Journal of Clinical Nursing 1998; 4: 5-12 Review Staphylococcus aureus: a review of the literature DINAH GOULD BSc, MPhil, PRD, RGN, RNT. Lecturer, Department of Nursing § London SEI 8TX, UK ies, King’s College, Cormall House Annex, Waterloo Road, ANGELA CHAMBERLAINE RGN Research Assistant, Department of Nursing Studies, King's College, Cornwall House Annex, Waterloo Road, London SEI 8TX, UK Accepted for publication 23 February 1994 Summary + Staphylococcus aureus has a long association with nosocomial infection. Problems date from the 1950s, although methicillin-resistant Staphylococcus ‘aureus (MRSA) did not emerge until the following decade. + Initially the pathogenicity of antibiotic-resistant strains was underestimated, and is still sometimes questioned, but today most authorities consider MRSA a serious threat, especially given current preoccupation with cost-effectiveness within the health service: nosocomial infection is associated with increased expen- diture and may be regarded as a hallmark of indifferent nursing and medical care. * This review documents the emergence of MRSA and recognition of the ensuing problems throughout the 1980s and early 1990s, with suggestions for nursing activities which could contribute towards improved control. + Lessons learnt during outbreaks are seen to be of value, but there is also a need for staff at ward level to review routine practice continually so that awareness of activities likely to result in cross-infection is maintained. The use of protective clothing emerges as less important than handwashing, which may be periodically audited to maintain standards, Keywords: handwashing, infection control, MRSA, protective garments, Staphy- lococeus aureus. Staphylococcus aureus is a Gram-positive bacterium able to withstand desiccation, although unlike many other Gram- positive species, it does not form spores. It thrives in saline environments, which explains its presence as part of the normal skin flora in approximately 30% of the general pop- ulation (Thomas, 1988). Males are more often carriers than females, especially at the perineal te, but the reason for this is unknown (Ayliffe e¢ a/,, 1977). Given the correct conditions (inoculation into tissues beneath the epidermis) ‘Staph. aureus displays considerable potential as a human pathogen (Burnet & White, 1972). It is able to synthesize enzymes (coagulase, haemolysins) catalysing the conver- sion of soluble fibrinogen to insoluble fibrin. This induces blood surrounding the bacteria to clot, so they are pro- 56 D.Gould and A. Chamberlaine tected from host defence mechanisms, particularly phago- cytosis. Toxins are also produced, contributing to virulence (Mims, 1990), Staphylococcus aureus has a long association with nosoco- ant strains. It is mial infection, especially antibiotic-re now impossible to treat many serotypes with penicillin, while others display resistance to a wide range of synthetic antibiotics: methicillin-resistant Staph, aureus (MRSA), The emergence of Staphylococcus aureus as a nosocomial pathogen Gram-positive infection emerged as a problem in hospitals during the 1940s, but according to contemporary writers (Goodall, 1952) and the later archival studies of Selwyn (1991) most reported nosocomial infections initially appear to have been streptococcal rather than staphylococcal. During the 1950s staphylococci became responsible for increasing numbers of infections, especially in wounds, leading to outbreaks which received extensive comment in the medical press (McDermott, 1956); reports of penicillin resistance appearing as early as the mid-1950s (Colebrooke, 1955). The difficulty of treating and containing staphylo- coceal wound inf ntributed to government policy towards the control of nosocomial infection in the UK. In 1959 the Ministry of Health recommended the appoint- ment of a control of infection officer and committee in all acute hospitals (Worsley, 1988). Their remit was to investi- gate outbreaks and to detect cross-infection. These recom- mendations have since become statutory requirements, although the work of the infection control committee is now much wider. METHICILLI ESISTANT STAPHYLOCOCCUS AUREUS New synthetic penicillins were introduced throughout the 1960s and strains resistant to methicillin were recorded before the end of the decade (Shanson, 1985). Invariably these were also resistant to cloxacillin, fluocloxacillin and the cephalosporins, which superseded methicillin because of their better oral absorption. These antibiotics brought such dramatic improvements in the treatment of