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Sheep Feed and Scrapie, France Sandrine Philippe,* Christian Ducrot,† Pascal Roy,‡ Laurent Remontet,‡ Nathalie Jarrige,* and Didier Calavas*

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Sheep Feed and Scrapie, France Sandrine Philippe,* Christian Ducrot,† Pascal Roy,‡ Laurent Remontet,‡ Nathalie Jarrige,* and Didier Calavas* RESEARCH Sheep Feed and Scrapie, France Sandrine Philippe,* Christian Ducrot,† Pascal Roy,‡ Laurent Remontet,‡ Nathalie Jarrige,* and Didier Calavas* Scrapie is a small ruminant, transmissible spongiform gut-associated lymphoid tissues and the placenta are con- encephalopathy (TSE). Although in the past scrapie has not sidered highly important in spreading the disease (8) and been considered a zoonosis, the emergence of bovine can contaminate the environment (9). Because feed is con- spongiform encephalopathy, transmissible to humans and sidered to be the main, if not the only, contamination experimentally to sheep, indicates that risk exists for small source of BSE in cattle (10,11), it can also be presumed to ruminant TSEs in humans. To identify the risk factors for introducing scrapie into sheep flocks, a case-control study be a potential risk factor for scrapie in sheep. was conducted in France from 1999 to 2000. Ninety-four A case-control study of infected and scrapie-free flocks case and 350 control flocks were matched by location and was conducted to identify risk factors for scrapie in sheep main breed. Three main hypotheses were tested: direct flocks in France. Various risk factors hypotheses were test- contact between flocks, indirect environmental contact, and ed from the most plausible to the weakest. foodborne risk. Statistical analysis was performed by using adjusted generalized linear models with the complemen- Materials and Methods tary log-log link function, considering flock size as an offset. A notable effect of using proprietary concentrates and milk Study Design replacers was observed. The risk was heterogeneous among feed factories. Contacts between flocks were not A case-control study of infected and scrapie–free flocks shown to be a risk factor. was designed (see online appendix for details; http:// www.cdc.gov/ncidod/EID/vol11no08/04-1223_app.htm). A flock was defined as having at least 20 adult ewes. To crapie is a transmissible spongiform encephalopathy consider the heterogeneity of exposure to scrapie risk, S(TSE) affecting sheep and goats (1), as is Creutzfeldt- cases and controls were matched according to main sheep Jakob disease (CJD) in humans or bovine spongiform breed and location. A “case” was any flock having >1 ani- encephalopathy (BSE) in cattle. Moreover, scrapie is con- mal that had been shown as scrapie-positive by the French tagious in natural conditions (2). Though genetic determin- surveillance network from January 1996 to July 2000 (12). ism is a major feature of scrapie, the infectious agent is Four frequency-matched control flocks were randomly nonetheless needed for the disease to develop (3,4). selected from the sheep flocks in which scrapie had never Known to exist for centuries, scrapie was thought to be been reported. Flocks that did not meet this criterion were a possible origin of BSE, although this hypothesis has not excluded. yet been verified. Sheep and goats can be experimentally The suspected risk factors were grouped into 3 cate- infected with BSE, resulting in a disease that is impossible gories corresponding to the main working hypotheses of to distinguish from natural scrapie (5). Since BSE is impli- scrapie dissemination. The first category covered risks for cated in the emergence of variant CJD (6,7), the existence transmission by direct contact between flocks and indirect- of BSE in small ruminants poses a further risk for human ly through the environment. The second category covered health. Scrapie has become a public health challenge, and foodborne risks. The third category covered other environ- its propagation must be stopped; therefore, the risk factors mental dissemination risks such as equipment sharing for the introduction of scrapie in sheep must be understood. between farms or transmission through hay mites. Table 1 In sheep infected with scrapie, the infectious agent is describes the 22 potential risk factors studied. widely distributed in the organism. In particular, the Data Collection *Agence Française de Sécurité Sanitaire des Aliments, Lyon, Information was collected by using a preestablished France; †Institut National de la Recherche Agronomique, Theix, questionnaire to interview farmers and analyzing farm France; and ‡Centre Hospitalo-Universitaire Lyon-Sud, Lyon, records. Questions related to potential risk factors covered France 1274 Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 11, No. 8, August 2005 Sheep Feed and Scrapie, France the 4-year period preceding detection of the first clinical regarding potential confounding factors including flock case of scrapie in case flocks and the 4-year period preced- size, production type (dairy, meat, or mixed), and intensi- ing the interview for controls. Additionally, information fication level of the flock production was recorded Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 11, No. 8, August 2005 1275 RESEARCH (Table 2). Interviews