Travel Associated Rabies in Pets and Residual Rabies Risk Western Europe Volume 22 Number 7—July 2016 Emerging Infectious Disease journal CDC

Dispatch

Travel-Associated Rabies in Pets and Residual Rabies Risk, Western Europe

Florence Ribadeau-Dumas , Florence Cliquet, Philippe Gautret, Emmanuelle Robardet, Claude Le Pen, and Hervé Bourhy

The Study

We calculated the risk that a given pet in western Europe is contagious for rabies on a given day by the equation

We describe factors associated with rabid pets (https://zenodo.org/record/49670#) and define pet transport as any noncommercial movement of a live cat, dog, or ferret and its owner or an authorized person across an administrative border.

During 2001–2013, a total of 21 animal rabies cases attributed to pets from rabies-enzootic countries were reported in western Europe (https://zenodo.org/record/49670#), which represented 1.6 pets/year and 23 days/year of potential contagiousness. Fifteen dogs and 1 kitten originated from rabies-endemic countries outside western Europe. Five dogs raised in western Europe acquired rabies outside this region. One dog subsequently infected 2 indigenous dogs in France (4). All pet owners were identified. All owners except 1 (a Spanish man living in a van) were official residents of western Europe. Circumstances that led to pet examination and rabies diagnosis were clinical suspicion (14 pets), bitten humans (3 pets), border quarantine (2 pets), and retrospective data (2 pets with indigenous secondary cases during the alert in France in 2008).

Average contagious period was 16 days/pet: 14 days in western Europe (8 days without signs of rabies and 6 days with signs of rabies) and 2 days before arriving in western Europe. For 1 dog, signs of rabies appeared before the animal entered western Europe. For each rabid animal, an average of 34 (range 0–187) persons and other animals received PEPs. The maximum value of this range corresponds to an alert in France in 2004. After this alert, 1,200 animals were tested and 759 were observed for 1 year. Human and pet vaccinations led to vaccine shortages that required importing of vaccines not authorized for use in France (5).

We identified animal origin and mode of entry into western Europe (Table 1). Most rabies cases originated in Morocco and were recorded in France. Three cases were imported from eastern Europe to Germany, 1 from The Gambia to France, and 1 from Sri Lanka to the United Kingdom. Customs officials could not identify any of 11 cases in animals transported mainly by road (e.g., after a ferry trip from Morocco to Spain, Portugal, or France). Seven pets were transported through other countries in western Europe before arriving in the country of diagnosis (https://zenodo.org/record/49670#). Six puppies and 1 kitten were transported by air, of which only 2 were identified by customs officials (in the United Kingdom and Germany).

Figure. European Union (EU) regulations (no. 998/2003 and no. 576/2013, http://eur-lex.europa.eu/legal-content/EN/TXT/?uri=CELEX:32013R0576) on movement of cats, dogs, and ferrets, 2003–2013. Before 2003, national rules applied (e.g., animal checked at destinations, rabies vaccination,...

Of 19 transported rabid pets, 8 (42%) had no rabies vaccination, pet passport, or health certificate. Only 6 were vaccinated (0/2 infected in France, 3/3 imported but raised in western Europe, 3/7 imported by air, and 0/8 imported by road). Most vaccinated pets did not comply with recommended age for vaccination (>12 weeks of age) or time between vaccination, serologic analysis, and transport. No reports mentioned valid rabies serologic analysis included in European Pet Movement Policy (Figure) for unlisted third countries (e.g., Morocco, the Gambia, Sri Lanka, or Azerbaijan) (6). Using data for 2001–2013, we calculated that, for contact on a given day with a pet in western Europe, the probability of the pet being contagious for rabies attributed to pet transport was 7.52 × 10?10 (Table 2).

We observed a significant correlation between number of contagious days for dogs in a country and number of tourists traveling from this country to Morocco (? = 0.73, p = 0.017). We found no correlation with other variables tested (total dog population, dog population density, number of dogs per inhabitant).