infection that the disappearance of MRSA during the 1970s was greeted with complacency (Cafferkey ef al., 1985) ‘Consequently the 1980s and 1990s have been punctuated with repeated outbreaks of MRSA throughout the world. Problems have been reported in the UK (Bradley et al, 1985), Ireland (Cafferkey et a/., 1985), Australia (Faoagali et al., 1992), the Far East (Hanifah et a/., 1992) and the USA (Thompson et al., 1982), with outbreaks reported in the acute hospital sector (Cafferkey et a., 1985) and among the chronically sick (Muder et a/., 1991). MRSA has now become an established risk of hospital admission and a problem faced by countless infection-control teams, Inevitably this has led to the question: ‘Does its presence matter?” and, if'so, then: ‘How much?” ‘The significance of methicillin-resistant Staphylococcus aureus colonization and infection Early clinical observations suggested that some strains of MRSA might be less virulent than others (Aielts et al, 1982) leading to a suggestion by Lacey (1987) that MRSA offers no greater threat than other agents associated with nosocomial infection. This author believes that, in common with many of the Gram-negative bacteria (e.g. Pseudomonas, Klebsiella, Proteus), MRSA is only weakly pathogeni Variation in ability to invade host tissues between strains has now been verified through laboratory studies (Cookson & Phillips, 1988) but Lacey’s (1987) argument is not tenable, ‘The literature is replete with accounts of outbreaks of Gram-negative infection sharing a common feature—that of problematic control despite relatively low levels of path- cogenicity (Casewell et al., 1977; Curie et al., 1978) ‘Comparisons between MRSA and Gram-ne; therefore lead to the conclusion that if the two are indeed similar, this must constitute an unfortunate parallel rather than a call to reduce infection-control efforts. Recent evi- dence emphasizes the need for stringent control. In a com- prehensive review of the literature Keane ef al. (1991) explained that evolution of staphylococeal strains of multi- ple-resistance is occurring continuously. Molecular studies indicate that numerous strains of Staph. aureus appear to have acquired resistance to methicillin so that ‘MRSA’ rep- resents a heterogeneous group of staphylococci, still responding to the selective pressures of exposure to anti- biotics, Their diversity, including variation in virulence, is explained by the different chemotherapeutic agents employed in different centres. One of their common char- acteristics appears to be ability to spread easily and this may be a factor related to virulence (Phillips, 1991). Many strains of MRSA, as well as showing epidemic potential (EMRSA), are known to be highly pathogenic. C: Hill (1986) used data from previous studies to demonstrate that under appropriate conditions MRSA could achieve full pathogenic potential, leading to overt signs and symp- toms of infection among its victims, not mere colonization as Lacey (1987) suggested. Most authorities believe that MRSA is a cause of serious concern in hospital because it contributes directly to mor- bidity and mortality (Locksley et al., 1982; Tufnell et al., 1987) and as with nosocomial infection generally, delays tive sepsisdischarge, increasing the cost of health care (Chaudhuri, 1993). Nosocomial infection rates are among the most readily quantified, valid and useful indicators of the quality of hospital care (Shaw, 1986). In the outbreak described by Locksley et al. (1982) transmission occurred from one index case admitted from another hospital to 34 patients on a burns unit. The out break continued for a period of 15 months. Twenty-s patients became infected and 17 died. Spread occurred to a neighbouring intensive care unit. ‘The account provided by Tffinell eal. (1987) detailed a longer outbreak (2.5 years) in a district general hospital involving 151 individuals. Although most were colonized rather than infected and only two patients died, morbidity ‘was considerable, taking the form of discharging wounds, otitis. media, urinary tract infections and pyrexia Unarguably, such symptoms must reduce quality of life, One patient had an eye infection, Allowing an outbreak of this nature to run its course unchecked cannot be sanctioned on humanitarian grounds. On this basis it is not possible to concur with Lacey's statement (1987) that MRSA carriage: ‘might be in groups of patients such as the elderly”. fected patients described by Tuflnell er af (1987) were elderly and many were already severely ill, but this group now forms the bulk of