Knowledge and attitudes towards food safety among Canadian dairy producers

Preventive Veterinary Medicine 94 (2010) 65–76

Contents lists available at ScienceDirect

Preventive Veterinary Medicine journal homepage: www.elsevier.com/locate/prevetmed

Knowledge and attitudes towards food safety among Canadian dairy producers I. Young a,b,*, S. Hendrick c, S. Parker c, A. Rajic´ a,b,c, J.T. McClure d, J. Sanchez d, S.A. McEwen a a

Department of Population Medicine, University of Guelph, Guelph, Ontario, Canada Laboratory for Foodborne Zoonoses, Public Health Agency of Canada, Guelph, Ontario, Canada c Department of Large Animal Clinical Sciences, University of Saskatchewan, Saskatoon, Saskatchewan, Canada d Department of Health Management, University of Prince Edward Island, Charlottetown, Prince Edward Island, Canada b

A R T I C L E I N F O

A B S T R A C T

Article history: Received 16 May 2009 Received in revised form 5 November 2009 Accepted 5 November 2009

The Canadian dairy industry has recently begun implementing an on-farm food-safety (OFFS) program called Canadian Quality Milk (CQM). For CQM to be effective, producers should be familiar with food-safety hazards in their industry and have an adequate understanding of on-farm good production practices that are necessary to ensure safe food. To assess their knowledge and attitudes towards food safety, a postal questionnaire was administered to all (n = 10,474) Canadian dairy producers enrolled in dairy herdimprovement organizations in 2008. The response rate was 20.9% (2185/10,474). Most producers (88.7%) reported that they or their families consume unpasteurized milk from their bulk milk tanks and 36.3% indicated that consumers should be able to purchase unpasteurized milk in Canada. Producers who reported completion of a dairy-health management course (OR = 0.74, 95% CI: 0.60, 0.92) and participation in CQM (OR = 0.79, 95% CI: 0.64, 0.97) were less likely to support the availability of unpasteurized milk for consumers, while organic producers (OR = 2.10, 95% CI: 1.27, 3.47), younger producers (aged <30) and producers with smaller herds were more likely to favour this practice. Two-thirds of producers (66.7%) were concerned that antimicrobial resistance (AMR) might preclude successful treatment of sick cattle. Producers who completed a dairyhealth management course (OR = 1.37, 95% CI: 1.11, 1.69), organic producers (OR = 2.00, 95% CI: 1.09, 3.69) and producers from Quebec compared to each other province were more likely to indicate concern about AMR. Most producers reported that Salmonella (74.2%) and Escherichia coli (73.0%) could be transmitted through contaminated beef or milk to humans, while most were not sure or did not think that Brucella (70.3%) and Cryptosporidium (88.5%) could be transmitted via these routes. Most producers did not perceive that any type of farm visitor has a high risk of introducing infectious agents into their herds. Producers rated veterinarians as very knowledgeable about OFFS (90.9% answered 4 or 5 on a five-point scale) and a favoured (73.1%) source of information about food safety. In contrast, only 13.2% and 30.2% of producers, respectively, indicated that consumers and government personnel are knowledgeable about OFFS. Targeted continuing education for dairy producers in Canada should address the major gaps in knowledge and attitudes towards food safety identified in this study, and veterinarians should be included as key knowledge-transfer informants. ß 2009 Elsevier B.V. All rights reserved.

Keywords: Food safety Questionnaire Dairy producers Knowledge Attitudes

* Corresponding author at: Laboratory for Foodborne Zoonoses, Public Health Agency of Canada, 160 Research Lane, Unit 206, Guelph, ON, Canada N1G 5B2. Tel.: +1 519 826 4067; fax: +1 519 826 2367. E-mail address: [email protected] (I. Young). 0167-5877/$ – see front matter ß 2009 Elsevier B.V. All rights reserved. doi:10.1016/j.prevetmed.2009.11.010

66

I. Young et al. / Preventive Veterinary Medicine 94 (2010) 65–76

1. Introduction In Canada, approximately 11 million cases of foodborne disease occur each year, and acute gastroenteritis is estimated to cost CAD $3.7 billion annually (Thomas et al., 2008). Dairy cattle are an important reservoir of Campylobacter, Salmonella, Shiga toxin-producing Escherichia coli (STEC), Listeria monocytogenes and other bacterial pathogens that can cause foodborne disease. These pathogens have been recovered with various frequencies from dairy-cattle faeces, bulk milk tanks and the dairy-farm environment (Jayarao and Henning, 2001; Murinda et al., 2002; Van Kessel et al., 2004; Srinivasan et al., 2005; Karns et al., 2007). Although most milk sold for public consumption in North America is pasteurized, outbreaks due to the consumption of unpasteurized milk (Peterson, 2003; Centers for Disease Control and Prevention [CDC], 2007; Denny et al., 2008), inadequately pasteurized milk (Fahey et al., 1995) and cheeses made from unpasteurized milk (Honish et al., 2005; CDC, 2007) continue to occur. Antimicrobial residues and antimicrobial-resistant bacteria from milk and milk products can also pose potential health risks to consumers (Katz and Brady, 2000; Straley et al., 2006). International authorities have recommended an integrated, farm-to-fork approach to ensuring safe food (OIE Animal Production Food Safety Working Group, 2006). Accordingly, major livestock commodity groups in Canada developed their own on-farm food-safety (OFFS) programs that are partially based on hazard-analysis critical controlpoint (HACCP) principles (Rajic´ et al., 2007). The Canadian dairy industry’s program, called Canadian Quality Milk (CQM), is currently in the implementation stages, with mandatory producer registration deadlines that vary by province and range from 2007 in Prince Edward Island (PEI) to 2012 in Quebec (Dairy Farmers of Canada, 2007; Rajic´ et al., 2007). Successful implementation of CQM requires that dairy producers are aware of the food-safety hazards associated with their industry and their role in ensuring safe food production. Previous research in the USA has shown that dairy producers are knowledgeable about Salmonella and concerned about antimicrobial resistance (AMR) and antibiotic residues but lack knowledge of Listeria and the health risks of consuming unpasteurized milk (Wilson, 1998; Vanbaale et al., 2003; Hoe and Ruegg, 2006; Jayarao et al., 2006; Raymond et al., 2006). These issues have never been investigated among Canadian dairy producers. Our study objectives were to describe the knowledge and attitudes of dairy producers in Canada towards various microbial food-safety issues using a postal questionnaire administered in the early stages of CQM implementation. We also evaluated associations between producer characteristics and their attitudes towards the consumption of unpasteurized milk and AMR. 2. Methods

