Prion Disease in Dromedary Camels, Algeria

Abstract

Prions cause fatal and transmissible neurodegenerative diseases, including Creutzfeldt-Jakob disease in humans, scrapie in small ruminants, and bovine spongiform encephalopathy (BSE). After the BSE epidemic, and the associated human infections, began in 1996 in the United Kingdom, general concerns have been raised about animal prions. We detected a prion disease in dromedary camels (Camelus dromedarius) in Algeria. Symptoms suggesting prion disease occurred in 3.1% of dromedaries brought for slaughter to the Ouargla abattoir in 2015-2016. We confirmed diagnosis by detecting pathognomonic neurodegeneration and disease-specific prion protein (PrP^Sc) in brain tissues from 3 symptomatic animals. Prion detection in lymphoid tissues is suggestive of the infectious nature of the disease. PrP^Sc biochemical characterization showed differences with BSE and scrapie. Our identification of this prion disease in a geographically widespread livestock species requires urgent enforcement of surveillance and assessment of the potential risks to human and animal health.

Keywords: Camelus dromedarius; Creutzfeldt-Jakob disease; Prion disease; bovine spongiform encephalopathy; camel prion disease; dromedary camels; prions; zoonoses.

Video 1

Dromedary camel found in the desert with difficulty getting up. At the abattoir, the animal showed aggressiveness (kicking). It became nervous when forced to cross an obstacle and showed the down and upwards movements of the head and teeth grinding. (Ahead of print - Video available in finalized issue)

Video 2

Dromedary camel waiting at the Ouargla abattoir for antemortem inspection. The animal shows down and upwards movements of the head and teeth grinding. (Ahead of print - Video available in finalized issue)

Figure 1

Hematoxylin and eosin staining (A, B), immunohistochemistry (C–O), and paraffin-embedded tissue blot analysis (P–S) of brains of dromedary camels brought for slaughter to the Ouargla abattoir, Algeria, 2016–2017. Spongiform change of neuropil, gliosis, and neuronal loss in thalamus (A) and intraneuronal vacuolation in pons (B) (scale bar = 50 μm). Immunohistochemistry for prion protein (PrP^Sc) with L42 monoclonal antibody evidenced dense synaptic/punctate deposition in thalamus (C) and intraneuronal and extraneuronal PrP^Sc deposits in pons (D), accompanied by spongiform change. Perineuronal, diffused in neuropil and glial-associated PrP^Sc staining were also observed in the nucleus of the solitary tract (E) and cerebellum (F), which showed rare vacuoles (scale bars = 50 μm). Immunohistochemical analysis performed on brains of symptomatic dromedaries revealed several PrP^Sc deposition patterns, such as synaptic/punctate pattern diffused in the neuropil (G); intraneuronal deposition in pyramidal cells of hippocampus (H); perineuronal and linear staining in frontal cortex (I); intraglial PrP^Sc deposition (J–L); perivascular deposition (M); atypical intracellular PrP^Sc deposition pattern in pons (N). PrP^Sc was absent in asymptomatic dromedary used as negative control (O) (scale bars = 50 μm). PrP^Sc distribution, by paraffin-embedded tissue blot analysis, was observed in several brain areas, such as prefrontal cortex (P), hippocampus (Q), cerebellum (R), and a sagittal section of pons (S) (scale bar = 3 mm).

Figure 2

Prion protein immunolabeling in the germinal center of lymphoid follicles of cervical (A) and prescapular (B) lymph nodes of dromedary camel no. 8, Ouargla abattoir, Algeria. The architecture of lymph nodes appears moderately compromised by the partial freezing of samples that accidentally occurred before fixation. Scale bars = 50 μm. Inset in panel A: higher magnification showing the germinal center marked with asterisk; scale bar = 25 mm.

Figure 3

Western blot analysis of protein-resistant core (PrP^res) of pathological dromedary prion protein. A) Western blot analysis of proteinase K (PK)–treated PrP^Sc in brain homogenates from dromedary camels with neurologic symptoms (nos. 4 and 8), Algeria. A sample of sheep scrapie was loaded as control (indicated as C+). Membranes were probed with L42 (left) and 12B2 monoclonal antibody (mAb) (right). Molecular weights (kDa) are indicated on the left. Tissue equivalents loaded per lane were 2 mg for camel samples and 0.1 mg for sheep scrapie. B) Samples after deglycosylation. Membrane was probed with L42 mAb. C) Comparison of dromedary PrP^res (from camel no. 4) with sheep bovine spongiform encephalopathy (BSE), bovine BSE, and sheep scrapie samples by ISS (Istituto Superiore di Sanità) discriminatory Western blot (17). Tissue equivalents loaded per lane were 2 mg for dromedary camel and bovine samples and 0.1 mg for sheep samples. In each blot, samples were loaded as follows: lane 1, ovine BSE; lane 2, bovine BSE; lane 3, dromedary camel no. 4; lane 4, ovine scrapie. Membranes were probed with L42, 12B2, and SAF32 mAbs, as indicated. For the analyses in panels B and C, protein standards were loaded and are indicated as M.

Video 3

Dromedary camels gathering and scavenging the waste dumps in the desert near an oil extraction plant. (Ahead of print - Video available in finalized issue)