the nares before the insertion of the catheter identifies patients at high risk of morbidity. Further research should evaluate the merits of suppressing the nasal carriage of S. aureus in patients about to undergo CAPD and should determine how to improve the care of the exit site in those at risk for exit-site infection.
Supported by a grant from the Baxter European Research and Development Center.
We are indebted to Bernadette Piret for technical assistance, Dr. Edward Vonesh for statistical analysis, Nelda Claeys for the preparation of the manuscript, and the members of the hospital nursing and microbiology laboratory staffs who made this research possible.
Source Information
From Baxter R&D Europe, Nivelles, Belgium (M.A.L., F.P.); the Cardiff Royal Infirmary, Cardiff, United Kingdom (G.A.C.); the Centre Hospitalier Général L. Pasteur, Colmar, France (B.F.); Mas de Rochet, Montpellier, France (A.S.); the Hôpital Régional d'Orléans, Orleans, France (G.D.D.); the Hôpital de la Durance, Avignon, France (C.B.); the Hôpital Saint André, Bordeaux, France (C.W., Y.K.); and the Centre Hospitalier Universitaire de Nancy, Vandoeuvre, France (M.K.). Address reprint requests to Ms. Luzar at Baxter R&D Europe, Rue du Progrès 7, B-1400 Nivelles, Belgium.
- References
References
1
Zimmerman
Web of Science2
Mitwalli A, Kim D, Wu G, et al. Single- vs. double-cuff peritoneal catheters: a prospective controlled trial. In: Khanna R, Nolph K, Prowant B, Twardowski Z, Oreopoulos D, eds. Advances in CAPD: proceedings of the fifth annual CAPD conference, Kansas City, Mo., February 1985. Toronto: University of Toronto Press, 1985:35–40.
3
Zimmerman
Web of Science | Medline4
Abraham
Web of Science5
Piraino
Web of Science | Medline6
Davies
Web of Science | Medline7
Yu
Full Text | Web of Science | Medline8
Sewell
CrossRef | Web of Science | Medline9
Ahrens 10
Ahrens
Web of Science11
Blair
CrossRef | Web of Science | Medline12
Smith PB. Bacteriophage typing of Staphylococcus aureus. In: Cohen JO, ed. The staphylococci. New York: Wiley-Interscience, 1972:431–41.
13
Pfaller
Medline14
Pierratos
Web of Science15
Vonesh
Web of Science16
Vas 17
Cantaluppi A, Castlenovo C, Scalamogna A, et al. ESI in patients on CAPD. In: Khanna R, Nolph K, Prowant B, Twardowski Z, Oreopoulos D, eds. Advances in CAPD: proceedings of the fifth annual CAPD conference, Kansas City, Mo., 1985. Toronto: University of Toronto Press, 1985:45–8.
18
Goldblum
Web of Science19
Kirmani
CrossRef | Web of Science | Medline20
Noble
CrossRef | Web of Science | Medline21
Rebel
CrossRef | Web of Science | Medline22
Williams
Web of Science | Medline23
Tuazon
CrossRef | Web of Science | Medline24
Kirmani
Medline25
Smith
CrossRef | Web of Science | Medline26
Tuazon
CrossRef | Web of Science | Medline27
Vas
Web of Science | Medline28
Gould
CrossRef | Web of Science | Medline
- Citing Articles (82)
Citing Articles
1
Steven Y. C. Tong, Luke F. Chen, Vance G. Fowler. (2011) Colonization, pathogenicity, host susceptibility, and therapeutics for Staphylococcus aureus: what is the clinical relevance?. Seminars in Immunopathology
CrossRef2
Andrew E Simor. (2011) Staphylococcal decolonisation: an effective strategy for prevention of infection?. The Lancet Infectious Diseases 11:12, 952-962
CrossRef3
D. Lepelletier, J.-C. Lucet. (2011) Impact du dépistage et de la décontamination sur la prévention des infections du site opératoire à Staphylococcus aureus. Journal des Anti-infectieux
CrossRef4
P. O. Verhoeven, F. Grattard, A. Carricajo, F. Lucht, C. Cazorla, O. Garraud, B. Pozzetto, P. Berthelot. (2011) An algorithm based on one or two nasal samples is accurate to identify persistent nasal carriers of Staphylococcus aureus. Clinical Microbiology and Infectionno-no
CrossRef5
Vanthida Huang, Samantha J. Eells. 2011. Staphylococcus Aureus. , 161-177.