practices (GPP) by dairy producers in Canada (supplementary online material). Initial questions were developed by authors J.S. and J.M., and feedback was received from five bovine clinicians at the Atlantic Veterinary College, Canada. The questionnaire was then administered as a pilot survey to 26 bovine practitioners in Canadian Maritime provinces in 2006. Based on these results, questions were further modified by authors A.R., S.H. and S.P. and a research assistant to reflect producers as a target population, and a pre-test was conducted with four veterinary-medicine students at the Western College of Veterinary Medicine, Canada, two of whom had a background in dairy production. The average time of completion was 15 min. Ambiguous or confusing questions were revised as needed. The questionnaire was translated to French by a veterinary student at the Western College of Veterinary Medicine, and the translation was reviewed and corrected by two additional bilingual veterinary students and a parasitologist. Some additional grammatical corrections were made prior to administration by the dairy herd-improvement (DHI) organization for Quebec and Atlantic Canada (Valacta). Our questionnaire consisted of four sections: ‘demographics’, ‘CQM program’, ‘GPP’ and ‘food-safety knowledge and attitudes’. Due to the broad scope of the questionnaire, the focus of this paper is limited to the ‘demographics’ and ‘food-safety knowledge and attitudes’ sections. Results from the other two sections are reported in a companion article (Young et al., 2010). Demographic questions included herd size, gender, age group, organic status, province and whether courses were completed in dairy-health management or food safety. The knowledge and attitudes section consisted of 10 multiple-choice questions related to testing for zoonotic pathogens (n = 1 question); AMR (n = 3); unpasteurized milk consumption (n = 2); communication preferences to receive new information about food safety (n = 1); perceived knowledge about food safety (n = 1); whether eight different microbial agents can be transmitted through beef or milk to humans (n = 1) (including established zoonotic agents, e.g. Salmonella, a possible but not confirmed zoontic agent, Mycobacterium avium subsp. paratuberculosis [MAP], and a non-zoonotic agent, bovine viral diarrhoea virus [BVD]); and the most important stage in the production chain to control six different microbial or chemical agents (n = 1). Five questions were formatted as tables with a five-point rating scale, in which producers were asked to indicate the knowledge of six different stakeholder groups about food safety (from ‘know little’ to ‘know a lot’), the likelihood that seven various types of farm visitors could introduce infectious agents into their herd (from ‘not’ to ‘very’ likely), their concern about four different microbial agents (from ‘not’ to ‘very’ concerned) in terms of possible negative economic impacts and whether consumers could become ill, and the usefulness of 16 different dairy-industry programs and initiatives to ensure safe milk (from ‘not’ to ‘very’ useful). Space was provided at the end of the questionnaire for additional comments.

2.1. Questionnaire design

2.2. Questionnaire administration

We developed a questionnaire to assess the knowledge and attitudes towards food safety and use of good production

The questionnaire was mailed to all dairy producers participating in DHI organizations in Canada in 2008

I. Young et al. / Preventive Veterinary Medicine 94 (2010) 65–76

(n = 10,474), representing 75% of all dairy producers in the country (Canadian Dairy Information Centre [CDIC], 2009). The mail-out consisted of a questionnaire along with a cover letter and pre-stamped, self-addressed return envelope, followed by a reminder letter. Canada’s two DHI organizations, CanWest DHI and Valacta, administered the mailings. In Alberta, British Columbia, Manitoba, Ontario and Saskatchewan, questionnaires and reminder letters were mailed from January 11 to March 14 and March 15 to May 2, 2008, respectively. In New Brunswick, Newfoundland and Labrador, Nova Scotia, PEI and Quebec, questionnaires and reminder letters were mailed from February 20 to March 26 and July 14 to August 26, 2008, respectively. As an incentive, producers could fill out a ballot for eight separate cash draws of $100. The ballots were detached from the questionnaires before data entry to keep responses anonymous. The questionnaire was administered in English in all provinces except Quebec and in French-speaking regions of Ontario and New Brunswick, where the French version was sent. This study received ethical approval from the University of Saskatchewan Behavioural Research Ethics Board (Protocol #07-263). 2.3. Data entry and analysis Questionnaire responses were entered into an electronic database (Access 2003, Microsoft Corporation, Redmond, WA), and entry-validation checks were performed on all questionnaires by manually comparing the database and hard-copy versions. Open-ended French responses were translated to English, and all comments and ‘other’ responses were coded in Microsoft Access. Extra categories were created if several respondents identified a particular ‘other’ response. In the interest of space, only comments with a frequency of 10 are summarized in this paper. For each variable, frequency tabulations were calculated using complete cases only. To assess the representativeness of the responses, a one-sample t-test was used to compare the average herd size of respondents in each province with the DHI averages (CanWest DHI, 2009). Significance was set at p < 0.05. We used logistic regression to evaluate the effect of various producer demographics on whether they reported: the consumption of unpasteurized milk by themselves or their families (yes = 1/no = 0; model 1), that consumers should be able to purchase unpasteurized milk (yes = 1/ no = 0; model 2), and that it is harder to treat sick cattle successfully due to AMR (yes = 1/no = 0; model 3). For all three models, predictors evaluated were: province; producer age and gender; herd size; organic status; CQM participation status; perceived knowledge of food safety; and whether courses were completed in dairyhealth management or food safety. In addition, whether producers reported the consumption of unpasteurized milk was evaluated as a predictor for models 2 and 3. We searched for associations between each pair of predictors using chi-square tests (or Fisher’s exact test if any cell values had <5 observations); p-values of <0.05 were considered statistically significant.

67

A manual backward-selection procedure was used to build each model. All predictors with a significant unconditional association with the outcome in univariable logistic regression models, using Wald tests at p < 0.2, were used to build multivariable models. Variables were retained in multivariable models if p < 0.05 using likelihood-ratio tests. All variables that had a significant univariable association with the outcome or any predictors in the final models were re-evaluated for significance in the final models and assessed for confounding (changes of >20% in the coefficients of other predictors). Two-way interactions were investigated between all variables in the final models. Herd size was originally modelled as a continuous variable, but in each model the linearity assumption was not met. Instead, a four-level categorical variable was created and evaluated, with categories based roughly on the quartiles of the continuous variable. The province of Newfoundland and Labrador was excluded from logistic regression because only one producer from this province responded. Pearson chi-square and deviance goodnessof-fit tests were used to assess the fit of each model, with suitable fit indicated at p > 0.05. Also for each model, Pearson residuals, standardized Pearson residuals and deviance residuals were used to examine for the presence of outliers and delta-beta, delta chi-square and deltadeviance residuals for the presence of influential observations. All p-values reported in this paper are two-sided. Analysis was performed in Stata 10 (Stata Corporation, College Station, TX). 2.4. Questionnaire validation Post-administration, two steps were taken to investigate the validity of the questionnaire. Firstly, to address equivalency of interpretation between the English and French questionnaires, the French questionnaire was backtranslated to English by a bilingual dairy veterinarian (and graduate student) at the Ontario Veterinary College, Canada, who was blinded to the original English version. Two authors (I.Y. and S.H.) then independently compared both English versions and noted differences in question wording that could have affected interpretation. Disagreements between authors were discussed and resolved, and a consensus decision was made on whether to exclude implicated questions. The translator was consulted if there was any uncertainty regarding interpretation of questions in the French version. Secondly, Chronbach’s alpha was used to assess the internal consistency of variables measuring the same construct (i.e. whether producers indicated the same response to two or more questions measuring the same underlying attitude). High values of Chronbach’s alpha (>0.7) indicate high reliability or low response variance, while low values indicate low reliability or that the variables are not truly measuring the same construct (Groves et al., 2004). The constructs assessed were producers’ attitudes towards testing for zoonotic pathogens, safe antimicrobial use (AMU), traceability and providing information about food safety to different stakeholders.

