One novel finding from this thesis, was that most gastroenteritis in LTCF residents was outbreak-associated. In the longitudinal surveillance study (Chapter 7), I estimated that 96% of all gastroenteritis cases were part of outbreaks. The author of the editorial (Appendix) responding to my publication regarding LTCF outbreak
surveillance (Chapter 10) was surprised by this finding [9].
The studies I present in this thesis show the commonness of outbreaks in LTCF. From national outbreak surveillance, I estimated that Australian facilities could expect to experience at least one outbreak every four years. This may be an under-estimate, given that I analyzed data from early years of surveillance when surveillance reporting may not have been as complete. In addition, Australia experienced a large increase in reported outbreaks of noroviruses in LTCF in 2006 due to introduction of novel pandemic GII.4 strains of this virus [27]. Given the comparison between the incidence of outbreak-associated gastroenteritis (0.07 episodes per person per year) and
longitudinal surveillance (0.23 episodes per person per year), it is likely that for every case in an LTCF reported as part of outbreak surveillance there are another two that are not reported, which is consistent with studies in other countries [28, 29]. However, due
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concern, surveillance for outbreaks in LTCF is more complete than for any other setting where outbreaks occur, such as restaurants, caterers, sporting events and private homes.
Predominance of norovirus
I identified that noroviruses were the most common cause of outbreaks in these facilities, which was consistent with findings from other countries [29-31]. Public health investigators often consider these outbreaks of noroviruses as spread from person-to-person, but given the low dose required to establish infection these viruses probably transmit from a variety of sources in closed environments, making the mode of transmission very hard to truly establish [9, 32]. The predominance of norovirus as a cause of gastroenteritis outbreaks was quite staggering, with norovirus responsible for up to half of all outbreaks occurring in LTCF. There are several reasons why elderly residents might be more likely to become infected through outbreaks than people in the community:
• possible declines in secretory immunity to norovirus in the gut, which has shown to be protective against infection [33-35],
• living in close quarters to other people, which may increase the risk of acquiring gastroenteritis,
• close contact with many carers, some of whom have intimate contact with many residents, such as bathing, dressing and feeding,
• environmental persistence of norovirus and lack of an effective disinfectant [34], and
• constant movement of staff from different facilities and other healthcare institutions [36].
A key problem for transmission of norovirus is where staff who are ill attend work and spread infection to other residents and staff [37]. This appears to be common, and in this thesis I have shown that LTCF staff members were commonly infected in the longitudinal surveillance I report in Chapter 7 and outbreak surveillance in Chapter 10. Not only is there lost productivity from a poorly functioning employee working while
Discussion & Conclusions ill, but there is also the possibility of an outbreak occurring in the facility, which are exceedingly difficult to control [37].
From this thesis, it is clear that a key research need to prevent gastroenteritis in LTCF residents is to identify robust interventions for noroviruses. Currently there are no treatment or vaccination options for gastroenteritis due to norovirus and the disease is generally mild [35]. The best approach to this vast problem of outbreaks in facilities is to establish procedures to manage these incidents, which are inevitable. Norovirus outbreaks are predominantly spread from one infected person to another and are a global phenomenon wherever there are institutions housing the aged or people gather in close proximity [34, 35, 38-40]. The occurrence of outbreaks of gastroenteritis in LTCF should not necessarily be viewed as a failure of infection control, but as a challenge to deal with the spread of these highly infectious viruses [34, 38, 41, 42].
To date, there has been one intervention trial for noroviruses in LTCF in the Netherlands, although this did not succeed in identifying suitable controls due to contamination of the control arm of the study [43]. The study did highlight some key measures that appeared to improve outbreak control, including implementing
interventions within 3 days, and measures to reduce aerosol transmission and
contamination of surfaces [43]. A recent study in the United States found that LTCF using alcohol-based hand washes were at higher risk of experiencing norovirus
outbreaks [41]. The retrospective cross-sectional survey was potentially subject to bias, as the investigators excluded one third of facilities reporting an outbreak that was not confirmed as norovirus, and were unable to confirm whether hand washing using alcohol or soap and water was conducted in any of the facilities [41]. Sandora et al.