CrossRef6
Sharon J. Nessim. (2011) Prevention Of Peritoneal Dialysis–Related Infections. Seminars in Nephrology 31:2, 199-212
CrossRef7
M E Fernández-Rubio, L Rebolledo-Lara, M Martinez-García, M Alarcón-Tomás, C Cortés-Valdés. (2010) The conjunctival bacterial pattern of diabetics undergoing cataract surgery. Eye 24:5, 825-834
CrossRef8
René te Witt, Alex van Belkum, Willem B van Leeuwen. (2010) Molecular diagnostics and genotyping of MRSA: an update. Expert Review of Molecular Diagnostics 10:4, 375-380
CrossRef9
R. J. Hay, B. M. Adriaans. 2010. Bacterial Infections. , 1-82.
CrossRef10
Sharon J. Peacock. 2010. Staphylococcus. .
CrossRef11
Vimal Chadha, Franz S. Schaefer, Bradley A. Warady. (2010) Dialysis-associated peritonitis in children. Pediatric Nephrology 25:3, 425-440
CrossRef12
Bode, Lonneke G.M., Kluytmans, Jan A.J.W., Wertheim, Heiman F.L., Bogaers, Diana, Vandenbroucke-Grauls, Christina M.J.E., Roosendaal, Robert, Troelstra, Annet, Box, Adrienne T.A., Voss, Andreas, van der Tweel, Ingeborg, van Belkum, Alex, Verbrugh, Henri A., Vos, Margreet C., . (2010) Preventing Surgical-Site Infections in Nasal Carriers of Staphylococcus aureus. New England Journal of Medicine 362:1, 9-17
Full Text13
R. J. Hay, H. R. Ashbee. 2010. , 1.
CrossRef14
Katherine A Barraclough, Carmel M Hawley, E Geoffrey Playford, David W Johnson. (2009) Prevention of access-related infection in dialysis. Expert Review of Anti-infective Therapy 7:10, 1185-1200
CrossRef15
Andrew E. Simor, Nick Daneman. (2009) Staphylococcus aureus Decolonization as a Prevention Strategy. Infectious Disease Clinics of North America 23:1, 133-151
CrossRef16
C M Philpott, A Sharma, D C McKiernan. (2009) Does methicillin-resistant Staphylococcus aureus have a significant role in the peri-operative course of patients undergoing rhinological surgery?. The Journal of Laryngology & Otology 123:02, 191
CrossRef17
A.M.D. Kooistra-Smid, E. van Zanten, A. Ott, S.R. van Dijk, G.I.J.M. Beerthuizen, W.H.M. Vogels, A. van Belkum, H.A. Verbrugh. (2008) Prevention of Staphylococcus aureus burn wound colonization by nasal mupirocin. Burns 34:6, 835-839
CrossRef18
F. Durupt, L. Mayor, M. Bes, M.-E. Reverdy, F. Vandenesch, L. Thomas, J. Etienne. (2007) Prevalence of Staphylococcus aureus toxins and nasal carriage in furuncles and impetigo. British Journal of Dermatology 157:6, 1161-1167
CrossRef19
Beata Krawczyk, Justyna Leibner, Wioletta Barańska-Rybak, Alfred Samet, Roman Nowicki, Józef Kur. (2007) ADSRRS-fingerprinting and PCR MP techniques for studies of intraspecies genetic relatedness in Staphylococcus aureus. Journal of Microbiological Methods 71:2, 114-122
CrossRef20
Robert N. Foley. (2007) Infections in Patients with Chronic Kidney Disease. Infectious Disease Clinics of North America 21:3, 659-672
CrossRef21
Kerry L. LaPlante. (2007) In vitro activity of lysostaphin, mupirocin, and tea tree oil against clinical methicillin-resistant Staphylococcus aureus. Diagnostic Microbiology and Infectious Disease 57:4, 413-418
CrossRef22
V. Schwenger. (2007) PD-assoziierte Peritonitis. Der Nephrologe 2:2, 107-118
CrossRef23
Thomas R. Talbot. (2005) Diabetes mellitus and cardiothoracic surgical site infections. American Journal of Infection Control 33:6, 353-359
CrossRef24
Adam Keene, Peter Vavagiakis, Mei‐Ho Lee, Kathryn Finnerty, Deborah Nicolls, Christian Cespedes, Bianca Quagliarello, Mary Ann Chiasson, David Chong, Franklin D. Lowy. (2005) Staphylococcus aureus Colonization and the Risk of Infection in Critically Ill Patients • . Infection Control and Hospital Epidemiology 26:7, 622-628
CrossRef25
Jan L. Nouwen, Marien W.J.A. Fieren, Susan Snijders, Henri A. Verbrugh, Alex van Belkum. (2005) Persistent (not intermittent) nasal carriage of Staphylococcus aureus is the determinant of CPD-related infections. Kidney International 67:3, 1084-1092
