Nasal Carriage as a Source of Staphylococcus aureus Bacteremia

doi:10.1056/NEJM200101043440102

Volume 344:11-16		January 4, 2001		Number 1

Nasal Carriage as a Source of Staphylococcus aureus Bacteremia

Christof von Eiff, M.D., Karsten Becker, M.D., Konstanze Machka, M.Sc., Holger Stammer, M.Sc., and Georg Peters, M.D.

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ABSTRACT

Background The consequences of infection with Staphylococcusaureus can be severe, so strategies for prevention are important.We examined S. aureus isolates from blood and from nasal specimensto determine whether the organisms in the bloodstream originatedfrom the patient's own flora.

Methods In a multicenter study, swabs for culture were obtainedfrom the anterior nares of 219 patients with S. aureus bacteremia.A total of 723 isolates were collected and genotyped. In a secondstudy, 1640 S. aureus isolates from nasal swabs from 1278 patientswere collected over a period of five years and then comparedwith isolates from the blood of patients who subsequently hadS. aureus bacteremia.

Results In the multicenter study of S. aureus bacteremia, theblood isolates were identical to those from the anterior naresin 180 of 219 patients (82.2 percent). In the second study,14 of 1278 patients who had nasal colonization with S. aureussubsequently had S. aureus bacteremia. In 12 of these 14 patients(86 percent), the isolates obtained from the nares were clonallyidentical to the isolates obtained from blood 1 day to 14 monthslater.

Conclusions A substantial proportion of cases of S. aureus bacteremiaappear to be of endogenous origin since they originate fromcolonies in the nasal mucosa. These results provide supportfor strategies to prevent systemic S. aureus infections by eliminatingnasal carriage of S. aureus.

Staphylococcus aureus is one of the most common causes of bothendemic and epidemic infections acquired in hospitals, whichresult in substantial morbidity and mortality. In U.S. hospitalsin the National Nosocomial Infections Surveillance system, S.aureus accounted for up to 13 percent of isolates recoveredfrom patients with nosocomial infections from 1979 through 1995,and the percentage has increased in recent years.¹^,² Community-acquiredinfections with S. aureus are also common.²^,³ Multidrug-resistantstrains of staphylococci have been reported with increasingfrequen-cy worldwide, including isolates that are resistantto methicillin, lincosamides, macrolides, aminoglycosides, fluoroquinolones,or combinations of these antibiotics.³^,⁴ Because glycopeptidesare the main drugs with reliable activity against methicillin-resistantstrains of S. aureus, the emergence of S. aureus strains withintermediate resistance to glycopeptides has aroused concernabout the development of strains resistant to all availableantibiotics.⁵ The severe consequences of infection with S. aureusheighten the importance of prevention. Colonized patients arethe chief source of S. aureus in hospitals.¹^,⁶ Approximately10 to 40 percent of people tested as outpatients or on admissionhave nasal carriage of S. aureus.⁷^,⁸ Colonizing strains mayserve as endogenous reservoirs for overt clinical infectionsor may spread to other patients. Several studies have shownthat elimination of carriage in the anterior nares, the principalreservoirs of S. aureus, reduces the incidence of S. aureusinfections.⁶^,⁹^,¹⁰^,¹¹^,¹²^,¹³ However, previous studies did notsystematically investigate the link between S. aureus isolatedfrom blood and S. aureus isolated from nasal specimens, takenbefore and after bacteremia was detected, with the use of modernmolecular methods. Therefore, we undertook this study to assessthe correlation between strains colonizing the anterior naresand strains in the blood of patients with S. aureus bacteremia.

