Courtesy of Dr. Gema Álvarez García.
Besnoitiosis, caused by tissue cyst–forming apicomplexan parasites of the genus Besnoitia, is usually a chronic and debilitating disease characterized by skin lesions and systemic clinical signs of varying severity. The disease compromises welfare and is responsible for severe economic losses: infected cattle may lose weight and have decreased milk production, dams may abort during the febrile stage, males may develop infertility or even sterility, and the hides of affected animals are of reduced value for leather production. Skin lesions and visible scleral tissue cysts characteristic of the chronic disease are similar in the different ungulate species affected. There are no effective treatments. For control in cattle, the only permitted vaccine worldwide is a live vaccine used to immunize imported bulls in Israel. Thus, control relies entirely on accurate diagnosis and herd management.
Etiology of Besnoitiosis in Animals
Genus Besnoitia belongs to a group of cyst-forming coccidians (subphylum Apicomplexa, family Sarcocystidae) related to Toxoplasma gondii and Neospora caninum. Besnoitia comprises 10 species currently recognized: B akadoni, B bennetti, B besnoiti, B caprae, B darlingi, B jellisoni, B neotomofelis, B oryctofelisi, B tarandi, and B wallacei. Several of these species have both definitive and intermediate hosts (heteroxenous life cycle). However, the identity of the definitive host remains unknown for B besnoiti, B tarandi, B bennetti, and B caprae, which infect ungulates (bovids, wild ruminants, equids, and goats, respectively) that act as intermediate hosts. The table summarizes the species included in the Besnoitia genus, their intermediate hosts (ungulates, rodents, lagomorphs, marsupials, or reptiles) and final hosts (if known), and their geographic distribution.
Courtesy of Dr. Gema Álvarez García.
Intermediate hosts harbor two asexual parasitic stages: tachyzoites and the cyst-forming bradyzoites responsible for the acute and chronic stages of the disease, respectively. Upon infection, tachyzoites proliferate mainly in endothelial cells. Next, tachyzoites transform into bradyzoites to evade the host's immune response, and they pack inside thick-walled cysts, which are found mostly in subcutaneous tissues and mucous membranes during the chronic stage of the disease and are considered pathognomonic of the disease.
Epidemiology of Besnoitiosis in Animals
Natural hosts and geographic distribution of Besnoitia spp
Species | Intermediate hosts | Definitive hosts | Geographic distribution |
|---|---|---|---|
B besnoiti | Bovine, antelope (Aepyceros melampus), impala, blue wildebeest (Connochaetes taurinus), red deer (Cervus elaphus), roe deer (Capreolus capreolus) | Unknowne | Africa, Asia, Europe, and Venezuela |
B bennetti | Donkey (Equus africanus asinus), horse (E ferus caballus) and zebra (E zebra, E quagga, E grevyi) | Unknowne | Africa, Asia, US, and France |
B caprae | Goat (Capra aegagrus hircus) | Unknowne | Iran and Kenya |
B tarandi | Muskox (Ovibos moschatus), reindeer (Rangifer tarandus), mule deer (Odocoileus hemionus) | Unknowne | Canada, Finland, Russia, and Sweden |
B akodoni | Akodon motensisa | Unknown | Brazilf |
B jellisoni | Dipodomys sppa, Peromyscus maniculatusa | Unknown | US |
B darlingi | Ameivab, Basiliscusb, Didelphis marsupialisc | Cat (Felis catus) | US and Panama |
B neotomofelis | Neotoma micropusa | Cat (Felis catus) | USg |
B oryctofelisi | Oryctolagus cuniculusd | Cat (Felis catus) | Argentinah |
B wallacei | Rattus exulansa | Cat (Felis catus) | Australia, Hawaii, Japan, and Kenya |