CrossRef26
M. Millar. 2005. Microbial biofilms and clinical implants. , 619-636.
CrossRef27
Damian C. Melles, Raymond F.J. Gorkink, Hélène A.M. Boelens, Susan V. Snijders, Justine K. Peeters, Michael J. Moorhouse, Peter J. van der Spek, Willem B. van Leeuwen, Guus Simons, Henri A. Verbrugh, Alex van Belkum. (2004) Natural population dynamics and expansion of pathogenic clones of Staphylococcus aureus. Journal of Clinical Investigation 114:12, 1732-1740
CrossRef28
Philip M. Polgreen, Loreen A. Herwaldt. (2004) Staphylococcus aureus colonization and nosocomial infections: Implications for prevention. Current Infectious Disease Reports 6:6, 435-441
CrossRef29
J. L. Nouwen, A. Ott, M. F. Q. Kluytmans-Vandenbergh, H. A. M. Boelens, A. Hofman, A. van Belkum, H. A. Verbrugh. (2004) Predicting the Staphylococcus aureus Nasal Carrier State: Derivation and Validation of a "Culture Rule". Clinical Infectious Diseases 39:6, 806-811
CrossRef30
Dulce Barbosa, Lidimara Lima, Suzane Silbert, Hélio Sader, Miguel Cendoroglo, Sergio Draibe, Luis Camargo, Lucila Vianna, Angelica Belasco, Ricardo Sesso. (2004) Evaluation of the prevalence and risk factors for colonization by vancomycin-resistant Enterococcus among patients on dialysis. American Journal of Kidney Diseases 44:2, 337-343
CrossRef31
Loreen A. Herwaldt, Joseph J. Cullen, Pamela French, Jianfang Hu, Michael A. Pfaller, Richard P. Wenzel, Trish M. Perl. (2004) Preoperative Risk Factors for Nasal Carriage of Staphylococcus aureus • . Infection Control and Hospital Epidemiology 25:6, 481-484
CrossRef32
Agnese Andollina, Alessandra Cesare, Giorgia Bertoni, Liliana Modelli, Gerardo Manfreda. (2004) Identification and genetic characterisation of orthopaedic Staphylococcus isolates collected in Italy by automated Eco RI ribotyping. FEMS Microbiology Letters 234:2, 275-280
CrossRef33
Alex Van Belkum, Marly Kools-Sijmons, Henri Verbrugh. (2002) Attachment of Staphylococcus aureus to eukaryotic cells and experimental pitfalls in staphylococcal adherence assays: a critical appraisal. Journal of Microbiological Methods 48:1, 19-42
CrossRef34
Michel Carrier, Richard Marchand, Pierre Auger, Yves Hébert, Michel Pellerin, Louis P Perrault, Raymond Cartier, Denis Bouchard, Nancy Poirier, Pierre Pagé. (2002) Methicillin-resistant Staphylococcus aureus infection in a cardiac surgical unit. The Journal of Thoracic and Cardiovascular Surgery 123:1, 40-44
CrossRef35
Sharon J. Peacock, Ishani de Silva, Franklin D. Lowy. (2001) What determines nasal carriage of Staphylococcus aureus?. Trends in Microbiology 9:12, 605-610
CrossRef36
Susie Q. Lew, Kianoosh Kaveh. (2000) Dialysis Access Related Infections. ASAIO Journal 46:6, S6-S12
CrossRef37
A.A. Alghaithy, N.E. Bilal, M. Gedebou, A.H. Weily. (2000) Nasal carriage and antibiotic resistance of Staphylococcus aureus isolates from hospital and non-hospital personnel in Abha, Saudi Arabia. Transactions of the Royal Society of Tropical Medicine and Hygiene 94:5, 504-507
CrossRef38
Mrinal K Dasgupta. (2000) Exit-site and catheter-related infections in peritoneal dialysis: Problems and progress. Nephrology 5:1-2, 17-25
CrossRef39