Methods

Study Design

To investigate the correlation between S. aureus isolates fromthe anterior nares and S. aureus isolates from blood, two approacheswere used. First, in a multicenter study performed from November1993 to September 1994, which comprised general and intensivecare units of 32 university and community hospitals in Germany,swabs were obtained from the anterior nares of patients withS. aureus bacteremia and cultured. As defined by the protocol,the nasal cultures were obtained immediately after the isolationof S. aureus from the blood. All isolates, including those fromfoci of infection as judged on clinical grounds, were sent toone center (the University of Münster) for genotyping.In addition, each patient's physician completed a case-recordform. The completed forms were sent to the Biometrics Departmentof SmithKline Beecham, Munich, for statistical analysis. Informationcollected in the case-record forms included data that identifiedthe patient (initials, date of birth, and patient identificationnumber); location in the hospital (general ward, specializedward, or intensive care unit); the dates when blood cultures,nasal swabs, and other clinical specimens that showed growthof S. aureus were obtained; and the clinically presumed focusof S. aureus bacteremia.

Identification of S. aureus was based on conventional criteria(including the coagulase tube test and the API Staph system[ATB32 Staph, BioMérieux, Marcy-l'Etoile, France]). Inaddition, all isolates of uncertain identity were confirmedas S. aureus by testing for the S. aureus–specific nucgene by the polymerase chain reaction.¹⁴ If nasal colonizationwith S. aureus was detected, all strains, including those isolatedfrom presumed foci of infection, were collected and characterizedby pulsed-field gel electrophoresis.

In a second study, performed from June 1994 to June 1999, S.aureus–positive cultures of swabs from the anterior nareswere collected prospectively at a single center in Münster,a 1568-bed tertiary-care hospital with five intensive care units,three of which were for surgical patients. The cultured specimenswere obtained over a period of five years from patients in generalwards as well as from patients in intensive care units duringroutine surveillance and were then frozen. These S. aureus isolateswere also compared by pulsed-field gel electrophoresis withS. aureus isolates from the blood of patients in whom bacteremiasubsequently developed during the same hospital stay or a laterone at the University of Münster.

Pulsed-field gel electrophoresis was performed in one center(the University of Münster), as previously described.¹⁵Strains isolated from an individual patient were randomly placedon the same gel. They were considered clonally identical ifno differences in the band pattern were observed.¹⁶

Whether the isolates were resistant to methicillin was determinedon Mueller–Hinton agar (Difco, Augsburg, Germany) supplementedwith 2 percent sodium chloride (after incubation for 48 hoursat 30°C) and was confirmed by testing for the mecA geneby the polymerase chain reaction, as previously described.¹⁷To test for resistance to methicillin, in general, only oneisolate from each patient was studied. If one patient had clonallydifferent strains, the other strains were also tested. The multicenterstudy was approved by the ethics committee of our institution,and oral informed consent was obtained from all participatingpatients.

Statistical Analysis

Demographic characteristics were compared with the use of Fisher'sexact test (two-tailed) and the Wilcoxon two-sample test. Statisticalcalculation of the 95 percent confidence intervals for binomialproportions was performed with the SAS statistical program (version6.12, SAS Institute, Cary, N.C.). The confidence interval forthe difference between two proportions was calculated accordingto the methods of Wallenstein.¹⁸ All reported P values are two-sided.

Results

In this study, pulsed-field gel electrophoresis, an establishedmethod of molecular typing, was used to compare colonizing S.aureus strains isolated from the anterior nares, strains isolatedfrom the blood in patients with S. aureus bacteremia, and strainsisolated from the clinically presumed focus of infection. Atotal of 723 S. aureus strains, isolated from 219 patients (meanage, 54.7 years), were included in the multicenter study. Sampleswere obtained from patients in general care units (55 percent),intensive care units (27 percent), oncology or hematology units(7 percent), and other units (11 percent). Patients were mostcommonly hospitalized in internal-medicine units (59 percent)and surgical units (21 percent). A total of 219 strains wereisolated from the blood, 350 from the anterior nares, and 154from other clinical specimens. These specimens were obtainedprimarily from skin, mucous membranes, and soft tissue (48 percent);from short-term or long-term catheters (27 percent); and fromthe respiratory tract (15 percent).

The most common causes of the S. aureus bacteremia, as judgedon clinical grounds, were catheter-related infections (in 46percent of patients); osteomyelitis or skin and soft-tissueinfections such as cutaneous abscesses and cutaneous ulcerations(in 27 percent); and infections of the lower respiratory tract(in 11 percent) (Figure 1).