I. Young et al. / Preventive Veterinary Medicine 94 (2010) 65–76

68

Table 1 Comparison of provincial, dairy-herd improvement and questionnaire respondent herd-size averages, Canada, 2008. Provincea

AB BC MB NB NLc NS ON PEI QC SK Total

DHIa herds (2007)

Province (2007)

p-Valueb

Respondents a

N

Mean herd size

N

Mean herd size

% Herds >50 cows

N (%) response

Mean herd size

SD

660 572 425 240 38 272 4508 222 6869 230 14,036

120 123 105 79 168 82 73 59 57 124 72

486 341 237 175 4 170 3300 138 5475 148 10,474

121 127 109 72 – 82 72 69 56 129 69

92.1 88.1 80.6 64.1 – 71.7 60.1 63.4 45.7 92.1 56.2

98 66 38 51 1 34 472 22 1358 32 2185

97 102 91 71 – 66 60 58 56 103 62

56 59 100 47 – 37 41 30 223 55 179

(20.2) (19.4) (16.0) (29.1) (25.0) (20.0) (14.3) (15.9) (24.8) (21.6) (20.9)d

% Herds >50 cows 86.7 80.3 65.8 58.0 – 55.9 43.4 50.0 34.2 81.3 42.4

<0.001 0.001 0.282 0.943 – 0.021 <0.001 0.103 0.996 0.013 0.053

CDIC (2009) and CanWest DHI (2009). a AB, Alberta; BC, British Columbia; DHI, dairy-herd improvement; MB, Manitoba; NB, New Brunswick; NL, Newfoundland and Labrador; NS, Nova Scotia; ON, Ontario; PEI, Prince Edward Island; QC, Quebec; SD, standard deviation; SK, Saskatchewan. b One-sample t-test comparisons of respondent mean herd size to the DHI average for each province. c No comparisons made with NL because there was only one respondent from this province. d Includes 13 responses where the province was not recorded by the respondent.

3.2. Attitudes towards unpasteurized milk consumption and antimicrobial resistance

3. Results 3.1. Producer and herd characteristics After removing 12 blank questionnaires, the final response percentage was 20.9% (2185/10,474). The average litres of milk picked up per farm every 2 days was 2993 (standard deviation [SD] = 2335). The average herd size of respondents was 62 (SD = 179), which was significantly lower than the DHI average in some provinces (Table 1). The percentage of herds with >50 cows was lower for respondents in all provinces (Table 1). Respondent demographic information (age, gender, organic status and herd size) is shown in Table 2. The number of respondents with education in dairy-health management or food safety and their attitudes towards unpasteurized milk, AMR, testing for zoonotic pathogens and food-safety information sources are shown in Table 3.

Table 2 Characteristics of questionnaire respondents, Canada, 2008. Characteristic

Total

Producer age <30 30–45 46–60 >60

2126

Producer gender Male Female

2110

Organic status No Yes

2107

Herd sizea <36 36–50 51–65 >65

2170

a

% 15.0 42.3 39.7 3.1

86.8 13.2

96.4 3.6

Based roughly on the quartiles.

24.8 32.8 17.4 25.0

No significant predictors were identified in the model evaluating producers’ reported consumption of unpasteurized milk (model 1). In contrast, factors associated with whether producers reported that consumers should be allowed to purchase unpasteurized milk (model 2) are shown in Table 4. Producers who reported having taken an educational course in dairy-health management and participation with CQM were less likely to indicate that consumers should be able to purchase raw milk, while younger producers (aged <30), producers with smaller herds, organic producers and producers who drink unpasteurized milk were more likely to indicate that consumers should be able to purchase raw milk (Table 4). Organic producers, producers who had taken a course in dairy-health management and producers from Quebec were more likely to be concerned about AMR (Table 4). 3.3. Knowledge and attitudes towards zoonotic pathogens Nearly three-quarters of producers knew that Salmonella (74.2%) and E. coli (73.0%) can be transmitted from beef or milk to humans, while 55.9% did not think that BVD could be transmitted and >50% were unsure about Brucella, Cryptosporidium, Toxoplasma, Johne’s disease (i.e. MAP) and anthrax (Fig. 1). Nearly three-quarters of producers (74.6% answered 4 or 5 on a five-point scale) were highly concerned about the potential negative economic impacts of BVD (Fig. 2). Nearly one-half of producers expressed a high concern that Salmonella could cause illness in consumers (48.3%), while most were not highly concerned about similar effects caused by BVD, Cryposporidium or Johne’s disease (Fig. 3). Most producers indicated that the farm is the most important control point for antibiotic residues (93.3%, 1965/2106), Johne’s disease (76.8%, 1471/1916), Listeria (53.4%, 815/1525), milk bacterial counts (69.5%, 1392/2003), somatic-cell counts

I. Young et al. / Preventive Veterinary Medicine 94 (2010) 65–76

69

Table 3 Producer-reported history of education in food safety and dairy-health management and attitudes towards unpasteurized milk, antimicrobial resistance and communication methods, Canada, 2008. Question

Total

% Yes response

Have completed a course in dairy-health management Have completed a course in food safety Self-perceived as knowledgeable about food safety in dairy production You or your family consume unpasteurized milk from the bulk milk tank Consumers should be able to purchase unpasteurized milk AMRa is making it harder to treat sick cattle successfully due to AMR

2140 2131 2143 2115 2126 2126

66.9 26.3 84.4 88.7 36.3 66.7

(If yes) most important factor causing AMRa in dairy cattle Antibiotics in feed Improper use of antibioticsb Mastitis therapy Other Treating sick cattle

1112

AMRa in humans is linked to AMUa in the dairy industry Meat and milk should be tested for zoonotic pathogens

2101 2074

(If yes) Who should pay for the testingc? Consumersb Government No opinion Processors Producers

1574

Would like to receive food-safety information in the future viac Education courses Newsletters Newspaper/magazines Other Veterinarians Websites

2185

a b c

17.5 21.3 40.4 10.3 10.5 10.1 75.9

9.0 66.1 9.8 29.2 16.5

36.2 57.8 50.2 2.5 73.1 38.4

AMR, antimicrobial resistance; AMU, antimicrobial use. Category created post hoc through open-ended responses. Multiple responses were allowed.