H Jakob. (2000) The endogenous pathway is a major route for deep sternal wound infection. European Journal of Cardio-Thoracic Surgery 17:2, 154-160
CrossRef40
L. Fierobe, D. Decre, C. Muller, J.-C. Lucet, J.-P. Marmuse, J. Mantz, J.-M. Desmonts. (1999) Methicillin-Resistant Staphylococcus aureus as a Causative Agent of Postoperative Intra-abdominal Infection: Relation to Nasal Colonization. Clinical Infectious Diseases 29:5, 1231-1238
CrossRef41
Joseph M. Mylotte, Lucinda Kahler, Ellen Jackson. (1999) “Pulse” Nasal Mupirocin Maintenance Regimen in Patients Undergoing Continuous Ambulatory Peritoneal Dialysis • . Infection Control and Hospital Epidemiology 20:11, 741-745
CrossRef42
A. Hoefnagels-Schuermans, W. E. Peetermans, M. Jorissen, S. Lierde, J. Oord, R. Vos, J. Eldere. (1999) Staphylococcus aureus adherence to nasal epithelial cells in a physiological in vitro model. In Vitro Cellular & Developmental Biology - Animal 35:8, 472-480
CrossRef43
Gilad E. Amiel, Anthony Atala. (1999) Current and future modalities for functional renal replacement. Urologic Clinics of North America 26:1, 235-246
CrossRef44
M Tao, H Yamashita, K Watanabe, T Nagatake. (1999) Possible virulence factors of Staphylococcus aureus in a mouse septic model. FEMS Immunology & Medical Microbiology 23:2, 135-146
CrossRef45
Kieren A. Marr, LiKuo Kong, Vance G. Fowler, Ajay Gopal, Daniel J. Sexton, Peter J. Conlon, G. Ralph Corey. (1998) Incidence and outcome of Staphylococcus aureus bacteremia in hemodialysis patients. Kidney International 54:5, 1684-1689
CrossRef46
Andreas VYCHYTIL, Walter H HÖRL. (1998) Catheter-related infections in peritoneal dialysis patients: New aspects. Nephrology 4:5-6, 321-325
CrossRef47
L.A. Herwaldt. (1998) Reduction of Staphylococcus aureus nasal carriage and infection in dialysis patients. Journal of Hospital Infection 40, S13-S23
CrossRef48
Karen A. Holbrook, Robert S. Klein, Diana Hartel, David A. Elliott, Todd B. Barsky, Liza H. Rothschild, Franklin D. Lowy. (1997) Staphylococcus aureus Nasal Colonization in HIV-Seropositive and HIV-Seronegative Drug Users. Journal of Acquired Immune Deficiency Syndromes and Human Retrovirology 16:4, 301-306
CrossRef49
Dinna N. Cruz, Mark A. Perazella. (1997) Biochemical aberrations in a dialysis patient following parathyroidectomy. American Journal of Kidney Diseases 29:5, 759-768
CrossRef50
Beth Piraino, Victor L. Yu. (1997) Nasal Mupirocin: Its Role in Dialysis Patients. Seminars in Dialysis 10:3, 145-147
CrossRef51
A.P.R. Wilson, C. Lewis, H. O'Sullivan, N. Shetty, G.H. Neild, M. Mansell. (1997) The use of povidone iodine in exit site care for patients undergoing continuous peritoneal dialysis (CAPD). Journal of Hospital Infection 35:4, 287-293
CrossRef52
MARGARET NAYLOR, BRENDA ROE. (1997) A study of the efficacy of dressings in preventing infections of continuous ambulatory peritoneal dialysis catheter exit sites. Journal of Clinical Nursing 6:1, 17-24
CrossRef53
Christian Ruef, Sergio Fanconi, David Nadal. (1996) Sternal wound infection after heart operations in pediatric patients associated with nasal carriage of Staphylococcus aureus. The Journal of Thoracic and Cardiovascular Surgery 112:3, 681-686