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Figure 1. Presumed Causes of the S. aureus Bacteremia in 156 Patients, on the Basis of Clinical Evidence.

Twenty of the 219 patients (9.1 percent) harbored methicillin-resistantstrains, of nine different genotypes. Twenty-six methicillin-susceptiblestrains, obtained from three hospitals in which no methicillin-resistantstrains were isolated from blood during the study, were comparedwith one another; these strains were all clonally different.

For most of the strains, the isolates from the blood were identicalto those from the anterior nares of the same patients (180 of219 [82.2 percent; 95 percent confidence interval, 76.4 to 87.1percent]), as well as to those from areas other than the nares(94.3 percent); identity was determined according to stringentcriteria for the evaluation of the band pattern revealed bypulsed-field gel electrophoresis. These results did not varysignificantly according to the time between sample collectionsin cases in which nasal swabs were obtained after the onsetof bacteremia (Table 1).

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Table 1. Distribution of Identical and Nonidentical Pairs of S. aureus Isolates Stratified According to the Time between the Onset of Bacteremia and the Subsequent Collection of Nasal Swabs in 219 Patients.

In the second study, conducted at a single institution, 1640S. aureus strains were isolated from nasal swabs from 1278 patientsduring a five-year period. In 74 of these patients (5.8 percent),methicillin-resistant strains of 34 different genotypes wereisolated from the anterior nares. In 14 of the patients whohad nasal colonization, including 1 with a methicillin-resistantstrain, S. aureus bacteremia subsequently developed. These ninefemale and five male patients (median age, 35 years; range,4 to 79) had a broad range of diseases and were hospitalizedin nine different units, including general care as well as intensivecare units specializing in internal medicine, pediatrics, surgery,neurosurgery, and neurology. There were no significant differencesbetween these 14 patients and the other 258 patients in whomS. aureus bacteremia developed at the University of Münsterduring the five-year period with respect to age (median, 53.5years; range, 1 to 86) or sex (103 female and 155 male patients).With regard to the proportion with methicillin-resistant strains,the rate of resistance was similar in the patients in whom S.aureus had previously been isolated from the anterior nares(1 of 14 patients [7 percent]) and in all other patients withS. aureus bacteremia (9 of 258 patients [3.5 percent]). Themethicillin-resistant strains isolated from blood representedsix different genotypes.

In 12 of the 14 patients who had nasal colonization and in whomS. aureus bacteremia subsequently developed (85.7 percent),strains isolated from the anterior nares days or months earlierwere clonally identical to the strains later isolated from theblood. In these patients, S. aureus isolates from nasal swabsthat were clonally identical to the isolates from blood wereobtained from six patients within 1 week before the onset ofbacteremia, from three additional patients within 1 month beforeonset, and from three further patients more than 3 months beforeonset (median time, 6.5 days) (Table 2). Only two patients withS. aureus bacteremia had nasal colonization with a clonallydifferent strain of S. aureus before the bacteremia developed.Figure 2 shows the results of pulsed-field gel electrophoresiswith selected isolates.

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Table 2. Distribution of Identical and Nonidentical Pairs of S. aureus Isolates Stratified According to the Time between the Collection of Nasal Swabs and the Subsequent Onset of Bacteremia in 14 Patients.

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Figure 2. Results of Pulsed-Field Gel Electrophoresis of Selected S. aureus Isolates Obtained from Nasal Swabs (Lanes 1, 3, 5, 7, 9, 11, and 13) and Subsequently from the Blood (Lanes 2, 4, 6, 8, 10, 12, and 14) of Seven Patients.
The intervals between sample collections are indicated in parentheses. DNA fragments were separated after digestion with Sma I. Lanes 1 and 2 show the results for Patient 1 (1 day); lanes 3 and 4, for Patient 2 (3 days); lanes 5 and 6, for Patient 3 (3 days); lanes 7 and 8, for Patient 4 (2 weeks); lanes 9 and 10, for Patient 5 (2 weeks); lanes 11 and 12, for Patient 6 (31 weeks); and lanes 13 and 14, for Patient 7 (60 weeks). The ${lambda}$ denotes the molecular size marker. In all patients except Patients 3 and 4, nasal and blood isolates were clonally identical.

