Knowledge of Zoonoses Among Those Affiliated with the Ontario Swine Industry: A Questionnaire Administered to Selected Producers,Allied Personnel,and Veterinarians

Introduction

I n the swine industry, pigs are defined as domesticated livestock kept for use or product and pork is the meat product derived from a pig after slaughter (McGlone and Pond, 2002). Zoonoses are diseases caused by infectious agents that can be transmitted from animals to humans. Campylobacter coli, Campylobacter jejuni, Escherichia coli, Erysipelothrix rhusiopathiae, swine influenza virus (SIV), Salmonella enterica, Streptococcus suis, Toxoplasma gondii, Trichinella spiralis, and Yersinia enterocolitica are pathogens that have been associated with pigs, pork production, and/or the pig industry as causing occupational and/or foodborne diseases (Bahnson et al., 2001; Lee and Middleton, 2003; Schlundt et al., 2004).

Many of the aforementioned microbial hazards are a problem from a food safety standpoint; however, pork is not known to be the main carrier. For example, poultry accounted for 37% of all foodborne illnesses associated with Salmonella spp., followed by cheese (22%), eggs (11%), beef (8%), and finally, pork (4.5%) (Lee and Middleton, 2003). However, undercooked pork is the main source of human trichinellosis in the world, and in the 1970s pork accounted for 73.2% of 254 cases reported in the United States (Stewart and Hoyt, 2006). Although more recent outbreaks of trichinellosis due to undercooked pork are rare in Canada (Schellenberg et al., 2003), outbreaks still occur in other countries (Haim et al., 1997).

Conversely, some of the aforementioned microbial hazards are not a food safety issue, but are a public health concern. Recently, SIV subtype H1N1 caused illnesses and deaths in many countries around the world and was officially upgraded to a “pandemic” by the World Health Organization in June, 2009 (WHO, 2009a). Although pig to human transmission of swine influenza is rare (Olsen et al., 2002; Myers et al., 2006; CDC, 2009; Weingartl et al., 2009), close contact (defined as less than 1 m) with an infected pig or human (CDC, 2009) and/or direct contact with a surface contaminated by the agent (CDC, 2009) may result in transmission of the virus (Weingartl et al., 2009). International health officials from the Center for Disease Control, the World Health Organization, and various food organizations have reaffirmed that pork is safe to eat (CDC, 2009; WHO, 2009b). Nevertheless, swine influenza (H1N1) is a public health hazard that pig and pork industry workers should be aware of. Enhanced knowledge in this area will help to better establish effective farm-level control measures aimed at preventing the transmission of diseases from pigs and/or pork to people and vice versa (Collins and Wall, 2004).

As a result of global pandemics and other isolated outbreaks, consumer concerns over microbial hazards (Brewer and Prestat, 2002; Hrudey et al., 2003; Brewer and Rojas, 2008) such as zoonoses and antimicrobial resistance (Bahnson et al., 2001; Lee and Middleton, 2003) have increased, and food safety and public health have never been more important. In Canada, to address pork food safety concerns, pork chain stakeholders have initiated and implemented food safety programs at various stages of food production, including on-farm food safety programs, with the main goal of ensuring that pigs leaving farms are healthy and free of a variety of hazards, including zoonoses caused by Salmonella spp., T. gondii, and T. spiralis (CQA^®, 2008). Further, to improve the health of Canadians, the federal government established the Public Health Agency of Canada (PHAC) in 2004 as a result of the severe acute respiratory syndrome outbreak in 2003 (PHAC, 2008). The PHAC helps Canadians achieve better health and well-being in their daily lives by protecting against infectious diseases and other noninfectious but equally important health issues that affect the Canadian population.

To have an effective on-farm food safety program, producers need to be knowledgeable about microbial hazards. Further, other professionals such as veterinarians and other industry workers (agronomists, feed salespersons, etc.) play an important role in implementing good production and public health practices that are recommended by on-farm food safety programs such as the CQA and government agencies such as PHAC, respectively. Veterinary professionals have substantial training in infectious diseases affecting human and animal populations and their transmission within and across species and the environment. However, swine producers, agronomists, and feed salespersons may not have had the opportunity to receive similar training and their awareness of microbial hazards is unknown and likely varied. The main purpose of our study was to determine the knowledge of and attitudes toward zoonoses and other microbial hazards among producers, veterinarians, and industry personnel working in the Ontario swine industry.

Materials and Methods

Results

Discussion

Overall, it was anticipated that the veterinarians would be most familiar and producers least familiar with zoonoses. Veterinarians are taught about these pathogens through their education. Additionally, understanding the ramifications of zoonoses on animal and human health is an important part of their professional responsibility. Other occupation groups are less likely to encounter these disease hazards during their education or as part of their day-to-day work. The SPPs were likely more familiar with the selected hazards than were the RSPs because many of the pathogens had been part of the OSSP surveillance program that the SPPs took part in.

