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Prion Disease in Dromedary Camels, Algeria

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Prion Disease in Dromedary Camels, Algeria Prion Disease in Dromedary Camels, Algeria Baaissa Babelhadj, Michele Angelo Di Bari, Laura Pirisinu, Barbara Chiappini, Semir Bechir Suheil Gaouar, Geraldina Riccardi, Stefano Marcon, Umberto Agrimi, Romolo Nonno, Gabriele Vaccari Prions cause fatal and transmissible neurodegenerative expand (2). Several new prion diseases—including variant diseases, including Creutzfeldt-Jakob disease in humans, Creutzfeldt-Jakob disease, atypical/Nor98 scrapie of sheep, scrapie in small ruminants, and bovine spongiform enceph- and atypical L- and H-type BSE—have been identified in alopathy (BSE). After the BSE epidemic, and the associated the past 20 years, and chronic wasting disease (CWD) is human infections, began in 1996 in the United Kingdom, spreading dramatically across cervid populations in North general concerns have been raised about animal prions. We America and recently was discovered in Norway (3). detected a prion disease in dromedary camels (Camelus dromedarius) in Algeria. Symptoms suggesting prion dis- Public health concern increased markedly after variant ease occurred in 3.1% of dromedaries brought for slaughter Creutzfeldt-Jakob disease was demonstrated to be caused to the Ouargla abattoir in 2015–2016. We confirmed diag- by the same prion strain responsible for the BSE epidemics nosis by detecting pathognomonic neurodegeneration and (4). Unprecedented efforts were made to control the epi- disease-specific prion protein (PrPSc) in brain tissues from demics in cattle and to contain the exposure of humans to 3 symptomatic animals. Prion detection in lymphoid tissues potentially infected cattle-derived materials. is suggestive of the infectious nature of the disease. PrPSc In addition to having fatal consequences for infected biochemical characterization showed differences with BSE animals, scrapie and BSE have a serious economic effect and scrapie. Our identification of this prion disease in a geo- on the livestock industry. Scrapie brings economic damag- graphically widespread livestock species requires urgent es through production loss, export loss, and increased cost enforcement of surveillance and assessment of the poten- for carcass disposal, which account for $10–$20 million tial risks to human and animal health. annually in the United States (5). In the United Kingdom, where BSE was diagnosed in >180,000 cattle and up to 3 rions are responsible for a group of fatal and transmissi- million were likely to have been affected, the cost to the Pble neurodegenerative diseases named prion diseases. A public was >£5 billion (≈$7.1 billion US) (6). misfolded and aggregated isoform of a cell-surface protein Prion diseases can manifest as sporadic (putatively termed cellular prion protein (PrPSc) is the main, if not the spontaneous), genetic, or infectious disorders (1). In ani- sole, component of prions (1). Creutzfeldt-Jakob disease mals, disorders resembling sporadic or genetic human prion in humans and scrapie in small ruminants are the longest diseases have been reported only recently, with the discov- known diseases in this group, but prion diseases entered the ery of atypical/Nor98 scrapie in small ruminants (7) and public spotlight with the massive bovine spongiform en- L- and H-type BSE in cattle (8,9). Infectious prion diseases cephalopathy (BSE) epidemic started in 1986 in the United have been known for much longer and have been described Kingdom, revealing the zoonotic potential of animal prions. in several animal species. Some diseases derived from acci- Since the BSE epidemic begin, interest in these dis- dental transmission, as is the case with BSE, which affected eases has increased, and the prion universe has continued to millions of cattle but also involved goats, domestic cats, nonhuman primates, and wild bovid and felid species, most Author affiliations: Ecole Normale Superieure Ouargla Laboratoire likely fed with material contaminated by the BSE agent de Protection des Écosystèmes en Zones Arides et Semi Arides (10). Even the outbreaks of transmissible mink encepha- University Kasdi Merbah Ouargla, Ouargla, Algeria (B. Babelhadj); lopathy reported in the United States and various European Istituto Superiore di Sanità Department of Food Safety, Nutrition countries in ranch-raised mink most likely originated from and Veterinary Public Health, Rome, Italy (M.A. Di Bari, L. Pirisinu, feedstuff accidentally contaminated by prions 10( ). B. Chiappini, G. Riccardi, S. Marcon, U. Agrimi, R. Nonno, Despite the long list of susceptible animal species, G. Vaccari); Laboratoire de Physiopathologie et Biochimie prion diseases behave as infectious and naturally occurring de la Nutrition University Abou Bekr Bélkaid, Tlemcen, Algeria