(89.6%, 1880/2099) and Salmonella (57.6%, 1080/1874). Most producers did not think that it was likely (responded 1 or 2 on a five-point scale) that farm employees (79.6%, 1245/1565), feed salesmen (59.6%, 1237/2077), milk-truck drivers (80.3%, 1653/2058), veterinarians (56.3%, 1185/ 2105), visiting farmers (45.3%, 901/1989) or inseminators (58.5%, 970/1659) could introduce infectious agents into their herd. Dead-stock handlers were considered most likely (33.5%, 537/1606, selected 4 or 5 on a five-point scale) to introduce infectious agents.

3.5. Questionnaire validation

3.4. Attitudes towards dairy-industry stakeholder knowledge and industry programs and potential initiatives to ensure safe milk

The response percentage in this study (20.9%) is comparable to previous postal questionnaires of dairy producers, which have ranged widely from 9% to 71.7% (Rauff et al., 1996; Payne et al., 1999; Vanbaale et al., 2003; Hoe and Ruegg, 2006; Matak et al., 2006; Kaylegian et al., 2008). Although we tried to increase the response rate in this study (e.g. use of a monetary incentive and reminder letter), other methods known to be effective in increasing responses to postal questionnaires could not be implemented due to limited resources, including sending notification letters and replacement questionnaires to all producers (Edwards et al., 2007). Whenever feasible, future postal questionnaires of dairy producers should use a variety of methods to assist in increasing response percentages. The average herd size of respondents was significantly lower than the DHI average in most provinces, and the percentage of herds with >50 cows was lower for

Most producers indicated that dairy farmers (72.2%, 1549/2148), milk processors (70.9%, 1521/2144) and veterinarians (90.9%, 1950/2146) know a lot about OFFS (answered 4 or 5 on a five-point scale). In contrast, 69.6% (1487/2135), 45.6% (967/2122) and 40.9% (874/2139) indicated that consumers, the government and grocery store chains, respectively, know little about OFFS (answered 1 or 2 on a five-point scale). Most producers (>50%) indicated that 15 different dairy-industry programs and potential initiatives are useful to ensure safe milk (Table 5). The only initiative that producers did not think was useful is lowering the fat content of milk (Table 5). Producers raised several topics in their open-ended comments (summarized in Table 6).

Our analysis of the questionnaire back-translation revealed that no questions presented in this paper were likely affected by differences in interpretation due to translation. Chronbach’s alpha was between 0.60 and 0.75 for each attitude construct, indicating moderate to good internal consistency for each of those measures (Table 7). 4. Discussion

70

I. Young et al. / Preventive Veterinary Medicine 94 (2010) 65–76

Table 4 Multivariable logistic-regression models of factors affecting producers’ attitudes towards antimicrobial resistance and the purchase of unpasteurized milk, Canada, 2008. Outcome

Predictor

ORa

SEa

95% CIa

Consumers should be able to purchase unpasteurized milkc

Have taken a course in dairy-health management

0.74

0.08

0.60, 0.92

0.006

CQM participation Organic producer Drink unpasteurized milk

0.79 2.10 4.07

0.08 0.54 0.84

0.64, 0.97 1.27, 3.47 2.72, 6.08

0.028 0.004 <0.001

Age <30 30–45 46–60 >60

1 0.74 0.61 0.67

– 0.11 0.09 0.21

– 0.56, 0.98 0.46, 0.82 0.36, 1.24

Herd size <36 36–50 51–65 >65

1 0.83 0.65 0.59

– 0.11 0.10 0.08

– 0.64, 1.07 0.48, 0.88 0.44, 0.78

Have taken a course in dairy-health management Organic producer

1.37 2.00

0.15 0.63

1.11, 1.69 1.09, 3.69

Provincea AB BC MB NB NS PEI ON QC SK

0.26 0.20 0.20 0.31 0.15 0.14 0.23 1 0.26

0.06 0.06 0.07 0.10 0.06 0.06 0.03 – 0.10

0.17, 0.12, 0.10, 0.16, 0.07, 0.05, 0.18, – 0.13,

Concern about AMRd

p-Valueb

0.011

<0.001

0.004 0.020 <0.001

0.39 0.35 0.40 0.58 0.31 0.34 0.29 0.53

a

AB, Alberta; BC, British Columbia; CI, confidence interval; MB, Manitoba; NB, New Brunswick; NS, Nova Scotia; ON, Ontario; OR, odds ratio; PEI, Prince Edward Island; QC, Quebec; SE, standard error; SK, Saskatchewan. b p-Values are from likelihood-ratio tests. c Pearson x2 = 133.8, p = 0.465; Deviance x2 = 150.0, p = 0.150. d Pearson x2 = 14.1, p = 0.593; Deviance x2 = 15.2, p = 0.509.

Fig. 1. Producer responses to whether each pathogen or infection can be transmitted from dairy-cattle beef or milk to humans, Canada, 2008. BVD, bovine viral diarrhoea; Crypto., Cryptosporidium; Johne’s, Johne’s disease; Salm., Salmonella.

I. Young et al. / Preventive Veterinary Medicine 94 (2010) 65–76

71

Fig. 2. Producer concern that each pathogen or infection could cause a negative economic impact on their herd (five-point scale from ‘not’ to ‘very’ concerned), Canada, 2008. BVD, bovine viral diarrhoea.

respondents in all provinces. However, the questionnaire asked producers to indicate the ‘average number of cows that they were milking in the previous year’, and while some producers might have reported their true herd size (i.e. lactating and non-lactating cows), others might have only reported the average number of cows being milked at any given point during the previous year (i.e. excluding non-lactating cows). Therefore, these differences might not indicate non-response bias. Nearly 90% of respondents reported that they or their families consume unpasteurized milk from their bulk milk

tanks, which is higher than the 42–61% reported in previous surveys of dairy producers in the USA (Jayarao and Henning, 2001; Hoe and Ruegg, 2006; Jayarao et al., 2006; Kaylegian et al., 2008). This difference might be a result of cultural or management differences between the USA and Canada. For example, the average herd size is much larger in the USA than in Canada (122 vs. 70) (United States Department of Agriculture [USDA], 2008; CDIC, 2009), and previous research has shown that producers with larger herds are less likely to consume unpasteurized milk (Hoe and Ruegg, 2006), although this factor was not

Fig. 3. Producer concern that each pathogen or infection could cause consumers to become ill (five-point scale from ‘not’ to ‘very’ concerned), Canada, 2008. BVD, bovine viral diarrhoea.