Acknowledgment

References

1. Cliquet F, Picard-Meyer E, Robardet E. Rabies in Europe: what are the risks? Expert Rev Anti Infect Ther. 2014;12:905–8. DOIPubMed
2. Freuling CM, Hampson K, Selhorst T, Schröder R, Meslin FX, Mettenleiter TC, The elimination of fox rabies from Europe: determinants of success and lessons for the future. Philos Trans R Soc Lond B Biol Sci. 2013;368:20120142. DOIPubMed
3. Ribadeau Dumas F, N’Diaye DS, Paireau J, Gautret P, Bourhy H, Le Pen C, Cost-effectiveness of rabies post-exposure prophylaxis in the context of very low rabies risk: a decision-tree model based on the experience of France. Vaccine. 2015;33:2367–78. DOIPubMed
4. French multidisciplinary investigation team. Identification of a rabid dog in France illegally introduced from Morocco. Euro Surveill. 2008;13:pii: 8066.PubMed
5. Servas V, Mailles A, Neau D, Castor C, Manetti A, Fouquet E, An imported case of canine rabies in Aquitaine: investigation and management of the contacts at risk, August 2004–March 2005. Euro Surveill. 2005;10:222–5.PubMed
6. Regulation (EC) no. 998/2003 of the European parliament and of the council, 2003 [cited 2015 Apr16]. http://eur-lex.europa.eu/legal-content/EN/TXT/?uri=CELEX:32013R0576
7. World Tourism Organization. UNWTO annual report 2014. Madrid: UNWTO 2015 [cited 2015 Jun 10].http://www2.unwto.org/annualreport2014
8. Carrara P, Parola P, Brouqui P, Gautret P. Imported human rabies cases worldwide, 1990–2012. PLoS Negl Trop Dis. 2013;7:e2209. DOIPubMed
9. Lankau EW, Tack DM, Marano N. Crossing borders: one world, global health. Clin Infect Dis. 2012;54:v–vi. DOIPubMed
10. Metlin AE, Holopainen R, Tuura S, Ek-Kommonen C, Huovilainen A. Imported case of equine rabies in Finland: clinical course of the disease and the antigenic and genetic characterization of the virus. J Equine Vet Sci. 2006;26:584–7 .DOI
11. Napp S, Casas M, Moset S, Paramio JL, Casal J. Quantitative risk assessment model of canine rabies introduction: application to the risk to the European Union from Morocco. Epidemiol Infect. 2010;138:1569–80. DOIPubMed
12. Altmann M, Parola P, Delmont J, Gautret P. Knowledge, attitudes, and practices of French travelers from Marseille regarding rabies risk and prevention. J Travel Med. 2009;16:107–11. DOIPubMed
13. Gautret P, Ribadeau-Dumas F, Parola P, Brouqui P, Bou
    

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Restaurant Cooking Trends and Increased Risk for Campylobacter Infection Volume 22 Number 7—July 2016 Emerging Infectious Disease journal CDC

Volume 22, Number 7—July 2016

Research

Restaurant Cooking Trends and Increased Risk for Campylobacter Infection

Anna K. Jones, Dan Rigby1, Michael Burton, Caroline Millman, Nicola J. Williams, Trevor R. Jones, Paul Wigley, Sarah J. O’Brien , Paul Cross1, and for the ENIGMA Consortium

Methods

Participants

We recruited a quota-based sample of 1,030 members of the UK public via an online market research panel (http://www.researchnow.com). Quotas were used to ensure representativeness in terms of age groups and social class. The quota permitted an unequal split by sex (up to 70% women) because in the United Kingdom, food preparation at home is more commonly performed by women than men. We also recruited 143 chefs through face-to-face convenience sampling at culinary shows and competitions and by online culinary forums.

All participants gave informed consent. Respondents were debriefed on the purpose of the survey after completion and given the opportunity to withdraw their data. Ethical approval was obtained from the College of Natural Science Ethics Committee at Bangor University (CNS/2014/AJ1).

Preparation of Visual Aids

To prepare cooked chicken liver dishes to serve as visual aids, we used methods similar to those used in studies of hamburgers (16) and beefsteaks (17). A chef cooked 7 batches of chicken livers for various times, recorded the maximum core temperature for each batch, and arranged each batch on a plate for photography by a professional photographer. The process was repeated (without the temperature being recorded) for 3 other meats (duck breasts, lamb racks, and beef burgers).

Surveys of Preference and Knowledge

Figure 1. Chicken liver images, in order of cooking time/rareness, used in survey to determine preferences and knowledge of safe cooking practices among chefs and the public, United Kingdom.

