Infection control knowledge, beliefs and behaviours amongst cystic fibrosis patients with epidemic Pseudomonas aeruginosa

Cheng et al. are largely recognized as identifying the first epidemic P. aeruginosa (ePA) infecting individuals with CF [ 1]. These researchers identified disproportionally high rates of ceftazidime resistance amongst P. aeruginosa isolated from their pediatric population and subsequently genotyped all isolates using molecular methodology identifying 85 % of patients harbored the same strain, the Liverpool Epidemic Strain (LES). LES has since been identified to be widespread in clinics across the United Kingdom, and in Eastern Canada [ 2– 5]. Furthermore, multiple other ePA strains have since been described in Australia, Europe and North America [ 2, 3, 6– 9].

Patients chronically infected with many of the ePA strains are associated with a worsened clinical course relative to those infected with unique, non-clonal strains. In particular, LES has been associated with increased rates of lung function decline, exacerbation frequency and progression to end stage lung disease [ 2, 10, 11]. We have recently described another ePA, termed the Prairie Epidemic Strain (PES), amongst patients attending the Calgary Adult Cystic Fibrosis Clinic. PES is unique to CF, and was not found causing infection in comparator populations of adults with non-CF bronchiectasis, or community-acquired bacteremia nor during extensive sampling of natural environmental reservoirs or the local hospital sampling [ 7, 12]. This strain was evident at first encounter amongst multiple patients transferring to our adult clinic from other Western Canadian CF clinics suggesting PES is prevalent across the Prairies [ 7]. PES was observed to exist in even the earliest samples collected in 1980 (unpublished observations), and has been identified in sequential cohorts of young adults transitioning into our clinic. Most importantly, infection with PES occurred almost universally prior to adulthood, and very few cases of super-infection were documented in an adult cohort despite prolonged follow-up [ 7]. Like LES, PES has been associated with a worse baseline lung function and nutritional status, increased rates of lung function decline and progression to end stage lung disease, and are more likely to be resistant to antibiotics [ 7, 13].

Risk factors for ePA are poorly understood. One of the major limitations is lack of historical context to determine when infections have occurred as most ePA related studies are prospective and of short duration. As we were previously able to establish infections occur generally prior to adulthood we sought to determine what behaviours and exposures associated with ePA infection. Few studies have been conducted on patient beliefs and behaviours with respect to infection control [ 14]. To date no published works have sought to determine if patients with transmissible pathogens in CF have different behaviours and beliefs that may explain their infection status and contribute to risk for spread. Accordingly we sought to prospectively assess attitudes, behaviours and beliefs amongst our clinic cohort regarding infection control to identify potential factors that may lead to lapses in infection control.

ePA infection in CF, including infection with strains such as LES and PES, have been associated with increased risk of disease progression and worsened pre-transplant survival [ 2, 13]. Accordingly, strategies to prevent transmission of ePA are of paramount importance.

Risk factors for acquisition of ePA have often been difficult to ascertain owing to uncertainty regarding timing of infection in prospective studies. As our group has previously demonstrated that ePA acquisition occurs before or shortly after adulthood [ 7], we looked to identify which past behaviours were most closely associated with ePA. Herein, we identified the greatest risk factor for ePA acquisition to be during periods of prolonged close contact such as might occur during CF camps. Indeed these camps were run through many parts of the world, and several studies report instances of super-infection of 60–100 % of attendees [ 20, 21]. These camps were also associated with outbreaks of Bcc and have largely since been abandoned for this reason [ 22]. Whereas personal involvement in past social CF fundraising was observed to associated with ePA, current non-social fundraising activities either by patients or family members was not demonstrated to be a significant factor.

Others have reported significant gaps in infection control knowledge of CF patients and family members [ 14, 23]. In a multi-center survey involving 1399 patients, only 53 % of patients understood the risks associated with socialization and social behaviours such as hand shaking (57 %) or the rationale for the 1 m bubble (67 %) [ 24]. However, herein we observed, in general our population to be quite knowledgeable. We did, however, find that patients with ePA were less likely to believe in or adhere to clinic policy against socialization. Patients may believe that the benefit of a close personal connection to other individuals with CF outweigh the potential risk of infection transmission [ 14]. Others have reported that young adults are more likely to be non-adherent to infection control standards than other age groups, and this was postulated to be related to the fact these patients grew up spanning two very different periods of CF care. Indeed, these patients were also more likely to have attended camps where socialization was previously encouraged.