Y. enterocolitica was the least familiar hazard to all respondents, including veterinarians. The respondent's lack of familiarity with this pathogen may be because it does not usually cause clinical disease in pigs. Across all occupation groups, only one third of respondents were concerned about transmission of Y. enterocolitica from pigs or pork to people. There are associations between the consumption of pork and the human cases of yersiniosis (Ostroff et al., 1994; Satterthwaite et al., 1999; Fredriksson-Ahomaa et al., 2001) observed in Europe and the United States among individuals consuming raw-pork–based products. However, between 1996 and 1998, only 23 people in Ontario were hospitalized because of yersiniosis and from 1997 to 2001 there were no reported human deaths due to Y. enterocolitica infections in this province (Lee and Middleton, 2003). Consequently, this hazard has not received media attention like Salmonella spp., which may also explain why it is the least familiar to respondents.

Interestingly, even though many of these microbial hazards (Salmonella spp., T. spiralis, and T. gondii) are part of the CQA program, less than 25% of the RSP group was familiar with T. gondii and T. spiralis. Salmonella spp. may be familiar to this group because it is part of the CQA program, but it may also be due to media attention that this hazard has received in the past (Bahnson et al., 2001; Currie et al., 2005; Marcus et al., 2007).

As expected, producers were least likely to correctly identify all of the zoonotic hazards. Across all occupation groups, respondents were most concerned about Salmonella spp. and S. suis causing illness in people compared with all the other disease hazards listed. The questionnaire was administered after a widely publicized outbreak of serious disease in swine farm workers in China, which was eventually attributed to S. suis (Gottschalk et al., 2007), which might explain why the majority of the respondents were concerned about the spread of S. suis from pigs or pork to humans despite the fact that, to our knowledge, no human cases associated with S. suis infection have ever been reported in Canada.

Similarly, Salmonella spp. has received much media attention as one of leading causes of foodborne illness in humans in North America, and poultry is often identified as the main carrier of this microbial hazard (Currie et al., 2005; Marcus et al., 2007). Additionally, many respondents are likely aware of the swine Salmonella spp. surveillance program in Denmark that has been in place for over 1 decade (Wegener et al., 2003).

Both OSVs and AIP were least concerned about E. rhusiopathiae likely because disease as a result of this agent is rare in people (Brooke and Riley, 1999).

The producers were least concerned about Campylobacter spp. Campylobacter spp. is a common cause of foodborne illness in humans, and in Ontario, of all foodborne pathogens, it accounts for the highest annual average infection incidence rate from 1992 to 1996 (Lee and Middleton, 2003); however, the most common source of campylobacteriosis in humans is poultry (Whyte et al., 2004). Also, ileitis, a common gastrointestinal disease of pigs, was originally believed to be caused by Campylobacter spp. It is now known that the hazard responsible for swine ileitis is Lawsonia intracellularis, but some producers still refer to ileitis as “Campylobacter.” Ileitis is not known to spread from pigs to people (Michalski et al., 2006) and confusion due to the name might be why at least some producers were not concerned about the zoonotic potential of Campylobacter spp. Interestingly, Campylobacter spp. was tested for with other pathogens in 2004 as part of the OSHP program (Varela et al., 2007) and therefore it was expected that more SPPs would be concerned about the zoonotic potential of this hazard.

The differences in the proportion of SPPs and RSPs who believed their herds were positive for microbial hazards may be due to pathogen testing that was undertaken in the SPP herds as part of the OSHP program from 2001 to 2006 (Farzan, 2007). In Ontario, the herd-level prevalence of Salmonella spp. was 46% in 2004 (Poljak et al., 2006), which is higher than the prevalence reported by producers who participated in this questionnaire.

While SPP herds were not specifically tested for St. suis as part of the OSSP program, postmortem and bacteriology investigations were completed at the Animal Health Laboratory Services of the University of Guelph as part of the OSSP program. If the test was positive, the producer was informed of the presence of S. suis in their herd. Interestingly, the majority of both producer groups believed that S. suis was present in their herd; however, its prevalence is greater than that of S. suis serotype 2 (25%) reported in Canada in 2001 (Higgins and Gottschalk, 2001). The discrepancy is intriguing because the typical clinical signs of S. suis in pigs (lateral recumbency, paddling, etc.) are easily recognizable, which should make identifying cases less difficult.

From 1988 to 1989 the seroprevalence of H1N1 was 30–50% at the pig level (Chambers et al., 1991), which is similar to the prevalence estimated by Ontario producers in both groups. However, because of the 2009 H1N1 pandemic, both the reported prevalence and the producers estimated that prevalence may be higher than previously indicated.

More than half of the producers (both groups) believed that E. rhusiopathiae is present on their farm even though the prevalence has been declining since the 1950s. The prevalence was 29% in the mid-1970s in the United States (Wood, 1984). In Canada, the prevalence of E. rhusiopathiae is low as well and is thought to be attributed to routine vaccination, maintaining closed herds, using confinement housing, improved waste disposal, and using antibiotics in the feed (Wood, 1984). As the mild cutaneous infection known as an erysipeloid is visible on infected pigs it is interesting that both producer groups overestimated the prevalence of the disease agent on their farms. Perhaps because E. rhusiopathiae is routinely vaccinated against, the producer groups assumed their herds were positive.

