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Introduction
Reindeer and caribou (Rangifer tarandus), often called Rangifer, are wild or semi-domesticated ruminants of the family Cervidae, with seven different subspecies distributed in arctic and subarctic ecosystems (1). Reindeer and caribou are also displayed in zoological and wildlife parks all around the globe (2). Depending on migration routes, ecosystems and besides herding conditions, Rangifer are exposed to numerous infectious agents, of which some may cause illness or may exist of zoonotic concern (three). Assessing health indicators and diseases in wild ungulate populations is challenging and oft neglected, and information technology is not fully known which established and potential pathogens are circulating (four–6). In add-on to Rangifer host-specific pathogens, ruminant species kept in zoos and parks may be exposed to a wide variety of emerging and zoonotic pathogens to which they are not exposed in their native habitat, reflecting the close contact with other host species and locally occurring arthropod vectors.
Cervid herpesvirus 2 (CvHV2) is an alphaherpesvirus that is enzootic in the semi-domesticated reindeer populations in Fennoscandia and in caribou in Due north America (7, 8). In reindeer, CvHV2 can cause infectious keratoconjunctivitis (IKC) (9) as well every bit respiratory disease (10).
Bluetongue virus (BTV; genus Orbivirus, family Reoviridae) may cause bluetongue (BT) in domestic and wild ruminants (11, 12). BTV is transmitted by biting midges of the genus Culicoides, only tin can too be transmitted via directly contact or transplacental transmission (11, 13).
Malignant catarrhal fever viruses (MCFV) is a group of 10 unlike herpesviruses classified in the genus Macavirus, subfamily Gammaherpesvirinae (14). Domestic sheep (Ovis aries) are considered to be reservoir hosts of ovine herpesvirus 2 (OvHV2), while goats (Capra aegagrus hircus) are hosts of caprine herpesvirus 2 (CpHV2) (14). MCFV may atomic number 82 to fatal disease in several ruminant species including reindeer (xv, 16). Anti-MCFV-related gammaherpesvirus antibodies have been detected in semi-domesticated reindeer in Fennoscandia, with a prevalence of 3.5–3.8% (17, eighteen).
Pestivirus A (formerly Bovine Viral Diarrhea Virus 1; BVDV1) and D (formerly Border Illness Virus; BDV) are members of the genus Pestivirus, family Flaviviridae (19). The susceptibility of reindeer to pestivirus A infection has been experimentally demonstrated (xx) and a pestivirus (V60-Krefeld), phylogenetically and antigenically closely related to pestivirus D and reclassified equally a genotype of this species (nineteen), was isolated from a captive reindeer in Duisburg Zoo, Federal republic of germany (21, 22). Serological screenings have demonstrated that pestivirus infections are present in semi-domesticated reindeer in Fennoscandia (23, 24) and in caribou in Northward America (25).
Schmallenberg virus (SBV; genus Orthobunyavirus, family Peribunyaviridae) was isolated for the first time from a cow in the urban center of Schmallenberg, Germany, in 2011, and spread chop-chop to about of Europe (26, 27). The virus is transmitted past arthropod vectors, of which biting midges (Culicoides spp.) are considered the almost of import (28). In domestic ruminants, the virus may crusade mummified fetuses, premature birth, and congenital malformations (27–29). No reports be on SBV in reindeer, or in any other host species in regions inhabited past wild or semi-domesticated reindeer (30).
The genus Brucella (family Brucellaceae) consists of multiple species with a broad variety of host preferences (31). Brucella suis biovar 4 is the causative agent of brucellosis in Rangifer (32) and may cause clinical signs nearly ofttimes associated with the reproductive systems (abortion, stillbirth, male sterility) and joints (synovitis and bursitis). The disease is also known every bit "rangiferine" brucellosis and continues to be an important public health business organisation in the Arctic, where many people depend on reindeer and caribou for their subsistence (33).
Toxoplasma gondii and Neospora caninum are both obligate intracellular coccidia with carnivore definitive hosts and a variety of intermediate hosts, including wild and domestic ruminants (34, 35). Several serological screenings have been performed in wild and convict cervids, with a seroprevalence varying from 0.9 to 34.0% for T. gondii and from 0.5 to twoscore.5% for North. caninum (34–38).