CrossRef54
Brijendra Gupta, Judy Bernardini, Beth Piraino. (1996) Peritonitis associated with exit site and tunnel infections. American Journal of Kidney Diseases 28:3, 415-419
CrossRef55
J. Zimakoff, F.Bangsgaard Pedersen, L. Bergen, J. Baagø-Nielsen, B. Daldorph, F. Espersen, B.Gahrn Hansen, N. Høiby, O.B. Jepsen, P. Joffe, H.J. Kolmos, M. Klausen, K. Kristoffersen, J. Ladefoged, S. Olesen-Larsen, V.T. Rosdahl, J. Scheibel, B. Storm. (1996) Staphylococcus aureus carriage and infections among patients in four haemo- and peritoneal-dialysis centres in Denmark. Journal of Hospital Infection 33:4, 289-300
CrossRef56
Judith Bernardini, Beth Piraino, Jean Holley, James R. Johnston, Ronald Lutes. (1996) A randomized trial of staphylococcus aureus prophylaxis in peritoneal dialysis patients: Mupirocin calcium ointment 2% applied to the exit site versus cyclic oral rifampin. American Journal of Kidney Diseases 27:5, 695-700
CrossRef57
Kailash K. Jindal. (1995) Avoiding Technique Failure in Chronic Peritoneal Dialysis. Seminars in Dialysis 8:6, 359-361
CrossRef58
Beth Piraino, Bernadette Faller. (1995) The Prevention of Staphylococcus uureus PeritoneaI DialysisRelated Infections. Seminars in Dialysis 8:6, 355-358
CrossRef59
J. Stewart Cameron. (1995) Host defences in continuous ambulatory peritoneal dialysis and the genesis of peritonitis. Pediatric Nephrology 9:5, 647-662
CrossRef60
R.P. Wenzel, T.M. Perl. (1995) The significance of nasal carriage of Staphylococcus aureus and the incidence of postoperative wound infection. Journal of Hospital Infection 31:1, 13-24
CrossRef61
Joanne M. Bargman. (1995) Nasal Carriage of Staphylococcus aureus in Dialysis Patients. Seminars in Dialysis 8:4, 220-225
CrossRef62
J. N. Maslow, S. Brecher, J. Gunn, A. Durbin, M. A. Barlow, R. D. Arbeit. (1995) Variation and persistence of methicillin-resistantStaphylococcus aureus strains among individual patients over extended periods of time. European Journal of Clinical Microbiology & Infectious Diseases 14:4, 282-290
CrossRef63
BARRY N. KREISWIRTH, SUZANNE M. LUTWICK, EDWARD K. CHAPNICK, JEREMY D. GRADON, LARRY I. LUTWICK, DOUGLAS V. SEPKOWITZ, WILLIAM EISNER, MICHAEL H. LEVI. (1995) Tracing the Spread of Methicillin-Resistant Staphylococcus aureus by Southern Blot Hybridization Using Gene-Specific Probes of mec and Tn 554. Microbial Drug Resistance 1:4, 307-313
CrossRef64
A.P.R. Wilson, G.M. Scott, C. Lewis, G. Neild, C. Rudge. (1994) Audit of infection in continuous ambulatory peritoneal dialysis. Journal of Hospital Infection 28:4, 265-271
CrossRef65
E. Stubbs, M. Pegler, A. Vickery, C. Harbour. (1994) Nasal carriage of Staphylococcus aureus in Australian (pre-clinical and clinical) medical students. Journal of Hospital Infection 27:2, 127-134
CrossRef66
I.R.B. Hudson. (1994) The efficacy of intranasal mupirocin in the prevention of staphylococcal infections: a review of recent experience. Journal of Hospital Infection 27:2, 81-98
CrossRef67
Zbylut J. Twardowski. (1993) RECURRENT PERITONEAL CATHETER EXIT-SITE INFECTIONS: II. Seminars in Dialysis 6:6, 406-408
CrossRef68
