Borrelia anserina infections

Pictures

Picture	Title	Caption	Copyright
Title Symptoms Caption A 'droopy chicken' due to spirochetosis. Note the ruffled feathers and cyanosis of the comb. Copyright ©Marcelo. B. Labruna	Symptoms	A 'droopy chicken' due to spirochetosis. Note the ruffled feathers and cyanosis of the comb.	©Marcelo. B. Labruna
Title Field signs Caption Aggregation of tick faeces (black detritus); around a crack in a pen infested by the Borrelia anserina vector, an Argas sp. tick Copyright ©Marcelo. B. Labruna	Field signs	Aggregation of tick faeces (black detritus); around a crack in a pen infested by the Borrelia anserina vector, an Argas sp. tick	©Marcelo. B. Labruna

Identity

Preferred Scientific Name

• Borrelia anserina infections

International Common Names

• English: avian borreliosis; avian spirochaetosis; avian spirochetosis; borreliosis, avian; fowl spirochetosis; spirochaetosis; spirochetosis; spirochetosis, borrelia anserina, in birds

Local Common Names

• Brazil: borreliose aviária

Pathogen/s

Overview

Avian (fowl) spirochetosis, or borreliosis, is an acute, septicaemic disease of a variety of avian species, including chickens, turkeys, geese, ducks and pheasants, caused by the bacterium Borrelia anserina (Barnes, 1997). It is of most significance in tropical and subtropical areas; extensively reared free-range flocks are more likely to be affected than confined flocks (Kanth, 2006). The disease was first described among geese in Russia (Sakharoff, 1891). A few decades later in Brazil, Marchoux and Salimbeni (1903) incriminated the role of ticks of the genus Argas as natural vectors of the disease; this was later confirmed by several authors in all continents (Prowazek, 1909; Knowles et al., 1932; Diab and Soliman, 1977).

B. anserina was classified under different taxonomic names at the beginning of the twentieth century (Knowles et al., 1932). These differences were mostly justified by the negative results obtained in cross-immunity tests performed on laboratory birds with different geographic strains. Nowadays, it is well known that different B. anserina antigenic types exist and active immunity is serotype-specific (DaMassa and Adler, 1979; Soni and Joshi, 1980; Sambri et al., 1999). 

Host Animals

Hosts/Species Affected

B. anserina is only pathogenic for birds. Birds are susceptible at all ages, but young birds tend develop more severe clinical signs with greater lethality rates. Joshi et al. (1985) showed dwarf chickens to be more resistant than White Leghorns and synthetic broilers. Native chicken breeds tend to be more resistant than are commercial ones (Rashid and Ali, 1991).

Systems Affected

Distribution

Avian spirochetosis occurs on all continents. B. anserina is primarily transmitted by ticks. Obviously, the prevalence of the disease should follow the tick vector distribution in the world. However, the vector distribution is much wider than that of spirochetosis. This difference is possibly a result of unrecorded cases of the disease in other countries, but also because some vector populations are not infected by B. anserina.

Distribution Table

The distribution in this summary table is based on all the information available. When several references are cited, they may give conflicting information on the status. Further details may be available for individual references in the Distribution Table Details section which can be selected by going to Generate Report.

Pathology

Post-mortem findings

The most characteristic post-mortem finding is the marked enlargement and mottling of the spleen, showing ecchymotic haemorrhages. The spleen becomes three to six times its normal size. The liver may also be enlarged, congested and friable containing minute areas of necrosis. The kidneys are enlarged and pale. Greenish mucoid enteritis is usually present.

Histopathology

The spleen shows hyperplasia of histiocytes and reticular cells, moderate depletion of lymphocytes and accentuation of the red pulp. Extensive erythrophagocytosis is evident in the sinusoidal macrophages of the spleen, in Kupffer cells of the liver and in bone marrow smears. Haemosiderosis is observed in the spleen, liver and intestines. Silver-stained spirochetes can be observed in the spleen, liver, small intestine, kidney or lungs (Bandopadhyay and Vegad, 1983; Cooper and Bickford, 1993).