72

I. Young et al. / Preventive Veterinary Medicine 94 (2010) 65–76

Table 5 Producers’ perceived usefulness of 16 dairy-industry programs or potential initiatives for ensuring safe milk, Canada, 2008. Practice

Total

Use antibiotics as per label Use appropriate drug-withdrawal times Time-temperature recording for bulk milk tanks Use of milk-line filters on farm Sanitation of milking equipment Animal traceability Milk traceability On-farm food-safety programs Food-safety information to producers Food-safety information to processors Food-safety information to consumers Test animals for zoonotic pathogens Test milk or meat for zoonotic pathogens Test milk or meat for antibiotic residues Removal of animal protein from cattle feed Lower fat content in milk

2154 2156 2116 2160 2162 2111 2087 2105 2129 2085 2073 2043 2043 2145 1983 1995

significant in our study. Although producers were not asked why they consume unpasteurized milk and we found no significant predictors, previous research has shown that many farm families drink raw milk because they believe it tastes better, is cheaper or more convenient to access than pasteurized milk, or because of perceived health or nutritional benefits (Jayarao et al., 2006; Kaylegian et al., 2008). The sale of raw milk for public consumption is illegal in Canada, although roughly one-third of producers reported that consumers should be able to purchase raw milk. This is a concern given that unpasteurized milk is a source of zoonotic pathogens such as Campylobacter, Salmonella,

Table 6 Producer open-ended comments summarized as concerns, recommendations or general comments, Canada, 2008. Comment code

Na

Concerns Food safety/price of imported milk products Government involvement in/regulation of OFFSb Antibiotic use in dairy industry Food-safety standards at other parts of food chain Industry costs People lack immunity/environment is too sterile Producers being asked to do too much/being blamed OFFSb programs are not practical/lack common sense Animal-feed safety/animal by-products in feed

50 29 28 22 21 21 18 17 10

Recommendations Consumer awareness of food-safety issues should be increased Producer/industry awareness of food-safety issues should be increased Milk should be tested for zoonotic pathogens General comments Noted importance of food safety/OFFSb Noted the high food-safety standards in Canada Noted importance of animal welfare/ farm hygiene in OFFSb

71 48 17

67 49 33

a N = the number of times a comment was raised (multiple topics were raised by some producers). Only comments with a frequency of 10 are shown here. b OFFS, on-farm food-safety.

From ‘not useful’ to ‘very useful’ (%) 1

2

3

4

5

1.1 0.4 10.8 0.4 0.6 14.1 7.3 3.8 2.7 4.0 10.6 3.9 3.6 1.4 5.8 67.4

0.6 0.2 9.4 1.3 0.1 9.0 6.0 6.1 5.3 4.5 8.6 6.8 5.3 1.4 5.6 14.9

4.2 1.2 17.4 3.2 1.3 17.6 13.8 22.1 22.3 20.4 18.0 18.5 16.5 7.4 12.0 9.5

12.9 7.8 17.0 8.3 6.5 18.4 22.4 29.0 32.5 29.8 20.6 25.4 25.0 21.5 15.0 3.3

81.2 90.4 45.4 86.8 91.4 40.9 50.5 39.1 37.2 41.3 42.3 45.4 49.6 68.4 61.7 4.9

STEC and L. monocytogenes, and unpasteurized milk continues to cause many outbreaks of foodborne disease in North America (Peterson, 2003; CDC, 2007; Denny et al., 2008). Producers with smaller herds were more likely to indicate that consumers should be able to purchase unpasteurized milk. This result corresponds to findings from Hoe and Ruegg (2006), who reported that dairy producers in Wisconsin with smaller herds (100 lactating cows) were less likely to consider raw-milk consumption to be a human-health risk compared to producers with larger herds (>100 lactating cows). Similarly, younger age (<40 years) has previously been associated with an increased likelihood of raw-milk consumption among California residents (Headrick et al., 1997). To our knowledge, this is the first time that the attitudes of organic producers towards raw-milk consumption have been evaluated. Organic dairy standards focus on sustainability and animal welfare while avoiding the use of certain chemical compounds (e.g. antimicrobials) and other offfarm inputs (Canadian General Standards Board [CGSB], 2006). Given these management principles, it is not unexpected that organic producers were more likely to report that consumers should be able to purchase unpasteurized milk. Increased education of both conventional and organic dairy producers about the public-health risks associated with drinking unpasteurized milk is warranted. Jayarao et al. (2006) previously found that a lack of knowledge of foodborne pathogens in raw milk was associated with an increased likelihood of raw-milk consumption among Pennsylvania dairy producers. In our study, producers who reported having completed an educational course in dairy-health management were less likely to indicate that consumers should be able to purchase unpasteurized milk, indicating that continuing education might affect producer attitudes towards food safety. Reported participation in CQM had a similar effect, indicating a potential relationship between producer participation in OFFS programs and their attitudes towards food safety. A high concern about AMR in dairy production was noted among producers, which corresponds to previous

I. Young et al. / Preventive Veterinary Medicine 94 (2010) 65–76

73

Table 7 Internal consistency of attitude constructs in a questionnaire of Canadian dairy producers, 2008. Attitude construct

Variable/categories

aa

Favourability of testing for zoonotic pathogens

(1) Meat and milk should be tested for zoonotic pathogens (no/yes) (2) Test animals for zoonotic pathogens (not useful/useful)b (3) Test meat and milk for zoonotic pathogens (not useful/useful)b

0.610

Perceived usefulness of safe antimicrobial use

(1) Use antibiotics as per label (1–5, ‘not’ to ‘very’ useful) (2) Use appropriate drug-withdrawal times (1–5, ‘not’ to ‘very’ useful)

0.630

Perceived usefulness of traceability

(1) Animal traceability (1–5, ‘not’ to ‘very’ useful) (2) Milk traceability (1–5, ‘not’ to ‘very’ useful)

0.678

Perceived usefulness of providing food-safety information to stakeholders

(1) Food-safety information to producers (1–5, ‘not’ to ‘very’ useful) (2) Food-safety information to processors (1–5, ‘not’ to ‘very’ useful) (3) Food-safety information to consumers (1–5, ‘not’ to ‘very’ useful)

0.736

a b

Chronbach’s alpha. Variables were dichotomized (values of 1–2 as ‘not useful’ and 3–5 as ‘useful’) to achieve comparable units.