the population in general ‘wards. A cross-sectional incidence study employing data from 38 hospitals established that carriage of Siaph. aureus is particularly high among older patients (Ayliffe et al., 1977), especially if they have already received antibiotics. Older people frequently undergo surgery, particularly orthopaedic implantation, a procedure falling into the high-risk category. Consequences are catastrophic in the event of deep joint sepsis: infection can reduce function to levels lower than those experienced before the original operation intended to improve mobility (Scheibel et a., 1991). ‘The cost of this invalidity must also be taken into account, It is also possible to infer costs in the epidemic described by Tuffinell et al, (1987). At its height 43 cases of MRSA were reported over a period of 3 months, contribut- ing enormously to medical and nursing workload while increasing the waiting list for elective surgery. It is of course possible to treat MRSA infections, but vancomycin, the drug of choice, which undesirable side-effects, must be given by slow intravenous enucleated following severe optic noted for its recourse may lead to further antibiotic resistance (Sorrell et al., 1982), ‘The main alternative presently available is teicoplanin. ‘This appears less toxic and is easier to admin- ister but is more expensive (Davey & Williams, 1991), Other antimicrobials have been tried, notably cipro- Staphylococcus aureus 7 floxacillin, but resistance has rapidly emerged (Daum et al, 1990). Combined chemotherapy may be attempted when single therapy has failed or is thought likely to be ineffec- tive. Rifampicin and sodium fusidate have sometimes been usefull in combined regimes (Keane e¢ al., 1991). Topical application of mupirocin eradicates nasal and skin carriage which, as discussed below, frequently precedes infection in patients and occurs among staff during outbreaks, but order to preserve its value use must be restricted to avoid the emergence of resistant strains (Cookson, 1990). Its therefore possible to conclude that identifying effec tive measures to control the spread of staphylococci consti~ tutes a worth while undertaking. ‘The literature falls into two broad categories: identifying the main mechanisms of staphylococcal dissemination and describing policies and procedures which appear to contribute to containment. DISSEMINATION Knowledge of bacterial dissemination provides essential information for effective control. Not surprisingly, this aspect has generated considerable research and. continues to receive attention. Initially it was believed that dissemination occurred by the airborne route from the contaminated skin and clothing of carriers (Hare & Thomas, 1956). This theory was refuted by Ridley (1959) in a series of experiments con- ducted with preclinical medical students who, because they lacked direct patient contact, could be regarded as repre- sentative of the general population. Fourteen per cent were identified as persistent perineal carriers and the studies, taking place in a specially designed chamber, focused on these. It was shown that hands and clothing became conta- minated with bacteria during normal activities, wi could lead to transfer by direct contact. It is now accepted that in hospital wards bacteria of all kinds are disseminated mainly by direct contact, chiefly via hands, because of the frequency with which patients are touched and equipment is manipulated (Reybrouck, 1983). However, direct evidence is difficult to obtain. Larson (1988) reviewing 400 research reports between 1854 and 1986 found that other than the original work of Semmelweis (Lilenfield, 1976), evidence rests on field trials in a neonatal unit conducted by Mortimer et al. (1966). These authors established that colonized and infected infants nursed in close proximity but without direct contact to unaffected babies, failed to transfer staphylococci or streptococci despite the passage of air currents which could have carried particles between individuals. Cross-infection occurred in 439 cases when nurses caring for both groups were given no particular instructions about handwashing. Institution8D. Gould and A. Chamberlaine of a handwashing regime reduced the rate of infection by 14%. This finding is reflected in other research reports Classic studies conducted by Casewell & Phillips (1977) in an intensive care unit revealed that sterotypes of Klebsiella ‘on nurses’ hands were the same as those colonizing patients. Although this constitutes indirect evidence it is persuasive, especially as handwashing