To determine preferences and knowledge of safe cooking practices among chefs and members of the public, we used the images of cooked chicken livers as visual aids. The images were presented in surveys (online and print), arranged in order of cooking time/rareness (Figure 1). The surveys for chefs and the public were similar, except that the chefs were asked about serving preferences and the public was asked about eating preferences.

To avoid biases (such as social desirability bias) resulting from respondents perceiving the survey to be about food safety, we described the survey as being about food preferences. Respondents were first asked preference questions about 3 of the 4 meats (in random order) to obscure the focus on chicken livers and safety. Chefs were asked to indicate which chicken liver dish was cooked “the way you would like to serve it” and “the way you think most customers would like it.” Members of the public were asked which dish they would prefer if “eating out” and “eating at home.”

Respondents were subsequently asked which chicken liver dish (if any) was the first they thought would meet FSA safe cooking guidelines. Additional questions were asked about perceived trends and influences regarding cooking meat, dining habits, and demographic information such as class and age. Chefs provided additional information about their current position, such as their training and industry experience.

Campylobacter Survival

To prepare a suspension of Campylobacter for experimental inoculation, we streaked Camplyobacter jejuni M1 strain (sequence type 137, clonal complex 45) on Columbia agar base containing 5% defibrinated horse blood, incubated it at 37°C under microaerobic conditions for 48–72 h, and then inoculated it into Camplyobacter enrichment broth. After subculture for another 24 h, a bacterial suspension was prepared in maximum recovery diluent to an optical density of 600 nm (?109 CFU/mL). The culture broth was diluted in Camplyobacter enrichment broth to give a suspension of ?105 CFU/mL for inoculation into fresh chicken livers.

The fresh chicken livers were purchased in packs from supermarkets and sorted into batches of 4 with similar weights. The connective tissue was cut between the 2 liver lobes, with the weight of the larger lobe recorded and assigned for inoculation with Campylobacter broth suspension; 4 livers were assigned to each cooking batch. A 1-cm2 area of each liver was scored at its thickest point by using a sterile scalpel blade and injected with 100 ?L (?104CFU) of culture broth, corresponding to the highest levels of Campylobacter reported to be found in naturally contaminated livers (18).

For each cooking time, 10 g butter was heated in a frying pan over moderate to high heat on an electric cooktop; when the butter had finished frothing, the 4 inoculated liver lobes in the batch were added. The maximum core temperature of the largest and smallest liver in each batch was recorded. To determine the survival of the inoculated M1 strain of C. jejuni within the cooked livers, we placed each liver in a sterile petri dish and a 4–5-g portion around the scored inoculated region was removed and added to a Stomacher bag (Seward BA6040, Worthing, UK); 10 mL of Exeter broth was added to each bag before Stomaching (mechanical pounding of the outer surface of the bag to remove bacteria) for 1 min. The homogenized suspension was poured into a 20-mL universal container and incubated at 41°C under microaerobic conditions (Variable Atmosphere Incubator; Don Whitely Scientific, Shipley, UK) for 24 h, after which 1 loopful of broth was plated onto Campylobacter blood-free medium (modified charcoal cefoperazone deoxycholate agar, containing cefoperazone and amphotericin) at 41°C under microaerobic conditions for 48–72 h. We picked 1 typical Campylobacter colony from at least 1 plate in each batch and confirmed it as C. jejuni by PCR; for a cooked liver to be deemed positive, 1 isolate per batch was confirmed as C. jejuni positive (19).

Data Analyses

Figure 2. Campylobactersurvival in cooked (pan-fried) chicken livers, by cooking time and temperature. Error bars represent minimum and maximum temperatures reached.

We modeled the probability of survival for the 60 livers for which temperature and Campylobacterpresence/absence after cooking were recorded. We used logistic regression to model the relationship between the core temperature of the livers and the survival of Campylobacter. The probability of Campylobacter survival as a function of core temperature was modeled via estimation of a logit model, which captured the nonlinear temperature-survival relationship (Figure 2). Parameter estimates were obtained by using logistic regression (Stata logit command; StataCorp LP, College Station, TX, USA) on the binary variable indicating Camplyobacter survival (1 = survival, 0 = nonsurvival) in a sample of 60 cooked chicken livers. Temperature was the maximum core temperature recorded for the batch from which the chicken liver was taken. This model was used to assign predicted survival rates for each photographed chicken liver dish.