Over 65% of both producer groups believed that their herds are positive for E. coli. Producers may be referring to pre- and postweaning E. coli, which is not a threat to humans, causes diarrhea in pigs, and is prevalent on pig farms. Other subtypes of E. coli, such as E.coli O157:H7, are zoonotic and can cause hemolytic uremic syndrome in people and is most often associated with cattle and rarely with pigs (Fairbrother and Nadeau, 2006). However, in Ontario, in early 2000, 44 herds were tested for E. coli O157:H7. Of the 44 herds that were tested, only one herd was positive for E. coli O157:H7. If producers were referring to E. coli O157:H7 their perceived prevalence was much higher than the actual prevalence in Ontario.

Y. enterocolitica, Tr. spiralis, and T. gondii were identified by producers as the least prevalent microbial hazards found in their herds. In Ontario, in 2004, the pig-level prevalence of Y. enterocolitica was 12.5% (Poljak et al., 2006). Y. enterocolitica was the least familiar to respondents. The lack of familiarity with Y. enterocolitica may also be why both groups believed that this microbial hazard was not present in their herds.

Currently, Canada's pork is considered free of Tr. spiralis (Stewart and Hoyt, 2006) because of enforced policies making it illegal to feed garbage to pigs, public health programs, and recently improved trichinoscopic and serodiagnostic techniques (Stewart and Hoyt, 2006). Producers should enforce the aforementioned good management practices to prevent Tr. spiralis in pork, and therefore, it is not surprising that they do not think it is prevalent on their farms.

The herd-level, true prevalence of T. gondii was 1.25% in Ontario in 2004 (Gadjadhar et al., 1998; Poljak et al., 2006). Producers correctly estimated the prevalence of T. gondii in their herds. The correct estimate may be attributed to enforcement of good farm-management practices, such as keeping cats out of the barn (Weigel et al., 1999), which have been recommended in Canada for many years (Smith, 1991).

There was agreement among all occupation groups that the government should pay for testing of any/all microbial hazards. It is possible that consistency in this response is due to a traditional belief that the government is in charge of meat inspection, ensuring that products of animal origin are safe for human consumption. This finding also underlines that despite widely accepted food safety paradigm based on shared responsibility of all stakeholders along the pork chain, the costs associated with monitoring and control of microbial hazards would be a major challenge for actual implementation and sustainability of specific microbial hazard-targeted on-farm programs. However, a study by Bahnson et al. (2001) showed that over half (53.4%) of 353 surveyed Illinois (United States) swine producers would be willing to implement a given hypothetical food safety practice (using a feed additive that reduced Salmonella spp. shedding), even if they did not profit from the practice.

Currently, there are global concerns about antimicrobial resistance and its negative impact on human and animal health (Rajic et al., 2004, 2007). Many health agencies, such as the PHAC and other agrifood agencies such as the CQA have initiated the development and/or expansion of existing antimicrobial surveillance programs internationally (Rajic et al., 2004). It is not surprising that more OSVs considered antimicrobial resistance a problem in Canada. The OSV group may be aware of current initiatives to monitor increasing Resistance through programs such as Canadian Integrated Program for Antimicrobial Resistance Surveillance, whose main objective is to monitor antimicrobial resistance in food animals and which has been in place since 2002 (Rajic et al., 2004).

Both producers and AIP ranked producer magazines as the most preferred source for obtaining new swine industry information, suggesting that including articles about zoonotic pathogens might be an effective method of informing large numbers of those working in the swine industry about zoonotic diseases. Veterinarians, however, preferred obtaining new information via producer meetings. To update this group of swine industry professionals about zoonoses, meetings that include speakers and discussions about zoonotic pathogens will likely be most effective. The majority of the producers indicated that farm visits by a veterinarian were a preferred source of new information, given that Ontario's swine veterinarians keep abreast of existing and emerging zoonoses and other food safety issues. The Ontario Pork webpage is also a popular mode of knowledge transfer among all occupation groups and this may be the most effective way for timely translation of information into practice for these people.

There are some limitations associated with our study. Because of limited time, resources, and funds, we chose to reduce the number of disease agents and remove the demographic information from the questionnaire. It was not possible to correct for nonresponse bias because of lack of missing demographic information (responders and nonresponders).

Further, some groups were collected by convenience sampling, which is a nonprobability sampling method. Random sampling is ideal, but it is almost always difficult and prohibitively expensive. Nonrandom sampling does limit, but does not completely rule out the possibility of gaining scientific knowledge from data contributed by a convenient sample.

Additionally, stakeholders were asked about which tests should be done on-farm. Although this is an interesting perspective from the stakeholder's point of view, their responses may be biased toward their interests.

Conclusions

The results of this questionnaire indicate that knowledge of zoonoses and other microbial hazards is relatively inconsistent among producers, allied professionals, and veterinarians working in the Ontario swine industry. Overall, stakeholder groups associated with the swine industry in Ontario appear to be more familiar with zoonoses and microbial hazards that are also relevant to pig health or have consistent and wide media coverage as a cause of human disease outbreaks. Educational efforts should focus on preferred methods (producer meetings and magazine), which may help to reduce the transmission of zoonoses and to improve pork safety in the Ontario swine industry.