again reduced the rate of infec tion (Casewell & Phillips, 1978) Epidemiological studies suggest that for many patients with MRSA, infection originates more often in the ward via the hands of staff than in theatre (Thompson ef al., 1982). Patients themselves appeared to operate as the main reservoirs, with nurses and doctors acting as transient car- riers. This confirmed earlier retrospective analysis of casenotes undertaken by Peacock et a/. (1980). During an epidemic very sick patients succumbed to infection, usually following initial colonization, especially if they required invasive therapy such as intubation and ventilation, Cross- infection appeared to occur predominantly via the hands of staff. Studies with a slit sampler to detect evidence of air- borne ‘occurred at all, it must operate over short distances only, no more than a few feet. ‘The situation in wards is not analogous to that in more specialist hospital during orthopaedic surgery there is considerable potential for air- borne dissemination, An investigation into sources of bac- terial contamination during hip and knee replacement ‘under conventional and laminar air flow conditions demon- strated that 98% of all bacteria, including staphylococci found to be contaminating wounds, originated either from the air directly or indirectly via hands or instruments (Whyte et a/., 1982). Similarly, in burns units considerable potential for cross-infection via the air is thought to exist because intact skin is the body’s greatest barrier against invading pathogens (Hambraeuss, 1973). semination suggested that if airborne spread In. theatre environments. POLICIES AND PROCEDURES TO REDUCE DISSEMINATION Policies reported to control MRSA have shown consider- able variation according to the available facilities and cir- cumstances surrounding a particular outbreak, ranging from very aggressive to more moderate approaches (Spi 1984). Control is difficult because asymptomatic carriage can occur for long periods, and methods currently available to detect carriers are slow and insensitive, so that by the time they are recognized, outbreaks may have become established (Keane ef ai., 1991). Laboratory findings give little indication of the likely behaviour of particular strains, despite evidence discussed above that they often differ in terms of pathogenicity and the precise spectrum of anti- biotics to which resistance is shown, Other factors con~ tributing to poor control include the difficulty of persuading staff to wash hands and the paucity of facilities for isolation, especially because so many hospitals have closed isolation wards. Guidelines from the Combined Working Party of the Hospital Infection Society and the British Society for wy (1990) emphasized the need vy net practical difficulties, particularly employing and motivating staff of sufficient calibre, Resentment is likely if nurses are redeployed from other areas of the same hospital, while problems may be experienced obtaining new recruits into what will hopefully be a temporary situation (Beedle, 1993), The outbreak described by this author was eventu- ally controlled by admitting all acutely ill patients with MRSA colonization or infection to a temporary unit where they were nursed in cubicles together: distress occurred on general wards where they were confined to rooms with the door shut. The protocol recommended by the Combined Working Party in 1990 was adopted (Table 1) with regular screening (Table 2) so that patients free of infection could , but there are Table 1 Protocol for the control of methicilin-resistant Staphylococcus aureus during oubreaks recommended by the Combined Working Party of the Hospital Infection Society and the ociety for Antimicrobial Chemotherapy Report (1990) [Adaptation] 1 Daily baths for all patients in 4% chlorhexidine 2 Application of hexacholorophane powder toaxillae and groin 3 Muepirocin ointment to treat nasal carriage three times daily 4 Mucpirocin ointment for wound; perineal carriage once dai 5 Oral rifampicin and sodium fucidate to treat throat colonics and clinical infections 6 Intravenous teicoplanin for serious infections and surgical prophylaxsis ‘Table 2 Regular programme of screening for methicilin-resistant ‘Staphylococcus aureus carriage during an outbreak recommended by Beedle (1993) On admission Weekly ‘Three consecutive ‘Transfer or days after discharge treatment Hair line Hairline Hair ine Hair line Nares Nares Nares Nares ‘Throat ‘Throat ‘Throat ‘Throat Axillae Axillae Axil Axillae Groin Groin Groin Groin csut SU csu csu Perineum Perineum —Perineum Perineum, Wound Wound Wound Wound (CSU, catheter specimen of urine.be identified as quickly as possible, minimizing their stay in the designated unit. The outbreak lasted for nearly 2 years with the isolation ward in operation for 16 months, but control was eventually successful, suggesting that the pro- tocol, which could be judged as ‘aggressive’ compared to others detailed in the literature, was justified. However, the commitment of the temporary nursing workforce and the efforts of their manager to enforce the necessary high stan- dards were seen to be of key importance in this account. Authors of journal accounts frequently conclude their descriptions of an outbreak by evaluating the control mea sures instituted, but as Goetz & Muder (1992) pointed out, these are generally restricted to short-term effectiveness. Few reports of longer term struggles against MRSA have reached. public reading, However, Faoagali et al. (1992) courageously shared their experience of MRSA spanning more than a decade. Initial identification within. their 1200-bed Brisbane teaching hospital occurred in 1975. Typically 700-800 cases of colonization and infection have been reported per annum and all attempts at control have been in yain despite the efforts of an_infection-control nurse described as ‘heroic’ by her colleagues. Like Lacey (1987), whose views were considered above, these authors have questioned the value of attempting to eradicate MRSA, but unlike him, are in no doubt about the problems when it is endemi Accounts of MRSA and the lessons to be learnt from them are of value to inf clinical nurses turn when secking specific information about MRSA, but at ward level practical guidance is also required concerning the prevention of staphylococcal infection during routine nursing activities. There i ion, perhaps because they make gloomy ion-control experts to whom doubt that nurses contribute to staphylococal dissemina- tion as they can become asymptomatic carriers (Shanson, 1985), whether employed in wards, theatre or intensive care units (Na’Was & Fakhoury, 1991), Mis ions abound: the importance of handwashing to reduce dissemination by direct contact is overlooked while the value of protective clothing to reduce spread tends to be overemphasized, ‘The nursing contribution USE OF PROTECTIVE CLOTHING Aprons and gowns A review by Mackintosh (1982) concluded that research concerning protective garments for use in theatre and burns units has become specialized, resulting in the manu- facture of sophisticated garments. which are justified because patients in these high-risk environments are par- Staphylococcus aureus 9 ticularly vulnerable, but that in wards, hazards of air- borne bacterial spread from skin scales on clothes have been exaggerated. This may date from the 1960s when Speers etal. (1969), sampling nurses’ uniforms by a ‘sweep plate’ method to simulate likely opportunities for contami- nation thought to occur during ward activity, established that heavy contamination could occur, especially when wounds infected with staphylococci had been dressed. Isolation of bacteria from dresses beneath the apron implied that particles carrying staphylococci could pass through cotton weave, leading the authors to recommend, their replacement with impermeable plastic aprons. They hypothesized that friction between the apron and the edge of the bed could release ‘bursts’ of airborne staphylococci near wounds exposed during dressing changes. Babb et al. (1983) have since demonstrated that even when clothes are heavily contaminated by staphylococci released in large numbers from heavily discharging wounds, this poses minimal threat to other patients on the same ward. In these experiments plastic aprons carried fewer bacteria than cotton ones, perhaps because staphylococci cannot adhere readily'to cold, slippery surfaces and dry out more quickly. ‘Today, there appears little justification for the use of cotton gowns. A trial by Hacque & Chagala (1989) indi- cated that use by medical and paramedical staff had no effect on rates of nosocomial infection in a neonatal unit, perhaps because most. infections were endogeneous. Routine use of gowns by visitors to such units is therefore unnecessary for those who will not have direct patient contact, although in the past it has been a standard recom- mendation (Nystrom, 1981). Despite these findings the decision to replace cotton with plastic aprons is still debated (Wilson, 1990; Gill & Slater, 1991). Curran (1991) ‘emphasized the superiority of plastic aprons, pointing out that they are