Anaplasma phagocytophilum is a tick-borne obligate intracellular bacterium that causes granulocytic anaplasmosis in humans but likewise in mammals such as dogs and ruminants (39). Wild ruminants (genus Cervus, Capreolus and Rupicapra) are expected to be master reservoirs in Europe (forty). There is only one report of A. phagocytophilum infection in reindeer from Kingdom of norway (41) but a high prevalence (80.0%) of Anaplasma ovis was found by PCR in reindeer from Mongolia (42). An experimental infection of Rangifer t. tarandus with A. phagocytophilum resulted in severe clinical symptoms such equally anemia and inappetence and 1 fatal case (43).
The aim of this study was to investigate the possible circulation of all tested pathogens in the selected captive reindeer populations in Deutschland, also as the possible role of convict reindeer as reservoir hosts for important pathogens of other domestic, convict and wild ruminant species.
Materials and Methods
Animals and Sampling
In a previous study on Babesia spp. in reindeer (R. t. tarandus) in zoos and wild animals parks in Deutschland (44), 33 facilities with reindeer were identified and contacted. Sixteen of these facilities, distributed throughout the country and property ~fifty% of all captive reindeer in Germany at that time, were called as sampling sites (Figure 1). Samples were taken from 123 reindeer of different age and sex (Tabular array 1). None of the animals showed whatever clinical signs of affliction at the fourth dimension of sampling. Husbandry characteristics and individual medical histories were obtained for each animal via standardized questionnaires and registered in a database.
Figure 1. Locations of animal facilities with reindeer (Rangifer t. tarandus) in Germany selected for sampling for the investigation of exposure to infectious agents.
Tabular array 1. List of sampling sites of convict reindeer (Rangifer t. tarandus) with number and historic period of animals tested.
Claret and Tick Sample Collection
EDTA blood samples and serum samples from reindeer were available from a previous study (44). For the same previous study, 49 ticks were collected from 22 reindeer in 7 different facilities equally previously described (44). All ticks were identified as adult stages of Ixodes ricinus (14 males and 35 females). Whole blood samples, serum samples and ticks were stored at −twenty°C until farther examination (44). For our study, 118 samples could exist tested against the complete console, while 1 of the samples was tested against 4 pathogens only, due to volume restrictions.
Dna Extraction
DNA was extracted from whole claret samples and ticks as previously described (44) and DNA concentration was measured by spectrophotometry (Nanodrop 2000c, Thermo Scientific, USA).
Serology
Sera were tested past ELISA for the presence of antibodies against seven pathogens known to cause disease in reindeer or other cervids (Table 2).
Table 2. Enzyme-linked immunosorbent assays (ELISA) used for investigating captive reindeer (Rangifer t. tarandus) in Germany for exposure to infectious agents.
Molecular Testing
The Dna concentration of the extracts from blood and tick samples were adjusted to 25 ng/μl for each sample. Diluted DNA samples were analyzed for the presence of Dna specific to A. phagocytophilum past PCR. Samples were tested with a real-time PCR protocol for the partial msp2 gene (77 bp) (49). Samples yielding a positive result were further analyzed by semi-nested PCR for the partial groEL gene (573 bp) (50) and by a nested PCR targeting the partial 16S rRNA gene (546 bp) (51). PCR products were purified (QIAquick PCR Purification Kit; Qiagen, Hilden, Frg) prior to sequencing as previously described (forty). Sequences were analyzed, aligned and compared with sequences deposited in GenBank with BLASTn (National Center for Biotechnology Information, Bethesda MD, USA) using the Bionumerics Software (Version 7.vi.ane. Applied Maths, Inc., Austin, TX, USA).
Statistical Analysis and Multivariate Correspondence Analysis
Conviction intervals (95% CI) for seroprevalence rates were determined past the Clopper and Pearson method with Graph Pad Software (Graph Pad Software Inc., San Diego, Ca., The states). Independence of compared samples was analyzed with the chi-squared test.