research that has shown that dairy producers are very concerned about the implications of AMR and antibiotic residues to food safety and human health (Wilson, 1998; Vanbaale et al., 2003; Raymond et al., 2006). It is not surprising that organic producers showed more concern about AMR, because AMU is limited in organic production and antimicrobials are used more frequently on conventional than organic dairy farms (Zwald et al., 2004; CGSB, 2006). Dairy producers in Quebec were more likely to be concerned about AMR than producers in any other province, which might be due to more restrictive drugavailability policies in this province. For example, in Quebec, antimicrobials for use in food animals are available only by prescription from a licensed veterinarian, while in other provinces some drugs can also be purchased without a prescription (Health Canada, 2002). However, it is not known whether these policies have led to a decrease in use of veterinary antimicrobials for food animals in Quebec. The impact of the Quebec veterinary drugavailability model on producer attitudes towards and use of antimicrobials should be more closely examined; we also recommend continuing education with producers about prudent AMU practices. Most producers correctly identified that Salmonella and E. coli can be transmitted through beef or milk to humans but that BVD cannot be transmitted in this way. However, knowledge of Brucella should be improved; many younger producers might not be familiar with this pathogen because its official eradication from Canadian cattle occurred several years ago. Indeed, 14.0%, 24.9%, 39.1% and 63.3% of producers aged <30, 30–45, 46–60 and >60, respectively, correctly indicated that Brucella can be transmitted from beef or milk to humans. Knowledge of Cryptosporidium should also be improved, because roughly 70% of producers were unsure whether it can be transmitted from dairy cattle to humans through beef or milk and 60% were not concerned that it could cause consumers to become ill. In contrast, the high percentage of producers who were not sure whether Johne’s disease (i.e. MAP) or Toxoplasma can be transmitted from beef or milk to humans is not surprising, given that evidence on the zoonotic potential of MAP is still debated (Feller et al., 2007; Abubakar et al., 2008; Waddell et al., 2008) and dairy

cattle are unlikely to be a source of Toxoplasma (Gajadhar et al., 2006). Most producers (>50%) indicated that the farm was the most important control point for six different microbial and chemical agents. This result corresponds to a previous survey by Payne et al. (1999), who reported that 99% of dairy producers in California agreed that they were responsible for the safety of milk leaving their farm. However, the question about Listeria resulted in 30.2% missing values, perhaps indicating unfamiliarity with this pathogen. A low knowledge of Listeria among dairy producers has been previously reported (Hoe and Ruegg, 2006). Given the severity of systemic listeriosis in human (with case-fatality risks ranging from 20% to 30%) (PosfayBarbe and Wald, 2004), and the role of dairy cattle as a reservoir for Listeria, increased education of dairy producers about this pathogen is also warranted. Most producers perceived a low risk that infectious agents could be introduced into their herd by farm visitors. Similar to findings by Hoe and Ruegg (2006), dead-stock handlers were considered more likely than other visitors to introduce infectious agents, even though other farm visitors could potentially pose an equal or greater risk. Controlled visitor access is an important component of most biosecurity programs (Moore et al., 2008), because farm visitors can be the source of zoonotic pathogens such as Salmonella that can be transferred to dairy cattle if proper precautions are not taken. For example, the use of protective clothing by veterinarians has been shown to be a protective risk factor for infection caused by bovine herpsevirus type 1, BVD virus, Salmonella dublin and Leptospira on Dutch dairy farms (van Schaik et al., 2002). Future education with producers should highlight the importance of controlled visitor access and the potential risks of introducing pathogens and infections from all types of farm visitors. A large proportion of producers indicated that consumers and government stakeholders know little about OFFS in dairy production, and several (n = 71) commented that consumer knowledge and awareness of food safety should be increased. These attitudes suggest a lack of communication or distrust between these stakeholder groups (Sargeant et al., 2007; Gunn et al.,

74

I. Young et al. / Preventive Veterinary Medicine 94 (2010) 65–76

2008). Future efforts should be made to enhance trust and knowledge exchange between producers and these stakeholders. In contrast, producers viewed veterinarians as very knowledgeable and as a favourable source of new information about food safety. Positive attitudes towards veterinarians among dairy producers has also been identified in previous questionnaires and focus groups in the USA and UK (Vanbaale et al., 2003; Gunn et al., 2008; USDA, 2008). Only one-third of producers were interested in learning about food safety through educational courses, which is a concern given that producers who had taken an educational course in dairy-health management were more likely to have precautionary attitudes towards the consumption of unpasteurized milk and be concerned about the impacts AMR in the dairy industry. Educational courses are an effective method of increasing awareness and motivation towards the use of biosecurity practices among dairy producers (Moore and Payne, 2007). However, our findings suggest that such courses might suffer from a lack of participation. Future research should evaluate the effectiveness of mandatory continuing-education courses in food safety and dairy-health management for dairy producers. Producers were largely in favour of implementing dairy-industry programs and initiatives to ensure safe milk production. However, although most producers rated milk and animal traceability as useful, nearly one-quarter (23.1% selected 1 or 2) indicated that animal traceability is not useful. All cattle in Canada are traceable through the Canadian Cattle Identification Program, an industry-led program that is regulated and enforced by the Canadian Food Inspection Agency (CFIA) (Rajic´ et al., 2007). It is possible that some producers were less favourable towards animal traceability due to the government regulation of this program, because several producers (n = 29) openly commented about their concern of government involvement in OFFS. Dairy-producer opposition of governmentled OFFS programs has been previously reported (Vanbaale et al., 2003). Several producers (n = 50) also commented about their concern of the food-safety standards and market price of imported dairy products. In Canada, imported dairy products must not pose animal-health risks, must be declared to be produced under sanitary conditions and fit for human consumption, and are required to meet the same labelling, compositional and health and safety standards as domestic products (CFIA, 2007). Imported dairy products are randomly inspected to ensure that Canadian standards are met, although such inspections are not obligatory (CFIA, 2007). Although federal health and safety standards equally apply to domestic and imported dairy products, the CQM program and other provincial onfarm testing requirements might not, which will likely continue to be a concern among some dairy producers in Canada unless equal standards can be assured for all stages of production in importing countries. Roughly three-quarters (75.9%) of producers indicated that meat and milk should be tested for zoonotic pathogens, an initiative that they thought the government should fund. In Canada, there is currently no routine