arodent breptile cmarsupial dlagomorph eA carnivorous definitive host is suspected for B besnoiti. One study (Peteshev VM, Galuzo IG, Polomoshnov AP. Cats—definitive hosts of Besnoitia (Besnoitia besnoiti). Izvest Akad Nauk Kazakh Ser Biol 1974;1:33–38) suggested the role of felids as definitive hosts. However, extensive studies carried out by other authors have been inconclusive. fDubey JP, Sreekumar C, Lindsay DS, Hill D, Rosenthal BM, Venturini L, Venturini MC, Greiner EC. Besnoitia oryctofelisi n. sp. (Protozoa: Apicomplexa) from domestic rabbits. Parasitology. 2003 Jun;126(Pt 6):521-39. PMID: 12879849. gDubey JP, Yabsley MJ. Besnoitia neotomofelis n. sp. (Protozoa: Apicomplexa) from the southern plains woodrat ( Neotoma micropus). Parasitology. 2010 Oct;137(12):1731-47. doi: 10.1017/S0031182010000636. Epub 2010 Jun 21. PMID: 20561393. hDubey JP, Sreekumar C, Rosenthal BM, Lindsay DS, Grisard EC, Vitor RW. Biological and molecular characterization of Besnoitia akodoni n.sp. (Protozoa: Apicomplexa) from the rodent Akodon montensis in Brazil. Parassitologia. 2003 Jun;45(2):61-70. PMID: 15266998. | |||
Bovine besnoitiosis is considered a reemerging disease in Europe, and it is widely distributed in sub-Saharan countries; besnoitiosis in reindeer and caribou populations is present in Arctic regions of North America and Europe; besnoitiosis in goats is restricted to a few countries, such as Iran and Kenya; besnoitiosis in equids has been reported in France and Belgium, and there are endemic cases in the US.
Courtesy of Dr. Gema Álvarez García.
In cattle, it has been postulated that transmission occurs mainly through direct contact between infected and noninfected animals. Tissue cysts can be present in penis mucosa and vestibulum vaginae, and tissue cysts can be ruptured and bradyzoites may cross mucosal barriers. Accordingly, parasite transmission may be favored by natural breeding. Mechanical transmission of B besnoiti was also achieved experimentally either with a syringe or with bloodsucking insects.
The role of arthropods in parasite transmission is also supported by the seasonal incidence of the disease. Arthropods have a restricted range of transmission, and the parasites that they harbor might be either tachyzoites or bradyzoites. Cats that are definitive hosts of these parasites get infected after consuming prey (eg, rodents) harboring tissue cysts; after intestinal replication similar to other coccidia, cats shed nonsporulated oocysts in their feces. Oocysts sporulate in the environment and are the infectious form for intermediate hosts by the oral route.
Clinical Findings of Besnoitiosis in Animals
Courtesy of Dr. Gema Álvarez García.
Courtesy of Dr. Gema Álvarez García.
Courtesy of Dr. Gema Álvarez García.
Courtesy of Dr. Gema Álvarez García.
Once cattle are infected with B besnoiti, the incubation period may last from 2 weeks up to 2 months. Next, bovine besnoitiosis progresses in two sequential phases: febrile acute (anasarca) and chronic (scleroderma).
The acute stage of the disease, which may go undetected, starts with fever when tachyzoites are invading the endothelia of blood vessels. Then, vascular permeability increases with the subsequent edema. Degenerative and fibrinoid necrotic vascular lesions, vasculitis, and thrombosis also develop, mainly in skin and testes. During this stage, swelling of superficial lymph nodes, inappetence, hyperemia of the skin, orchitis, and lameness may arise. In severe cases, edema in alveolar and interstitial tissues in the lungs, accompanied by pneumonitis and emphysema, may also cause severe respiratory disorders.
Chronic infection is produced by the slow replication of bradyzoites inside tissue cysts that have tropism for connective tissue—especially the superficial layers of skin, of the mucous membranes of the upper respiratory tract, and of the vestibulum vaginae—and in males, in the testes and epididymis. Tissue cysts in the scleral conjunctiva are pathognomonic. Other typical clinical signs of the chronic stage are cutaneous lesions such as thickening and folding of the skin in the neck and in the perineal region (also in the scrotal skin), loss of necrotic epidermis, and atrophy and induration of the testes of bulls. Male sterility is likely to be due to vascular damage in the pampiniform plexus and scrotal skin lesions.