conducted a cluster-randomized trial in school-children examining the effect of alcohol- based hand washing and cleaning with quaternary ammonium wipes and found that the intervention significantly lowered both absenteeism due to gastroenteritis and
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Foodborne disease outbreaks
Prior to this study, reliable information on the relative frequency of food- and waterborne outbreaks in these facilities was unavailable, particularly for Australia. I have shown that classic point-source outbreaks of foodborne disease in LTCF were rare, but have severe consequences when they do occur (Chapter 11). Salmonella was the most common cause of foodborne disease outbreaks and resulted in a case fatality ratio of approximately 6.1%. Clostridium perfringens was the next most common agent causing foodborne outbreaks. It was surprising to identify multiple outbreaks of diarrheal illness due to suspected toxins in LTCF residents as part of the longitudinal surveillance of gastroenteritis in LTCF residents (Chapter 7). Toxin-mediated illnesses due to C. perfringens are probably under-recognized as a cause of disease in residents, as they can be very mild in presentation [45]. Given that most outbreaks in LTCF are due to viral agents, it is common for public health investigators to assume that all outbreaks of gastroenteritis are due to noroviruses. However, it is likely that outbreaks of toxin-mediated illness are easily distinguished from viral agents by features of the outbreak, in terms of presenting symptoms, duration of the outbreak, ratio of staff to residents affected and duration of symptoms [46]. This is an area that requires further research, as it would greatly assist public health staff and facility managers to identify outbreaks that are high-priority for follow-up and investigation.
Absence of C. difficile
It was surprising not to identify Clostridium difficile as a problem for elderly people living in Australian LTCF. Internationally, C. difficile has been cited as a common cause of diarrhea and resulting in severe complications in LTCF residents [9, 47]. One of the main reasons that I would not have identified outbreaks or cases of C. difficile in the studies I conducted was that Australian laboratories rarely test for C. difficile, unless it is specifically requested on pathology request forms [48]. There were several outbreaks in national outbreaks surveillance data (Chapter 10) where C. difficile
was detected in stool of residents affected as part of outbreaks, although these were usually single stool specimens positive and there were often other pathogens, such as norovirus, isolated from multiple specimens [49]. Things are changing in regard to
Discussion & Conclusions testing for C. difficile in Australian hospital patients and LTCF residents, due to
increasing awareness about new highly virulent strains [48].
The northern hemisphere has experience a rising incidence of a particularly virulent strain of C. difficile, designated Polymerase Chain Reaction (PCR) ribotype 027 or North American pulsed-field type 1 (NAP1) [48, 50]. Recently, Australian
investigators have identified cases of this new strain, some of which have clustered in LTCF [51, 52]. As a result of increased awareness among Australian clinicans, there will be an increase in the number of cases recognized in LTCF residents, although there is much to be learned of the epidemiology of C. difficile-associated disease in Australia. One of my recommendations from longitudinal surveillance in Chapter 7 was that future studies of gastroenteritis in LTCF should include extensive microbiological work-up of fecal specimens, which would improve our understanding about the etiological agents responsible for disease in residents, including C. difficile.
Impact of outbreaks
The cost of outbreaks in LTCF can be very high, particularly costs due to
isolation of the facility [53]. Piednoir et al. estimated that the direct costs of an outbreak of rotavirus affecting 63 LTCF residents was €17,959, equating to approximately AUD$23,155 or AUD$368 per case [53]. One quarter of the cost was estimated as medical treatment and investigation, another quarter for isolation, one third for staff costs, and the remainder for bed-day loss [53]. From the surveillance of outbreaks presented in Chapter 10, I found that rotavirus outbreaks affected fewer people than many other etiological agents and were of shorter duration. To obtain a crude estimate of the cost of outbreaks in Australia, it is possible to apply the cost per case from Piednoir et al. to the number of people affected in the six-years of national outbreak surveillance (Chapter 10), which would equate to approximately AUD$31 million, or AUD$5.2 million annually [53].