testing for zoonotic pathogens in milk, although all milk is tested for bacterial inhibitors (including antimicrobial residues) and, in some cases, for generic bacterial counts or indicator bacteria (Department of Justice, 2009; Dairy Farmers of Ontario, 2007). Testing for specific pathogens could have merit if part of a specific pathogen-control program (e.g. HACCP), for milk that is to be used for unpasteurized cheese production or for other organisms (such as MAP) that could survive the pasteurization process. However, the overall net-benefit of such an approach would need to be evaluated before regulatory action is considered. Although our questionnaire was pre-tested on veterinary students, it was not pre-tested on producers, and this could have affected their understanding of certain questions. For example, there was a high percentage of missing values for the questions presented in Figs. 2 and 3, and it is possible that a more extensive pre-test could have led to improvements in the wording of these questions. However, we believe that the validity of this study was not significantly compromised, because many of our results agreed with those of previous studies. We also believe that potential biases in question interpretation due to translation were likely minimal, given the multiple checks of the original translation and our evaluation of the backtranslated questionnaire. The assessment of internal consistency indicated that producers’ responses to questions that asked about the same underlying attitudes were consistent, although for the construct representing producers’ attitudes towards testing for zoonotic pathogens, the value for Chronbach’s alpha improved greatly (from 0.6 to >0.8) when the original dichotomous variable was removed. This could be related to our choice of cut-point for the rating-scale questions, but might also indicate that producers were more likely to agree with statements on a five-point scale compared to giving a yes vs. no response. This potential for positivity bias (i.e. clustering of responses on the positive end of a scale) should be considered when interpreting our results (Groves et al., 2004). 5. Conclusion We found that dairy producers in Canada have positive attitudes towards food safety and are knowledgeable about certain microbial agents (e.g. Salmonella). However, we also identified gaps in awareness of Brucella, Cryptosporidium and the risks of introducing infectious agents from farm visitors. There is a need for increased communication and knowledge exchange between dairy producers and other industry stakeholders (such as consumers and government personnel) to increase trust and collaboration between these groups. Veterinarians should have an important role in continuing education of producers, because they are seen as a knowledgeable and trusted source of information about food safety. Conflict of interest We have no conflicts to declare.

I. Young et al. / Preventive Veterinary Medicine 94 (2010) 65–76

Acknowledgements We thank CanWest DHI and Valacta for their participation and for mailing questionnaires and letters to producers; Ian Weinrich for development of the electronic database; Heather Desjardins for assistance with survey printing; Jessica Fung, Amanda Waldner, and Corinne Sawatzky for data entry and validation; Jean-Francois Tetreault and Jocelyn Dubuc for translation of the questionnaire; Erica Pufall for translation of open-ended responses; Ann Godkin and Lucie Dutil for their input on the discussion; and the Public Health Agency of Canada for funding this project. This study was designed, data were collected and analyzed and this manuscript prepared in collaboration with Public Health Agency of Canada researchers. The first author was the recipient of an Ontario Graduate Scholarship. Appendix A. Supplementary data Supplementary data associated with this article can be found, in the online version, at doi:10.1016/j.prevetmed. 2009.11.010. References Abubakar, I., Myhill, D., Aliyu, S.H., Hunter, P.R., 2008. Detection of Mycobacterium avium subspecies paratuberculosis from patients with Crohn’s disease using nucleic acid-based techniques: a systematic review and meta-analysis. Inflamm. Bowel Dis. 14, 401–410. CanWest DHI, 2009. Ontario Progress Report 2008. http://www. canwestdhi.com/pdf_files/2008 progress report statistics.pdf. Centers for Disease Control and Prevention, 2007. Salmonella Typhimurium infection associated with raw milk and cheese consumption— Pennsylvania. MMWR Morb. Mortal. Wkly. Rep. 56, 1161–1164. Canadian Dairy Information Centre, 2009. Number of Farms, Dairy Cows and Dairy Heifers. http://www.dairyinfo.gc.ca/index_e.php?s1= dff-fcil&s2=farm-ferme&s3=nb. Canadian Food Inspection Agency, 2007. Canadian Import, Export and Interprovincial Requirements for Dairy Products. http://www. inspection.gc.ca/english/fssa/dailai/cdnreqe.shtml#grade. Canadian General Standards Board, 2006. Organic Production Systems: General Principles and Management Standards. CAN/CGSB-32.3102006. Dairy Farmers of Canada, 2007. Canadian Quality Milk Program (CQM)—Provincial Summaries. http://www.dairygoodness. ca/NR/rdonlyres/58DA4ECC-D890-4F4F-8916-6FEDE0EC7FC3/0/ CQMProvSummariesDec07.pdf. Dairy Farmers of Ontario, 2007. Dairy Farmers of Ontario policies. http:// www.milk.org/Corporate/pdf/Publications-DFOPolicyBook.pdf. Denny, J., Bhat, M., Eckmann, K., 2008. Outbreak of Escherichia coli O157:H7 associated with raw milk consumption in the Pacific Northwest. Foodborne Pathog. Dis. 5, 321–328. Edwards, P., Roberts, I., Clarke, M., DiGuiseppi, C., Pratap, S., Wentz, R., Kwan, I., Cooper, R., 2007. Methods to increase response rates to postal questionnaires. Cochrane Database Syst. Rev. (2), MR000008. Fahey, T., Morgan, D., Gunneburg, C., Adak, G.K., Majid, F., Kaczmarski, E., 1995. An outbreak of Campylobacter jejuni enteritis associated with failed milk pasteurisation. J. Infect. 31, 137–143. Feller, M., Huwiler, K., Stephan, R., Altpeter, E., Shang, A., Furrer, H., Pfyffer, G.E., Jemmi, T., Baumgartner, A., Egger, M., 2007. Mycobacterium avium subspecies paratuberculosis and Crohn’s disease: a systematic review and meta-analysis. Lancet Infect. Dis. 7, 607–613. Gajadhar, A.A., Scandrett, W.B., Forbes, L.B., 2006. Overview of food- and water-borne zoonotic parasites at the farm level. Rev. Sci. Technol. 25, 595–606. Department of Justice, Government of Canada, 2009. Food and Drug Regulations, C.R.C., c. 870, http://laws.justice.gc.ca/en/F-27/C.R.C.c.870/index.htm. Groves, R.M., Fowler, F.J., Couper, M.P., Lepkowski, J.M., Singer, E., Tourangeau, R., 2004. Survey Methodology. John Wiley and Sons, Inc., Hoboken, NJ.