Death may occur in both the acute and chronic stages of the disease. Although mortality is low, convalescence is slow in severe cases. Severely affected bulls can become sterile during acute and chronic infection. Affected animals remain carriers for life. In endemically infected herds, most animals remain subclinically infected, with a few animals developing the characteristic acute and chronic disease. Clinical cases are sporadic in animals younger than 1 year of age, and the prevalence of seropositive animals and animals with clinical signs increases with age. The disease in goats is similar to that in cattle. Infected donkeys have similar clinical signs, which are often more severe than those in horses.
Prevention and Treatment of Besnoitiosis in Animals
Biosecurity measures
Early and accurate diagnosis to prevent spread of disease in cows
Serologic diagnosis to detect subclinical infections
Selective culling of animals with clinical signs, including tissue cysts in the vestibulum vaginae and low body condition scores; culling of unproductive cattle; regular monitoring of clinical signs and sperm quality before breeding season
Seropositive animals kept and managed separately from the rest of the seronegative herd
Regular clinical and serologic diagnosis of the herds:
Two sequential samples by immunoblot
Replacements older than 6 months: regular annual monitoring by immunoblot or validated ELISA
Breeding bulls: annual regular monitoring before breeding season by immunoblot
Whole herd: at least annual regular clinical inspection in Besnoitia-free herds from regions where the disease is endemic
Use of repellents and ectoparasiticides indoors and outdoors
There are no effective treatments and no licensed vaccines for besnoitiosis, with the exception of a live vaccine used in Israel. Thus, biosecurity measures are key to controlling it. Risky practices (eg, sharing pastures or bulls) should be avoided, introduction of the disease by new infected entries should be prevented, and repellents and ectoparasiticides should be used both indoors and outdoors. In addition, early and accurate diagnosis is essential to prevent and avoid the spread of bovine besnoitiosis. The appearance of cysts in the scleral conjunctiva and vestibulum vaginae is a useful diagnostic indicator during clinical inspection, and clinical cases can be confirmed by skin biopsy and microscopic observation of tissue cysts. However, serologic diagnosis is essential to detect subclinical infections.
Selective culling of animals with clinical signs, as well as unproductive cattle, is recommended. However, culling of seropositive animals is recommended only in herds with low seroprevalence. In herds with high seroprevalence, noninfected animals should be separated from infected animals, with appropriate reproductive management: noninfected cows bred with noninfected breeding bulls, and infected cows artificially inseminated or bred with seropositive fertile breeding bulls. In addition, clinical and serologic diagnosis of the herd and monitoring of sperm quality before breeding season should be included in the regular herd health program.
Key Points
Besnoitiosis is characterized mainly by skin lesions during the chronic disease, and it impairs fertility.
Infected cattle frequently develop persistent fever and orchitis. Scleral conjunctival tissue cysts are pathognomonic of chronic besnoitiosis.
Serologic diagnosis, biosecurity, and an adequate reproductive and selective culling strategy are key in a control program.
For More Information
García-Bocanegra I, Zafra-Leva R. Enfermedades infecto-contagiosas en rumiantes. Elsevier SLU; 2019.
Gutiérrez-Expósito D, Ferre I, Ortega-Mora LM, et al. Advances in the diagnosis of bovine besnoitiosis: current options and applications for control. Int J Parasitol 2017;47(12):737-751. doi:10.1016/j.ijpara.2017.08.003
Alvarez-García G, García-Lunar P, Gutiérrez-Expósito D, et al. Dynamics of Besnoitia besnoiti infection in cattle. Parasitology 2014;141(11):1419-1435. doi: 10.1017/S0031182014000729
Alvarez-García G, Frey CF, Mora LM, et al. A century of bovine besnoitiosis: an unknown disease re-emerging in Europe. Trends Parasitol 2013;29(8):407-415. doi: 10.1016/j.pt.2013.06.002
Oryan A, Silver IA, Sadoughifar R. Caprine besnoitiosis: an emerging threat and its relationship to some other infections of ungulates by Besnoitia species. Res Vet Sci 2014;97(1):1-7. doi: 10.1016/j.rvsc.2014.06.004
Olias P, Schade B, Mehlhorn H. Molecular pathology, taxonomy and epidemiology of Besnoitia species (Protozoa: Sarcocystidae). Infect Genet Evol 2011;11(7):1564-1576. doi: 10.1016/j.meegid.2011.08.006