Multiple correspondence assay (MCA) (52) was used to explore relationships between the explanatory variables using the package FactoMineR (53) in R Core Squad (54). Individual MCA analyses were performed on each pathogen using a combination of the following parameters: sex, age class (calf <1 twelvemonth onetime, juvenile between 1 and 2 years old, developed >2 years old), origin of the individual (i.e., imported from away, translocated from other parts of Germany or in-house zoo-bred), neighboring species (grouped in cervids, other artiodactyla, perissodactyla, carnivora and birds), presence of vegetation, rodent control and antiparasitic treatment (Ivermectin) (Table two).
Results
Serology
Due to small volumes of sera available, not all samples from the 123 individual reindeer were available for testing in all assays. Results are summarized in Table iii.
Table 3. Presence and prevalence of antibodies confronting a range of infectious agents in captive reindeer (Rangifer t. tarandus) in Deutschland (2013), presented as seropositive/tested (percentage and confidence interval) by age grouping.
Alphaherpesvirus
24 samples were positive for the presence of antibodies against alphaherpesviruses (northward = 119; 20.iii%; CI: xiii.9–28.iii). Seroprevalence increased with age, with 10.7% (CI: 2.9–28.0) for calves, 12.five% (CI: 3.five–31.viii) for juveniles and 26.9% (CI: 17.7–38.6) for adults.
BTV
4 out of 119 animals had antibodies against BTV (iii.iv%; CI: 1.0–8.7). All seropositive animals were adults (n = 67).
MCFV-Related Gammaherpesvirus
Antibodies against MCFV-related gammaherpesvirus were detected in seven out of 119 animals (5.9%; CI: 2.7–11.nine).
Pestivirus
Five out of 118 serum samples were positive for the presence of antibodies confronting pestivirus (4.2%; CI: 1.6–nine.8).
SBV
Antibodies against SBV were detected in 70 out of 118 reindeer (59.iii%; CI: l.3–67.8), with increasing prevalence with age; 14.3% (CI: five.1–32.ane) in calves, 58.3% (CI: 38.8–75.half dozen) in juveniles and 75.eight% (CI: 64.one–84.6) in older animals.
Brucella spp.
Anti-Brucella antibodies were detected in 1 healthy adult female reindeer (northward = 118; 0.nine%; CI: 0–5.1).
Neospora caninum
Antibodies against N. caninum were nowadays in v of 118 reindeer (iv.2%; CI: i.half-dozen–ix.8).
Toxoplasma gondii
62 out of 119 tested reindeer were positive for the presence of antibodies against T. gondii (52.1%; CI: 43.2–60.9). Seroprevalence increased with historic period, being vii.i% (CI: 0.9–23.seven) in calves, 33.3% (CI: 17.8–53.iv) in juveniles, and 76.ane% (CI: 64.six–84.8) in developed reindeer.
The seroprevalence was significantly college for pathogens of which the prevalence was positively linked with age (χ2 = 225.5; p < 0.0001), i.e., alphaherpesvirus, SBV and T. gondii.
Molecular Testing on Anaplasma phagocytophilum
Seventeen of 123 reindeer (13.eight%; CI: 8.vii–21.one) were positive for A. phagocytophilum Dna past real-time PCR targeting the msp2 factor. Assay of the groEL factor yielded positive results for nine of these. PCR amplicon sequences from vi out of these nine reindeer showed 99–100% identity to ecotype 2 (55), whereas the remaining iii showed 99% similarity to ecotype ane. Thirteen of the 17 samples (76.iv%) positive with the msp2 gene likewise generated PCR amplicons when testing with primers targeting the 16s rRNA factor. Vi of these 13 samples showed 100% identity to strain "16S−22 Y" (51), iv showed 99–100% identity to strain "16S−21 X," ii showed 99% similarity to "16S−8 J" and one showed 100% identity to strain "16S-20 Due west."