Wai Choong Lye, See Odd Leong, Evan Jon Choon Lee. (1993) Methicillin-resistant Staphylococcus aureus nasal carriage and infections in CAPD. Kidney International 43:6, 1357-1362
CrossRef69
(1993) Risk of CAPD Complications in Carriers of Staph. Aureus. Seminars in Dialysis 6:1, 71-71
CrossRef70
T. Weinke, R. Schiller, F. J. Fehrenbach, H. D. Pohle. (1992) Association betweenStaphylococcus aureus nasopharyngeal colonization and septicemia in patients infected with the human immunodeficiency virus. European Journal of Clinical Microbiology & Infectious Diseases 11:11, 985-989
CrossRef71
M. Dan, Y. Moses, F. Poch, R. Gutman, J. Asherov. (1992) Carriage of methicillin-resistantStaphylococcus aureus by non-hospitalized subjects in Israel. Infection 20:6, 332-335
CrossRef72
Zbylut J. Twardowski. (1992) Peritoneal Dialysis Catheter Exit Site Infections: Prevention, Diagnosis, Treatment, and Future Directions. Seminars in Dialysis 5:4, 305-315
CrossRef73
Zheng-Yi Yuan, Elias Balaskas, Amit Gupta, Joanne M. Bargman, Dimitrios G. Oreopoulos. (1992) CAPD Is More Advantageous. Seminars in Dialysis 5:3, 181-188
CrossRef74
Antonio Pignatari, Linda D. Boyken, Loreen A. Herwaldt, Richard Hollis, Ivani Leme, Ricardo Sesso, Michael A. Pfaller. (1992) Application of restriction endonuclease analysis of chromosomal DNA in the study of Staphylococcus aureus colonization in continuous ambulatory peritoneal dialysis patients. Diagnostic Microbiology and Infectious Disease 15:3, 195-199
CrossRef75
B. A. Lipsky, R. E. Pecoraro, J. H. Ahroni, R. L. Peugeot. (1992) Immediate and long-term efficacy of systemic antibiotics for eradicating nasal colonization withStaphylococcus aureus. European Journal of Clinical Microbiology & Infectious Diseases 11:1, 43-47
CrossRef76
Peter Kornfeld, Sondra Fox, Karen Maier, Mazen Mahjoub. (1992) Ten years experience with therapeutic apheresis in a community hospital. Journal of Clinical Apheresis 7:2, 63-68
CrossRef77
J.R. Boelaert, Y.A. De Baere, M.A. Geernaert, Claudine A. Godard, H.W. Van Landuyt. (1991) The use of nasal mupirocin ointment to prevent Staphylococcus aureus bacteraemias in haemodialysis patients: an analysis of cost-effectiveness. Journal of Hospital Infection 19, 41-46
CrossRef78
Ruggero Battan, Mario C. Raviglione, Tancredi D'Amore, Ariel Pablos-Mendez, Paolo Raggi, Ravi Hedni. (1991) A Pilot Study. Aids Patient Care 5:3, 120-124
CrossRef79
Ruggero Battan, Mario C. Raviglione, Joyce Wallace, Susannah Cort, John F. Boyle, Angelo Taranta. (1991) S. aureus nasal carriage among homosexual men with and without HIV infection. American Journal of Infection Control 19:2, 98-100
CrossRef80
David N. Churchill. (1991) CAPD Peritonitis: A Critical Appraisal of Prophylactic Strategies. Seminars in Dialysis 4:2, 94-100
CrossRef81
W. M. Mawhinney, C. G. Adair, S. P. Gorman. (1991) Development and treatment of peritonitis in continuous ambulatory peritoneal dialysis. International Journal of Pharmacy Practice 1:1, 10-18
CrossRef82
Jean L. Holley, Beth M. Piraino. (1990) Complications of Peritoneal Dialysis: Diagnosis and Management. Seminars in Dialysis 3:4, 245-248
CrossRef