conditions only in ruminants. Scrapie affects sheep and (S.B.S. Gaouar) goats, and CWD affects different species of the Cervidae DOI: https://doi.org/10.3201/eid2406.172007 family: mule deer (Odocoileus hemionus), white-tailed Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 24, No. 6, June 2018 1029 RESEARCH deer (O. virginianus), elk (Cervus canadensis), and moose We collected brain samples from 3 dromedaries (nos. (Alces alces) (11). Furthermore, CWD has been recently 3, 4, and 8) showing neurologic symptoms and from 1 clin- diagnosed in reindeer (Rangifer tarandus) (3) and moose ically healthy animal (no. 5), as well as cervical, prescapu- (12) from Norway. lar, and lumbar aortic lymph nodes from 1 animal (no. 8). We report prion disease in dromedary camels (Cam- The animals were all females, belonging to the Sahraoui elus dromedarius) from a Saharan population in Ouargla population, 10, 11, 13, and 14 years of age, respectively. in southeastern Algeria, where the disease was observed We fixed samples in formalin for histologic and im- in animals brought for slaughter at the Ouargla abattoir. munohistochemical examination. We also collected frozen Dromedaries are widespread throughout northern and east- brain samples from animals 4 and 8 for Western blot and ern Africa, the Middle East, and part of Asia, where they genetic analysis and sampled formalin-fixed brain tissue are the means of subsistence for millions of families who from a clinically healthy animal (no. 5). We obtained brain live in the most hostile ecosystems on the planet. Since an- samples from BSE-infected cattle and from ARQ/ARQ cient times, camels have been exploited as beasts of burden sheep, either naturally affected by scrapie or experimen- and sources of milk and meat and for riding; today, they tally infected with BSE, from the surveillance system in are tremendously important as a sustainable livestock spe- Italy or from previous studies (14). cies. During the past 10 years, the camel farming system has evolved rapidly and improved substantially (13). The Neuropathologic, Immunohistochemical, emergence of a prion disease in a farmed animal species and Paraffin-Embedded Tissue Blot Analyses of such importance requires a thorough risk assessment for We embedded brain and lymph node samples in paraffin implementing evidence-based policies to control the dis- wax, sectioned at 5 µm, and stained with hematoxylin and ease in animals and minimize human exposure. eosin or subjected to immunohistochemical or paraffin-em- bedded tissue blot analysis. We pretreated sections for im- Materials and Methods munohistochemistry with 98% formic acid for 5 min, fol- lowed by autoclaving in citrate buffer for 5 min at 121°C. Animals and Tissue Samples We then treated sections with 6% normal goat serum (Vec- The Ouargla abattoir is one of the largest slaughterhouses tor Laboratories, Burlingame, CA, USA) in phosphate- in slaughtered volume for cattle, camels, and small ru- buffered saline for 60 min. We performed immunohisto- minants in Algeria. In the past 5 years, neurologic symp- chemical detection of PrPSc with L42 monoclonal antibody toms have been observed more often in adult dromedar- (mAb) (R-Biopharm, Darmstadt, Germany) at 0.01 µg/mL ies at antemortem examination. The signs include weight in phosphate-buffered saline overnight at 4°C. We treated loss; behavioral abnormalities; and neurologic signs, such sections with secondary biotinylated mouse antibody (Vec- as tremors, aggressiveness, hyperreactivity, typical down tor Laboratories), ABC Complex (Vector Laboratories) for and upward movements of the head, hesitant and uncer- 45 min, and diaminobenzidine (Sigma-Aldrich, St. Louis, tain gait, ataxia of the hind limbs, occasional falls, and dif- MO, USA) for 3 min. We used Mayer’s hematoxylin for ficulty getting up (Video 1, https://wwwnc.cdc.gov/EID/ counterstaining. Each run comprised positive- and neg- article/24/6/17-2007-V1.htm; Video 2, https://wwwnc.cdc. ative-control sections. We analyzed 3 sections from each gov/EID/article/24/6/17-2007-V2.htm). lymph node sample. According to breeders’ descriptions, the early stage We collected sections for paraffin-embedded blot of the disease was mainly characterized by behavioral on prewetted 0.45-µm–pore nitrocellulose membranes signs, such as loss of appetite and irritability. Separa- (Schleicher & Schuell, Dassel, Germany) and dried mem- tion from the herd at pastures along with aggressiveness branes for 24 h at 55°C. We performed membrane treat- and tendency to kick and bite when handled were usually ments, proteinase K (PK) (Sigma-Aldrich) digestion (50 observed. With disease progression, neurologic signs be- µg/mL), and immunodetection as described (15). We used came obvious; animals showed ataxia that eventually led mAb L42 (0.01 µg/mL) as the primary antibody.
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