Droplet nuclei containing CF pathogens including P. aeruginosa have long been known to be created by those with CF [ 25, 26]. These have been shown to be the same strains causing chronic infection and to persist in the air for extended periods. However, in the absence of information regarding minimum infectious inoculum for ePA the risk of ePA in droplet nuclei within the clinic environment is unknown. In our study, patients associated coughing with heightened risk of infection acquisition but did not equate mere talking as a risk. Indeed, many health care works and patients believe that it is during periods of illness associated with increased coughing that the greatest risk of transmission occurs [ 24]. This is not the case as others have demonstrated that the amounts of infectious droplets generated during cough were similar during periods of stability and at exacerbation [ 27]. Indeed, P. aeruginosa in droplet aerosol are even identified during tidal breathing, albeit at lower levels then during cough. While use of masks has been advocated in the recent American infection control guidelines [ 28], recent work suggests that masks do not reduce risk of infectious aerosol generation [ 29]. This raises the potential concern of false security as use of masks may be viewed as a means amongst CF patients to facilitate safer socialization.

Strategies adopted for controlling the spread of ePA are quite diverse. Those advocated include: cohort segregation (where patients infected with ePA are seen at separate clinic/hospital facilities from those without) [ 30, 31], cohort segregation with environmental controls (whereby patients with any P. aeruginosa infection were seen separately in addition to strict environmental controls including faucet filters and splash back preventing sinks), and strict patient segregation incorporating the use of gowns and masks by patients and health care workers alike [ 32]. These increasingly complex strategies have all been attributed as being responsible for reduction in transmission. However, based on our observations herein we put forth that patient segregation, preventing socialization and the basics of hand and cough hygiene are the primary means of preventing ePA. Indeed, discussions about infection control knowledge and beliefs, and critically avoiding socialization with other unrelated CF individuals need to be addressed, and become part of the annual review [ 33].

Whereas prevalence of ePA are discouragingly high across multiple clinics, incident infections with these strains remain very low when simple measures are invoked [ 2, 7]. In prospective studies, in the few instances where ePA strains have been observed to superinfect patients, social connections have been identified [ 30, 34, 35]. Discouraging socialization thusly must be prioritized as ultimately the most important and controllable means of preventing ePA transmission. However, studies have suggested that CF care providers are often unfamiliar with the importance of this strategy, or may disagree entirely, and lack confidence in encouraging this practice [ 24, 36].

Within our cohort of patients we assessed if there was an association between number of clinics attended and risk of epidemic strains. While no association was found we did observe a high frequency of patients attending multiple CF clinics, including patients who had attended CF clinics in all regions of Canada, parts of the United States, Europe and Australia. As many surveillance projects rely exclusively on screening against local epidemic strains, we must remain mindful that focused strategies such as PCR targeting local epidemic strains may be insensitive to identification of novel or new strains as new strains may become established through patient transfers [ 30].

Interventions to improve infection control as it pertains to ePA must account for the fact that social connectedness appears to be the greatest risk factor. As this group seems also to be the most inclined to socialize and thereby potentially transmit infection, strategies both discouraging face-to-face contact while supporting the desire and perceived benefit of socialization need to be recognized. In this light the use of CF “online” social networking sites offer promise provided they can be adequately supported and regulated. Indeed, “offline” face-to-face meetings do occur and peer-to-peer or external safety measures must be continually emphasized. Whereas online message boards have traditionally been the means of communication, next generation peer-peer video chat and conference call systems are being developed and hold greater promise yet [ 37]. Unfortunately, uptake within the CF community remains limited and both promotion and continued expansion of this medium to meet the evolving needs of the community are required. Furthermore, social scientists can monitor these medium enabling great insight into the CF patient population with respect to beliefs, perception, concerns and understanding how patients individualize their disease and its management [ 38]. In an environment where health care resources are increasingly limited, and ever increasingly complex and expensive infection control protocols exist we suggest that investment in online platforms to enable these connections pose great “bang for the buck”.

ePA infections are both common and associated with accelerated clinical decline. The most important risk factor for ePA infection remains peer-peer socialization, something now routinely discouraged. As patients continue to desire peer-peer support, novel strategies that enable this desire to be met are warranted. Investment in online peer-peer communication technologies represents a cost effective intervention for preventing further ePA transmission.