We used the Kolmogorov Smirnov 2-sample test to compare differences in the distribution of knowledge and preferences between groups (chefs and the public). We investigated within-person differences by using the Wilcoxon signed-rank test for paired data. Ordered logit models (20) were estimated to determine the effects of observable characteristics on respondents’ preferences for chicken liver rareness and their choices of FSA-compliant livers.

Results

Campylobacter Survival

We discuss the results of the Campylobacter survival experiment first because an understanding of those results is useful for interpreting the preferences and knowledge analyses. The relationship between core temperature and Campylobacter survival rate was inverse (Table; Figure 2). Of the 32 batches of 4 inoculated livers, the shortest cooking time was 1 minute, leading to a mean core temperature of 36°C and a 100% Campylobacter survival rate. At the maximum mean core temperature (72°C), Campylobacter survival rate was 8.3%.

The logistic model predicted a survival rate of 98% in liver with core temperature that reached 52°C (liver 1) and equivalent survival rates of 95% and 48% at core temperatures of 56°C and 66°C (livers 2 and 3). Liver 4 reached a maximum temperature of 70°C, but the temperature was not held for the recommended 2 minutes; predicted Campylobacter survival rate was 22%. Livers 6 and 7 met the FSA guidelines, and their predicted Campylobactersurvival rate was <0.001%.

Preferences and Knowledge of the Public

Of the 1,030 members of the public surveyed, 43.0% ate chicken livers and hence were asked to select the chicken liver dishes they preferred and which they thought met FSA guidelines. Half (49.3%) of all male respondents and 38.4% of all female respondents ate chicken livers. Rates of chicken liver consumption varied by age group: 18–34 years, 34.7%; 35–44 years, 44.7%; 45–54 years, 49.0%, 55–64 years: 51.5%; and >65: 42.9%. Chicken livers were eaten by half (51.0%) of respondents belonging to UK socioeconomic grouping ABC1 (upper, middle, and lower middle class) and 32.3% of those belonging to C2DE (working class and those at the lowest level of subsistence).

Figure 3. Rarest chicken livers visually identified by members of the public as complying with FSA cooking guidelines and associated core temperatures and probabilities ofCampylobacter survival in survey to determine preferences and...

Members of the public poorly identified whether a chicken liver met FSA guidelines for safe cooking (Figure 3). Thirty percent identified livers 1–3 as being safe to eat; the predicted rates of Campylobacter survival in these livers were 48%–98%. Another 22% thought that liver 4 (Campylobacter survival rate 22%) was safe to eat.

Figure 4. Proportion of public identifying which chicken liver dishes they preferred and which they believed complied with FSA cooking guidelines in survey to determine preferences and knowledge of safe cooking practices among...

No significant difference was found between the public’s choices of FSA-compliant livers and their preferences when dining out (p = 0.776, Wilcoxon signed-rank test; n = 386) (Figure 4); respondents were consistent between what they wanted to eat and what they thought was safe. Respondents showed a significant preference for pinker livers when eating out rather than at home (p = 0.007, Wilcoxon signed-rank test; n = 446). Paradoxically, respondents reported being more concerned about food safety when eating out than at home (p<0.001, Wilcoxon signed-rank test; n = 999).

Ordered logit results (not reported) identified no systematic differences in rareness preferences by respondent sex, age, or class. Livers that were more pink were preferred by respondents who described themselves as adventurous (p<0.030, n = 444) and who were less concerned about restaurant food safety (p<0.001, n = 444).

Perceptions and Knowledge of Chefs

Among the 143 chefs, of those who indicated their sex, 134 (88%) were male. Among the 141 who indicated their type of work, 31.9% worked in fine dining, 17% in contract catering, 11.3% in casual restaurants, 5.7% in pubs, and 19.1% in multiple kitchen types. The most commonly held position among 131 chefs who responded was head chef (54.0%), followed by chef trainer (11.5%), chef de partie (10.7%), commis chef (6.9%), and sous chef (6.1%).

Figure 5. Proportion of chefs identifying which chicken liver dishes they preferred and which they believed complied with FSA cooking guidelines in survey to determine preferences and knowledge of safe cooking practices among...

Chefs were much better than members of the public at

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