The proportion of patients who had nasal colonization by S.aureus before clonally identical strains of S. aureus were detectedin the blood was 85.7 percent (95 percent confidence interval,57.1 to 98.2 percent). The 95 percent confidence interval forthe 3.5 percentage point difference in this proportion betweenthe two parts of our study (82.2 percent in the first, multicenterstudy and 85.7 percent in the second, five-year study) was –22.4to 14.7 percent. Thus, the results of the multicenter studydemonstrating that nasal and blood isolates are clonally identicalin about 82 percent of patients with S. aureus bacteremia wereconfirmed by the second study, in which about 86 percent ofthe patients were colonized in the anterior nares by the sameclone that was subsequently isolated from the blood. Hence,it can be stated with 95 percent confidence that at least 50percent of the patients with S. aureus bacteremia were firstcolonized in the anterior nares by an identical strain.

Discussion

The anterior nares are reservoirs for S. aureus. Mucin appearsto be the critical surface that is colonized in a process involvinginteractions between staphylococcal protein and mucin carbohydrate.¹⁹The role of interference by other commensal bacteria, secretoryIgA, or specific staphylococcal adhesins is unknown. Three patternsof carriage can be distinguished, although the criteria usedto identify these patterns have been inconsistent.¹^,⁸^,²⁰ First,approximately 20 percent of healthy people almost always carrya strain. Second, a large proportion of the population (approximately60 percent) harbors S. aureus intermittently, and the strainschange with varying frequency. Third, only a minority of people(approximately 20 percent) almost never carry S. aureus.¹^,⁸^,²¹Persistent carriage is more common in children than in adults,and the carrier type changes in many people between the agesof 10 and 20 years.²²

Carriage of S. aureus in the nose appears to play a key partin the pathogenesis of infection. Nasal carriage has been associatedwith an increased risk of infection in patients after surgery,in patients receiving continuous ambulatory peritoneal dialysis,and in patients receiving hemodialysis.⁶^,⁷^,¹³^,²³^,²⁴ In a studyof the epidemiology of S. aureus infections in patients receivinghemodialysis, Ena et al. investigated 12 infections in threepatients and reported that 11 of these infections were causedby isolates previously identified in surveillance studies.²⁵Luzar reported that 45 percent of the patients she studied werenasal carriers before catheters were inserted. Catheter exit-siteinfections occurred at a rate of 0.4 episode per patient peryear in carriers but less frequently in noncarriers (0.1 episodeper patient per year).²⁶ Nasal carriage of S. aureus was a riskfactor for the development of nosocomial bacteremia during anoutbreak of methicillin-resistant S. aureus in an intensivecare unit, with rates of bacteremia of 38 percent for carriersof methicillin-resistant strains, 9.5 percent for carriers ofsusceptible strains, and 1.7 percent for noncarriers.²⁷

In several studies, the elimination of nasal carriage reducedthe incidence of S. aureus infections.¹⁰^,¹²^,¹³^,²⁸ Kluytmanset al. observed a significant reduction in the rate of surgical-woundinfection after intervention with mupirocin nasal ointment.⁹Nasal treatment with mupirocin led to a reduction by a factorof four in the incidence of S. aureus bacteremia per patient-year(from 0.097 to 0.024 episode) in carriers receiving hemodialysis.¹¹When the nares were treated topically to eliminate nasal carriage,S. aureus usually disappeared from other areas of the body.²⁹^,³⁰^,³¹In patients receiving hemodialysis, 87 percent of those whocarried S. aureus in their nares and on their hands carriedthe same strain at both sites.³⁰ Treatment with topical mupirocin,which eliminates nasal carriage, also eliminates hand carriage.²⁹The proposed mechanism of pathogenesis for a number of endogenousinfections is the colonization of the skin from the anteriornares, which causes subsequent infection in patients with areasof impaired skin, such as patients receiving dialysis and patientswith intravascular catheters.