Fifteen out of 49 ticks (xxx.vi%; CI: 19.four–44.6) were PCR-positive for A. phagocytophilum. These fifteen ticks had been collected from v individual reindeer from two different facilities. The prevalence for A. phagocytophilum did non differ significantly (P = 0.7349) between males (35.7%) and females (28.six%). Due to the high CT value obtained from ticks, only one tick yielded a positive issue concerning the 16S rRNA gene ("16S-21 X"), matching the issue of the reindeer from which it was collected. Three of the five reindeer with ticks having A. phagocytophilum DNA too had such Deoxyribonucleic acid in the blood.
Multivariate Analysis
Brucella, pestivirus, MCFV-related gammaherpesvirus, BTV and Neospora antibodies were found in few individuals only, thus the interpretation of MCA was not conclusive due to the scarcity of data. MCA showed an association betwixt having alphaherpesvirus antibodies and being imported to Frg from abroad. Schmallenberg virus antibodies were present predominantly in developed individuals, thus historic period was identified as the most relevant variable, followed by the presence of vegetation in the enclosure. Toxoplasma, on the other hand, was positively related to presence of neighboring cervids and vegetation, and negatively related to the presence of carnivores in neighboring enclosures. Finally, the detection of Anaplasma-DNA was positively associated with being corralled with other herbivores. Detailed MCA results are displayed in Appendix 1 (Supplementary Material).
Discussion
The reindeer alphaherpesvirus (CvHV2) is widespread among wild and semi-domesticated reindeer populations (7, 8). The lower seroprevalence against alphaherpesviruses in adult reindeer reported in this study (26.9%) as compared with seroprevalence found in developed wild and semi-domesticated reindeer (~50.0%) (three, 7), may suggest that captive animals are less decumbent to stress events that could facilitate reactivation and spread of a latent herpesvirus infection. All the same, if simply the facilities in which there are seropositive animals are selected, seroprevalence in adult animals increases to fifty.0% (northward = 36), ranging between 22.2 and 100.0%, and MCA analysis pointed to the importance of importing reindeer from abroad in the manual of alphaherpesviruses. This finding suggests that facilities with CvHV2-seronegative reindeer have most probably avoided the contact of their reindeer with CvHV2-infected animals, either through the import of unexposed animals or past replenishing their stock through their own breeding programme.
BTV tin can infect a wide range of domestic animals, but also nigh species of wild ruminants are susceptible (11, 12, 56). Bluetongue epizootics occurred in Deutschland in 2006–2009, with more 1.8 1000000 domestic ruminants exposed to the virus and generating high mortality rates amongst infected sheep (57). Despite the appearance of the illness in Scandinavia in 2007–2009, there are no indications that wild or semi-domesticated reindeer were exposed to BTV. Recent serological screenings in Norway and Finland revealed no antibodies against BTV in semi-domesticated reindeer (xxx). Prophylactic immunization of susceptible populations seems to be the nearly effective way of controlling the disease, but later the annunciation of Germany every bit a Bluetongue disease-complimentary country in 2012, the vaccination against BTV was forbidden and information technology is therefore not available for the captive reindeer population and other captive wild ruminants (58). Four seropositive adult reindeer (6.0%) were detected in our study, indicating that reindeer were exposed to BTV, only in that location are no indications these animals became sick upon exposure. As samples were taken in 2013, the fact that simply adult animals showed antibody titers fits nicely to the emptying of the circulation of the virus in Germany 2 years earlier.
Seven reindeer had antibodies against MCFV-related gammaherpesvirus (five.9%), which is in line with the prevalence detected in wild and semi-domesticated reindeer in Fennoscandia (17, xviii) and caribou in Alaska (59). Transmission of MCFVs to reindeer in zoo settings may exist associated with the contact of the animals with captive wild sheep (Ovis spp.) and goat species (Capra spp.) (xv). Due to the low prevalence of antibodies against these pathogens, it was not possible to written report this relation in our MCA model. With the lack of a suitable vaccine against MCFVs in reindeer, it would exist recommended not to proceed them in close proximity to sheep and goat species (15).