cheap and should be used as intended by man- ufacturers—discarded between patients or after activities which may result in heavy soiling. Masks Use of masks is similarly questioned. Early simulations of contamination after sneezing, coughing and speech demonstrated that paper masks are superior to fabric (Madsen & Madsen, 1967) but it has even with modern designs incorporating filters, efficiency is imperfect because bacteria-laden particles can escape around the sides (Davis, 1991). Use outside theatre is unnecessary and, except during high-risk operations, this may eventually be abandoned (Tunevall, 1991; Orr & Bailey, 1992), ince emerged that10D. Gould and A. Chamberlaine Hair Hair is a known source of staphylococci (Summers ef al., 1965; Noble, 1966) but a recent study has demonstrated that disposable hair coverings had no effect on bacterial air counts generated by six volunteers providing they worked under ventilated conditions (Humphreys et a/., 1991). Asa consequence the authors recommended that use of head- gear by non-scrubbed staff could be safely abandoned, although considered it advisable for the surgeon and assis- tants because of their close proximity to the operative field. ‘The combined results of the studies reviewed in this section suggest that considerable time and expense could be spared if the unjustified use of protective clothing could bbe abandoned in many areas of the hospital with the intro- duction of cheaper alternatives where protection is neces- sary. Emphasis could instead be placed on handwashing which, as discussed above, is the most important method of preventing nosocomial infection. HANDWASHING It has been suggested that nurses operate as vectors of infection because they lack motivation to wash hands (Bartzokas & Slade, 1991). This view is not supported by the results of an earlier tightly controlled study in which excessive workload and hot weather were strongly associ- ated with the number of reported neonatal staphylococcal infections (Haley & Bregman, 1982). Nurses and doctors participating in data collection were keenly aware of the need to wash hands and concerned about their inability to maintain standards when very busy. In a later study work- load emerged as an important factor influencing the number of handwashes performed, especially in conjune- tion with resources (Gould & Ream, 1993). When levels of nursing activity were very high, hand hygiene was reduced ‘except on wards where alchoholic handrub was available at the bedside, relieving staff of the need to walk to a distant sink. Other factors may contribute to infrequent handwash- ing. It has been suggested that nurses lack knowledge of bacteriology, receiving minimal instruction about tech- nique (Sedgwick, 1984). This was also confirmed in Gould’s (1993) study. Questionna nurses’ knowledge of infection control was poor, especially in relation to MRSA, although individuals with better understanding performed more handwashes during non- participant observation (P<0.04). Another variable which has so far received even less con- sideration is the unconscious behaviour of staff’ during routine clinical activities. Cookson et al (1989) observed results revealed that that during an outbreak of MRSA, staff in closest patient ccontact were inevitably those who became most heavily col- onized. Transfer from patient to nurse probably occurred via hand contamination. Nurses frequently touched their ‘own faces, especially the nose, which is a site of staphylo- coceal carriage. ‘The same unconscious behaviour was wit- nessed in the observation study by Gould (1993). In both studies staff were not only aware that they were being watched, but also knew that the aim of observation was to document occasions when cross-infection could take place, From these results it is apparent that clinical nurses would benefit from more information about infection control but that efforts should not be directed merely toward the provision of increased theory. ‘There is a need to combine theoretical input with frequent updates designed to increase awareness of opportunities for cross-infection during routine ward activities. Much could be achieved by ‘occasional audit of nursing performance with feedback to indicate where hand hygiene could be improved and when cross-infection through unconscious behaviour could have occurred. This would be effective only in a supportive atmosphere with adequate resources. ‘The value of handrub, especially when workload is high, has been clearly demonstrated. 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