were conducted from May 1999 to All exposures were considered as binary, and the absence July 2000 with 453 flock owners (98 cases and 355 con- of exposition was the reference modality for each risk fac- trols). Nine flocks were excluded because they did not tor. Factors notably associated with the flock status at 20% meet the inclusion criteria. A total of 444 flocks (94 cases level through univariate analysis (Table 1) were selected and 350 controls) were included in the study. Data were for subsequent multivariate analyses. The univariate analy- encoded and then stored in an Access database (Microsoft sis consisted of the construction of a Clog-log model for Access 97 SR-2, Microsoft Corporation, Redmond, WA, each risk factor; strata were systematically introduced as USA). covariate. Furthermore, 2 distinct multivariate models were applied to consider colinearity between feed type and Study Sample feed factories in the foodborne risk study. The first model The flocks were mainly located in 2 departments (multivariate Clog-log 1) analyzed feed types without (Pyrénées Atlantiques, n = 267/444, Aveyron n = 51/444). regard to factories, whereas the second one (multivariate The others were widely distributed throughout metropoli- Clog-log 2) evaluated the risk according to the feed facto- tan France. Ten mixed breeds and 23 pure breeds were ries that produced milk replacers and proprietary concen- included in the study. The flocks were mainly specialized trates. Regarding the proprietary feed factories, only the in 1 type of production (66% in dairy production, 32% in purchase of milk replacers and proprietary concentrates at meat production) (Table 2). The flock size ranged from 21 factory 1 and the purchase of proprietary concentrates at to 1,787 ewes (mean 274, SD 198). factory 2 occurred frequently enough to be studied sepa- rately. Statistical software Splus (S-Plus 2000 Professional Analysis Release 2, Mathsoft, Inc., Seattle, WA, USA) was used to Data analysis was conducted in 2 steps by using statis- analyze the data. tical models adjusted for the 2 matching factors through the corresponding cross-variable “strata” (main breed and Results location) treated as a stratification variable (13). First, to According to the univariate analysis, 8 potential risk identify the confounding factors to be further analyzed factors were selected (Table 1). Six risk factors were relat- (14), a log-linear model considered 5 factors, including ed to foodborne risk; the other 2 were related to purchas- flock size (number of ewes), production type, intensifica- ing ewes, and cesarean sections performed by the tion level of the flock production as potential confounding veterinarian. The subsequent multivariate model (multi- factors, flock status, and strata. The model introduced the variate Clog-log 1) (Table 3) showed a significant associa- main effect of these 5 factors with all second interaction tion between the flock status and using milk replacers. In terms. Flock size was the only potential confounding fac- addition, using the multivariate Clog-log 2 model milk tor notably associated with the flock status (Table 2). replacers and proprietary concentrates from factory 1 were Second, to assess associations between flock status and significantly associated with the flock status (Table 3). risk factors, a generalized linear model for binary outcome was set up with the complementary log-log link function Discussion (Clog-log model) (14) (see online Appendix, available at The main finding of the study was the role of feed as a http://www.cdc.gov/ncidod/EID/vol11no08/04- risk factor for scrapie. This is consistent with what has 1223_app.htm). This model considered the flock size by been shown for BSE in cattle. The use of proprietary con- using the logarithm of the flock size as an offset (15,16). centrates, and more precisely the use of feed containing 1276 Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 11, No. 8, August 2005 Sheep Feed and Scrapie, France meat and bone meal (MBM), was shown to have a major fat is not infectious, the animal fats that were incorporated role in BSE infection of cattle (11). The agent of BSE is in milk replacers may have been contaminated. not inactivated by MBM processing methods, which were Contamination could have occurred during collection at put into place by the industry in the late 1970s (17). the slaughterhouse by contact with infectious material In France, MBM was authorized for small ruminants such as central nervous system or paravertebral ganglia. In until July 1994. Moreover, the MBM ban proved to be France, these fats were prohibited for use in farm animal <100% efficient; hundreds of BSE cases were observed in feed in November 2000. cattle in France born after the MBM ban of feed for cat- The same factory was identified as selling both the milk tle. The exposure period that was investigated in the cur- replacers and the proprietary concentrates at risk for rent study was from 1991 to June 2000, depending on the scrapie. Most farmers buy both their feed concentrates and case. It occurred before the French MBM ban in feed for milk replacers from the same wholesaler (which, in turn, all farmed animals in November 2000; furthermore, the buys from the same factory).
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