Although nasal carriage of S. aureus has been suggested as thesource of subsequent infections, previous studies were limitedto single hospitals²³^,²⁴^,²⁵^,²⁷^,²⁸^,³² or to defined patient groups— such as patients receiving hemodialysis,¹⁰^,¹²^,¹³^,²⁵patients in intensive care units,²³^,²⁷^,³² or patients infectedwith the human immunodeficiency virus²⁴^,³³ — or they wereperformed in the setting of an outbreak with methicillin-resistantstrains.²⁷^,³² In addition, in most studies, typing systems ofhigh discriminatory power were not systematically used to showthat the strain colonizing the anterior nares was identicalto the strain from the focus of infection, the strain from theblood, or both and thus to support the hypothesis that S. aureusbacteremia is of endogenous origin.⁷^,⁹^,¹⁰^,¹¹^,¹²^,¹³^,²⁴^,²⁵^,²⁸

Modern methods of molecular typing, which have high discriminatorypower and which differentiate among strains isolated from multiplesources in one patient, are essential to studies of the originof S. aureus bacteremia.³⁴^,³⁵ We systematically used pulsed-fieldgel electrophoresis in a large multicenter study to determinewhether there was identity between S. aureus strains isolatedfrom blood and those isolated from the anterior nares beforeand after the detection of bacteremia. In the large majorityof patients with S. aureus bacteremia, the isolate from bloodwas identical to that from the anterior nares. Strains isolatedfrom blood cultures and from nasal-swab cultures were clonalin 82.2 percent and 85.7 percent of patients, as shown by pulsed-fieldgel electrophoresis in the two studies. Thus, a substantialproportion of cases of bacteremia may be caused by endogenousstrains of S. aureus.

In summary, in patients with S. aureus bacteremia there is astrong correlation between strains colonizing the anterior nares,strains isolated from foci of infection, and strains isolatedfrom blood, suggesting that S. aureus bacteremia may have anendogenous origin. Our results provide evidence that strategiesto interrupt transmission of S. aureus by the elimination ofnasal carriage may prevent systemic S. aureus infections.

Supported by a grant from SmithKline Beecham, Munich, Germany,and conducted under the auspices of the Paul Ehrlich Society(Staphylococcus Working Group) and the German Society for Hygieneand Microbiology (Hospital Hygiene Working Group).

We are indebted to A. Heinecke and W. Köpke at the Institutefor Medical Informatics and Biomathematics, University of Münster,for statistical advice; to M. Herrmann and B. Sinha for helpfuldiscussions; and to M. Brück, U. Hörling, S. Weber,and M. Schulte for expert technical assistance.

^* Participants in the study group are listed in the Appendix.

Source Information

From the Institute of Medical Microbiology, University of Münster, Münster (C.E., K.B., G.P.); and SmithKline Beecham, Munich (K.M., H.S.) — both in Germany.

Address reprint requests to Dr. von Eiff at the Institute of Medical Microbiology, Westf älische Wilhems-Universität Münster, Domagkstr. 10, 48149 Münster, Germany, or at eiffc{at}uni-muenster.de.

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Appendix

In addition to the authors, the following were participantsin the study group: D. Bitter-Suermann, Hannover; W. Ehret,Augsburg; P. Emmerling, Munich; F. Fehrenbach, Berlin; H. Finger,Krefeld; H. Freiesleben, Hamburg; D. Fritsche, Ludwigshafen;H. Hahn, Berlin; J. Heesemann, Munich; U. Hoeffler, Düsseldorf;H.-M. Just, Nuremberg; E. Kühnen, Trier; H. Langmaack,Berlin; R. Laufs, Hamburg; R. Lütticken, Aachen; R. Marre,Ulm; W.A. Müller, Magdeburg; B. Neuhaus, Münster;M. Röllinghoff, Erlangen; G. Ruckdeschel, Munich; J. Sander,Hannover; G. Schroeter, Stuttgart; P. Shah, Frankfurt; W. Sietzen,Hamburg; H.G. Sonntag, Heidelberg; E. Straube, Jena; R. Tauchnitz,Leipzig; U. Ullmann, Kiel; H. Werner, Tübingen; H. Wolf,Regensburg; and P. Wutzler, Erfurt — all in Germany.

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