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Causes of foodborne disease
In this thesis, I have established the basic causes of foodborne diseases in elderly people living in LTCF and the community, in terms of etiological agents and some risk factors. From Chapter 9, it is clear that the most common agent potentially transmitted by food affecting elderly people was Campylobacter, followed by Salmonella. In Australia, rates of both these infections are high in comparison to other developed countries, such as Europe and the United States [54-56]. In terms of public health importance, listeriosis has one of the highest case fatality rates of any foodborne infection [25, 57, 58]. In European countries the rate of listeriosis cases in people >60 years of age have increased in recent years, which is in contrast to the United States where infection rates have been declining, along with consequent mortality [26, 57, 59, 60]. I did not find that there was a significant change in rates of listeriosis over time in Victoria (Chapter 9). From longitudinal and outbreak surveillance, I propose that C. perfringens is a common cause of foodborne intoxication in elderly people living in LTCF, but is under recognized. In the second Infectious Intestinal Diseases (IID2) study conducted in the United Kingdom, the rate of C. perfringens intoxication in the general population was higher than that of Salmonella infection [8]. Information on the
incidence in elderly people from the IID2 study has not yet been published.
In the two community surveys (Chapter 8), I identified some risk factors for gastroenteritis and foodborne disease in elderly people, including travel and use of acid- suppressive medication. Use of acid-suppressive medication is a risk factor for a variety of foodborne infections, so it was not surprising to find it as a risk factor for
gastroenteritis [61]. Travel is well-recognized as a risk factor for gastroenteritis, and specific foodborne infections, such as campylobacteriosis [62, 63]. In these surveys, not only was international travel a risk factor, but travel within the State was a risk factor as well. As a consequence of the low incidence of gastroenteritis in elderly people, this study was under-powered due to very few elderly cases. I was not able to explore demographic or social risk factors for illness. Despite this, the study is one of the first that specifically examines risks of gastroenteritis in elderly people.
Discussion & Conclusions Information arising from outbreaks of foodborne diseases can provide robust evidence for development of food safety policy [64]. It is important to recognize that food sources are very difficult to identify in these facilities, due to the poor or absent recall of residents about what food they had eaten. I showed that foods that were milled or pureed were the cause of 12% of foodborne outbreaks in LTCF during the eight years of surveillance. Pureed food as a cause of disease in LTCF residents has been noted before, but is probably more important than first realized [65, 66]. In recent years, Australian health departments have reported a general increase in egg-associated outbreaks of Salmonella, which I also observed in LTCF residents. Surprisingly, I identified three waterborne outbreaks in LTCF residents, all of which were suspected to be caused by contaminated rain water tanks.
Preventing disease in the elderly
Kendall et al. reviewed the epidemiology of foodborne disease in the elderly and provided key food safety advice for elderly people [61]. These recommendations
included: avoidance of raw or undercooked high-risk foods, consuming pasteurized milk and fruit juices, careful attention to kitchen hygiene, proper storage of foods and washing of fresh produce [61]. Despite the efforts of food safety agencies to promote safe food handling to vulnerable populations, there are numerous reports in the literature that elderly people still eat foods considered high-risk [24, 58, 67]. Elderly people are a difficult target group for food safety prevention messages, and may require special approaches on specific issues [68]. Many of the host factors that may predispose older people to infection, such as use of acid-suppressive medication or immunosupression, are not ameliorable through health promotion, making it more important to alert clinicians to their role in disease prevention.
With the exception of salmonellosis and listeriosis, the incidence of foodborne infections in elderly people is lower when compared to younger people. Listeriosis is one disease where incidence increases with age, and age is an independent risk factor for infection regardless of whether the person is immune-compromised or not [57, 69]. Despite this, there are only 60–70 non-perinatal cases of this opportunistic infections
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[70]. Food safety agencies, including those in Australia, have devoted specific attention to preventing these serious infections, including consumer advice and legislative
approaches. However, in an Australian case control studyof listeriosis, host factors were the most important predictors of infection and a high proportion of cases and controls ate foods considered high-risk [24]. In terms of listeriosis prevention, efforts are probably best focused on industrial production and processing of foods, rather than concentrating on health promotion measures.
Food service staff in residential care and hospitals can have relatively poor knowledge of food safety and the principles of Hazard Analysis Critical Control Points (HACCP) [71-74]. There is little published information on food safety in LTCF in Australia, although most State and Territory governments have introduced legislation incorporating a national food safety standard for vulnerable populations that is based on HACCP [75]. From my analysis of foodborne outbreaks in LTCF in Chapter 11, it is clear that LTCF should not feed residents dishes containing raw or undercooked eggs. There is a need to better understand how blenders are used to puree food in LTCF. LTCF should not use rainwater tanks as a drinking water supply, unless there is a scheduled program of disinfection and maintenance.