An eradication entrada confronting BVDV (Pestivirus A and B) has been enforced in Frg since 2011 and it is considered to be in the final stage of eradication (sixty). However, screenings for BVDV antibodies in wild ruminants in Europe reported the incidental spillover of the virus from cattle to cervids (28, 61). The detection of antibodies against pestivirus in reindeer in this study (4.ii%) indicates the exposure to a virus from this genus in the convict reindeer in Frg. However, antibodies against pestivirus are routinely detected in semi-domesticated reindeer from BVDV-costless countries, i.eastward., Norway, Sweden and Republic of finland (xviii, 23, 24). These findings, together with the isolation of a pestivirus (V60-Krefeld; Reindeer-1), phylogenetically and antigenically more than closely related to Pestivirus D (old BDV) than Pestivirus A or B (quondam BVDV1 and BVDV2) in Duisburg Zoo (Germany) (21, 22), suggest that the pestivirus in question may not be Pestivirus A or B, but rather a virus more than specific to reindeer or cervids. Notwithstanding, further studies characterizing the pestivirus infecting zoo-kept reindeer are necessary to draw whatever business firm conclusions about the nature of the exposure.
Serological screenings have demonstrated the presence of antibodies against SBV in a diversity of wild ruminants in Europe (28). Nonetheless, serological screening of 187 wild (2010–2013) and 450 semi-domesticated reindeer (2013–2015) in Norway, and 635 semi-domesticated reindeer in Republic of finland, all R. t. tarandus, revealed no antibodies against SBV (30) and, to our cognition, in that location are no reports on SBV in reindeer. A seroprevalence of 59.three% was detected for SBV in this study (Table 3). Adult (75.8%) and juvenile animals (58.3%) had a significantly college seroprevalence than calves (14.3%), suggesting that almost animals could take been exposed during the 2011–2012 outbreaks in Deutschland. The seroprevalence in our study was comparable to the ane in German cattle (61.0%) and Belgian roe deer (63.0%) in the aforementioned flow (27, 61). The lower seroprevalence detected amid calves is in line with the fact that SBV was only sporadically detected in 2013 (62), when the outbreak was fading out.
Anti-Brucella antibodies were detected in one healthy reindeer. The ELISA used in this study detects antibodies against shine Brucella spp. lipopolysaccharides (LPS) in reindeer (46). B. suis biovar 4 is the only Brucella species isolated from Rangifer (32), but to our knowledge, B. suis biovar two is the only one known to occur in Frg thus far, with seroprevalence rates upwards to 28.5% in wild boar depending on the geographic region in the country (63). Brucella suis biovar two has been reported to infect cattle, and spill over from wild boar was assumed to be the source of infection (64).
Serological cross-reactions and faux positives may occur when detecting anti-Brucella antibodies. In cattle, an immune response of the animate being to other microorganisms sharing epitopes with brucellae O-polysaccharides (65), like due east.g., Yersinia enterocolitica O:9, may crusade false positives (66). Investigation of fecal samples (north = 2,243) from eight herds of semi-domesticated reindeer in Kingdom of norway and Finland yielded detection of Yersinia spp., but no detection of Y. enterocolitica O:9 (67). Since also other microorganisms may be serologically cantankerous-reacting agents, serological results should e'er exist interpreted with circumspection and the gold standard in brucellosis diagnostics nevertheless remains bacterial isolation.
Ane of the virtually common wellness challenges for captive reindeer are parasitic diseases (3). For T. gondii, large differences in seroprevalence have been reported among reindeer and caribou populations, from 0.9 to 1.0% in wild and semi-domesticated reindeer in Fennoscandia (38, 68) to 37.0% in arid-basis caribou (R. tarandus groenlandicus) in Canada (69). Toxoplasma gondii antibodies were detected in 52.1% of the studied zoo reindeer population, with 76.1% of the developed reindeer being exposed to the parasite. In this study, MCA revealed a positive relation betwixt the presence of antibodies confronting T. gondii and the presence of vegetation, while it was negatively associated with the presence of carnivores in neighboring enclosures. These findings may exist explained past the ecology of toxoplasmosis, with domestic and wild cats being master hosts and their feces being the carriers of the infective oocysts. The presence of vegetation may increment the presence of small rodents, common cat preys, in the reindeer facilities, while the absence of other predators in the vicinity may as well contribute to the colonization of the area by domestic and feral cats which tin contaminate the pasture and other food resources with their feces (35). With this information in listen, pasture maintenance, together with rodent and cat control would probably help to reduce the prevalence of toxoplasmosis in convict reindeer. Nevertheless, a review paper by Hide et al. (70) discussed the vertical manual of T. gondii every bit an important factor in the ecology of this parasite in sheep, with congenital transmission in up to 66% of pregnancies. Nevertheless, the importance of vertical manual in sheep and other animals is still under give-and-take (70), and further studies in reindeer should exist conducted in order to analyze if that is besides the case in this species.