75

Gunn, G.J., Heffernan, C., Hall, M., McLeod, A., Hovi, M., 2008. Measuring and comparing constraints to improved biosecurity amongst GB farmers, veterinarians and the auxiliary industries. Prev. Vet. Med. 84, 310–323. Headrick, M.L., Timbo, B., Klontz, K.C., Werner, S.B., 1997. Profile of raw milk consumers in California. Public Health Rep. 112, 418–422. Health Canada, 2002. Final Report of the Advisory Committee on Animal Uses of Antimicrobials and Impact on Resistance and Human Health. Uses of antimicrobials in food animals in Canada: impact on resistance and human health. http://www.hc-sc.gc.ca/dhp-mps/pubs/vet/ amr-ram_final_report-rapport_06-27_4-eng.php. Hoe, F.G., Ruegg, P.L., 2006. Opinions and practices of Wisconsin dairy producers about biosecurity and animal well-being. J. Dairy Sci. 89, 2297–2308. Honish, L., Predy, G., Hislop, N., Chui, L., Kowalewska-Grochowska, K., Trottier, L., Kreplin, C., Zazulak, I., 2005. An outbreak of E. coli O157:H7 hemorrhagic colitis associated with unpasteurized Gouda cheese. Can. J. Public Health 96, 182–184. Jayarao, B.M., Henning, D.R., 2001. Prevalence of foodborne pathogens in bulk tank milk. J. Dairy Sci. 84, 2157–2162. Jayarao, B.M., Donaldson, S.C., Straley, B.A., Sawant, A.A., Hegde, N.V., Brown, J.L., 2006. A survey of foodborne pathogens in bulk tank milk and raw milk consumption among farm families in Pennsylvania. J. Dairy Sci. 89, 2451–2458. Karns, J.S., Van Kessel, J.S., McClusky, B.J., Perdue, M.L., 2007. Incidence of Escherichia coli O157:H7 and E. coli virulence factors in US bulk tank milk as determined by polymerase chain reaction. J. Dairy Sci. 90, 3212–3219. Katz, S.E., Brady, M.S., 2000. Antibiotic residues in food and their significance. Food Biotechnol. 14, 147–171. Kaylegian, K.E., Moag, R., Galton, D.M., Boor, K.J., 2008. Raw milk consumption beliefs and practices among New York state dairy producers. Food Prot. Trends 28, 184–191. Matak, K.E., Hovingh, E., Smith, C.E., Waterman, K., Hackney, C.R., Sumner, S.S., 2006. Virginia/West Virginia dairy practices survey. Food Prot. Trends 26, 20–26. Moore, D.A., Payne, M., 2007. An evaluation of dairy producer emergency preparedness and farm security education. J. Dairy Sci. 90, 2052– 2057. Moore, D.A., Merryman, M.L., Hartman, M.L., Klingborg, D.J., 2008. Comparison of published recommendations regarding biosecurity practices for various production animal species and classes. J. Am. Vet. Med. Assoc. 233, 249–256. Murinda, S.E., Nguyen, L.T., Ivey, S.J., Gillespie, B.E., Almeida, R.A., Draughon, F.A., Oliver, S.P., 2002. Prevalence and molecular characterization of Escherichia coli O157:H7 in bulk tank milk and fecal samples from cull cows: a 12-month survey of dairy farms in East Tennessee. J. Food Prot. 65, 752–759. OIE Animal Production Food Safety Working Group, 2006. Guide to good farming practices for animal production food safety. Rev. Sci. Tech. 25, 823–836. Payne, M., Bruhn, C.M., Reed, B., Scearce, A., O’Donnell, J., 1999. On-farm quality assurance programs: a survey of producer and industry leader opinions. J. Dairy Sci. 82, 2224–2230. Peterson, M.C., 2003. Campylobacter jejuni enteritis associated with consumption of raw milk. J. Environ. Health 65, 20–21. Posfay-Barbe, K.M., Wald, E.R., 2004. Listeriosis. Pediatr. Rev. 25, 151– 159. Rajic´, A., Waddell, L.A., Sargeant, J.M., Read, S., Farber, J., Firth, M.J., Chambers, A., 2007. An overview of microbial food safety programs in beef, pork, and poultry from farm to processing in Canada. J. Food Prot. 70, 1286–1294. Rauff, Y., Moore, D.A., Sischo, W.M., 1996. Evaluation of the results on a survey of dairy producers on dairy herd biosecurity and vaccination against bovine viral diarrhea. J. Am. Vet. Med. Assoc. 209, 1618–1622. Raymond, M.J., Wohrle, R.D., Call, D.R., 2006. Assessment and promotion of judicious antibiotic use on dairy farms in Washington State. J. Dairy Sci. 89, 3228–3240. Sargeant, J.M., Ramsingh, B., Wilkins, A., Travis, R.G., Gavrus, D., Snelgrove, J.W., 2007. Constraints to microbial food safety policy: opinions from stakeholder groups along the farm to fork continuum. Zoonoses Public Health 54, 177–184. Srinivasan, V., Nam, H.M., Nguyen, L.T., Tamilselvam, B., Murinda, S.E., Oliver, S.P., 2005. Prevalence of antimicrobial resistance genes in Listeria monocytogenes isolated from dairy farms. Foodborne Pathog. Dis. 2, 201–211. Straley, B.A., Donaldson, S.C., Hedge, N.V., Sawant, A.A., Srinivasan, V., Oliver, S.P., Jayarao, B.M., 2006. Public health significance of antimicrobial-resistant Gram-negative bacteria in raw bulk tank milk. Foodborne Pathog. Dis. 3, 222–233.

76

I. Young et al. / Preventive Veterinary Medicine 94 (2010) 65–76

Thomas, M.K., Majowicz, S.E., Pollari, F., Sockett, P.N., 2008. Burden of acute gastrointestinal illness in Canada, 1999–2007: interim summary of NSAGI activities. Can. Commun. Dis. Rep. 34, 8–15. United States Department of Agriculture, 2008. Dairy 2007, Part III: Reference of Dairy Cattle Health and Management Practices in the United States, 2007. http://www.aphis.usda.gov/vs/ceah/ncahs/ nahms/dairy/dairy07/Dairy2007_PartIII_rev.pdf. Van Kessel, J.S., Karns, J.S., Gorski, L., McCluskey, B.J., Perdue, M.L., 2004. Prevalence of Salmonellae, Listeria monocytogenes, and fecal coliforms in bulk tank milk on US dairies. J. Dairy Sci. 87, 2822–2830. van Schaik, G., Schukken, Y.H., Nielen, M., Dijkhuizen, A.A., Barkema, H.W., Benedictus, G., 2002. Probability of and risk factors for introduction of infectious diseases into Dutch SPF dairy farms: a cohort study. Prev. Vet. Med. 54, 279–289. Vanbaale, M.J., Galland, J.C., Hyatt, D.R., Milliken, G.A., 2003. A survey of dairy producer practices and attitudes pertaining to dairy market beef food safety. Food Prot. Trends 23, 466–473.

Waddell, L.A., Rajic´, A., Sargeant, J., Harris, J., Amezcua, R., Downey, L., Read, S., McEwen, S.A., 2008. The zoonotic potential of Mycobacterium avium spp. paratuberculosis: a systematic review. Can. J. Public Health 99, 145–155. Wilson, D.J., 1998. Dairy producer attitudes and farm practices used to reduce the likelihood of antibiotic residues in milk and dairy beef: a five state survey. Large Anim. Pract. 19, 24–30. Zwald, A.G., Ruegg, P.L., Kaneene, J.B., Warnick, L.D., Wells, S.J., Fossler, C., Halbert, L.W., 2004. Management practices and reported antimicrobial usage on conventional and organic dairy farms. J. Dairy Sci. 87, 191–201. Young, I., Rajic´, A., Hendrick, S., Parker, S., Sanchez, J., McClure, J.T., McEwen, S.A., 2010. Attitudes towards the Canadian Quality Milk program and use of good production practices among Canadian dairy producers. Prev. Vet. Med. 94, 43–53.