Anaplasma phagocytophilum is known to crusade tick-borne fever in cattle and infect gratuitous-ranging wild ruminant species in Germany (40, 71, 72). The finding of A. phagocytophilum DNA in reindeer blood and in ticks from the same animals confirms the function of ticks as vectors, too in zoo-kept animals. However, the lack of clinical signs of disease in the studied population advise that subclinical anaplasmosis may be more mutual than clinical infections in captive reindeer. No specific risk factors could be identified by MCA. The genetic types 16S-22Y, 16S-21X, and 16S-8J are well-known to be nowadays in a diverseness of wild cervids in Europe, merely, although sometimes detected in cervids, 16S-20W is mostly found in cattle (72). This further provides evidence for the interspecies exchange of this pathogen in particular in the context of a zoo. Male person ticks which rarely feed on hosts showed almost the aforementioned prevalence charge per unit as females. Transstadial transmission for A. phagocytophilum has been reported in ticks and may explain the high prevalence in males (73). However, since infected animals remain life-long carriers, subclinical infections could have been maintained without the regular presence of ticks in the enclosure (39). Anaplasmosis should definitely be included in the differential diagnosis whenever zoo-kept reindeer show signs consequent with tick-borne fever.
Nearly animal facilities have routines for addressing wellness parameters and infectious diseases, as well in animals non displaying clinical signs, and especially for import and export purposes. Nevertheless, local vector populations, such as ticks, only maybe besides mosquitos and midges, should be screened for pathogens like BTV, SBV, A. phagocytophilum and others.
Conclusions
The results of our analyses confirmed the exposure to all tested pathogens in the selected captive reindeer populations in Germany. The captive reindeer populations may thus serve as reservoir hosts for important pathogens that are circulating in local domestic, captive, and wild ruminant populations and arthropod vectors. These findings indicate that zoo animals should exist included in national surveillance and control programs. The detection of antibodies against BTV was of special interest, since this pathogen was included in the German surveillance programs at the time of the sampling. Furthermore, animals infected with BTV were detected in areas where the diseases were not reported in other species at the fourth dimension of the sampling.
Data Availability Statement
The datasets generated for this report can be found in https://dataverse.no/dataset.xhtml?persistentId=doi:10.18710/4PQKKQ.
Ideals Statement
Claret samples were taken for preventive medical care and leftovers were used for this study. When this was not the example, a research proposal was submitted to the advisable authorities and approved (Landesamt für Landwirtschaft, Lebensmittelsicherheit und Fischerei Mecklenburg-Vorpommern, file number 7221.three-two-034/xiii). All procedures were performed in compliance with relevant laws.
Author Contributions
JS and LG organized the dataset. JS, LG, and AO wrote the first draft of the manuscript. MT and MP secured funding for the study and organized the sampling and analyses. AO conducted the statistical analyses. FA-One thousand conducted the multivariate analyses. LG did the sampling of animals. AO, NK, and MP contributed to the processing and examination of the samples. All authors contributed to the laboratory analyses and contributed to the writing and accepted the final version of the manuscript.
Funding
The publication charges for this article have been funded by a grant from the publication fund of UiT The Arctic University of Kingdom of norway.
Conflict of Interest
LG was employed by Zoo Duisburg AG.
The remaining authors declare that the inquiry was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of involvement.
Acknowledgments
We thank Eva Marie Breines and Ellinor Hareide, UiT Arctic University of Norway, for fantabulous help in the lab.
Supplementary Material
The Supplementary Fabric for this article can be establish online at: https://www.frontiersin.org/articles/ten.3389/fvets.2019.00461/full#supplementary-cloth
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