Diagnosis

Clinical and Epidemiological Diagnosis

Increased mortality in flocks followed by clinical signs such fever, depression and greenish diarrhoea are suggestive of spirochetosis, but they are also observed in other acute avian diseases. These clinical signs, associated with splenomegaly at necropsy and the presence of Argas infestations, constitute epidemiological evidences of spirochetosis. A flock infested by Argas ticks can be identified by searching for attached larvae on the underneath side of wing webs.

Laboratory Diagnosis

Spirochetosis can be confirmed by the demonstration of spirochetes in Giemsa-stained blood or organ smears from ill birds. In the late disease phase, stained blood smears show the spirochetes aggregated in clumps due to agglutination antibodies. Highly motile spirochetes can be observed in a drop of fresh blood observed under dark-field microscope. B. anserina can also be demonstrated in the buffy coat in the microhematocrit tube (Higgins, 1986).

B. anserina can be isolated in 6-day-old embryonating chicken or turkey eggs by inoculating infective blood into the yolk sac. Spirochetes may be demonstrated 2-3 days later by examining the allantoic fluid. As it has been possible to cultivate B. anserina in BSK medium, this medium could also be used for isolation assays.

Spirochetes disappear from blood after the acute phase or following antibiotic therapy. Under this situation, several serologic tests have been developed to identify antibodies in convalescent birds, including serum plate agglutination test, slide agglutination and immobilization test, agar gel precipitin test, and indirect fluorescent antibody test (Barnes, 1997). Birds recovered from spirochetosis develop solid immunity for more than 6 months against homologous strains (McNeil et al., 1949; Verma and Rao, 1988).

List of Symptoms/Signs

Disease Course

Natural infection via either tick bites or ingestion of infective faeces, blood or ticks results in an incubation period of 3-12 days. Intravenous inoculation of infected blood into susceptible birds induces the disease after 24 to 48 hours (Knowles et al., 1932; Labruna et al., 1999). The most common clinical symptoms are fever, generalized weakness, ruffed feathers, loss of appetite, thirst, greenish diarrhoea, dropped head, and finally paralysis of wings and legs. Cyanosis or pallor of comb and wattles are visible. A few spirochetes may be found in the peripheral blood coincident with the initial temperature rise, thereafter increasing in concentration in 2 or 3 days, and then usually disappearing after a further 1 or 2 days. The disease course lasts for 3 to 7 days, followed by bird recovery or death. Recovered birds develop solid immunity and are not carriers of the bacterium. Under natural outbreaks, mortality rates vary from 1-2% up to almost 100%. The lowest rates occur in closed flocks where spirochetosis is endemic. The highest rates occur when susceptible flocks are placed in pens inhabited by infected ticks or when infected ticks are introduced in clean flocks by either infested birds or equipment.

Birds develop anaemia, the severity of which is maximum when spirochetemia is in decline. Studies have revealed the role of cold agglutinins and soluble immune complexes in the production of anaemia during acute spirochetosis. It is suspected that these adhere to erythrocytes, enhancing their phagocytosis by macrophages in tissues, especially in spleen (Soni et al., 1980; Joshi et al., 1982; Barnes, 1997).

Epidemiology

Besides being the primary vector, Argas spp. ticks are also reservoirs of the bacterium in nature. B. anserina can survive trans-stadially during all tick stages and is transmitted transovarially (Zaher et al., 1977). Once infected, a tick remains infected by B. anserina for its entire life (Hoogstraal, 1985).

Argas ticks have a multi-host life cycle pattern, consisting of eggs, larvae, two to four nymphal stages and the adults (males and females). Larvae feed for 4-6 days, whereas the nymphal instars and adult ticks feed for only 20 to 50 minutes, at night, when birds are housed. Egg deposition and incubation, mating and all tick moults occur off the host, inside cracks and crevices. Each female may lay as many as 900 eggs during her entire life. These are produced in as many as seven batches with a blood meal preceding each batch of eggs. Hungry ticks leave the cracks or crevices at dark hours, and move toward a sleeping chicken. Larvae attach mainly on the underneath side of the wing web. Nymphs and adults feed mainly on the shanks. Fed ticks detach from the hosts and immediately walk and hide in cracks or crevices. As engorged ticks walk toward hidden places they usually release black faeces which are characteristic. Highly infested flocks can be carefully identified by the presence of several small black spots <1 mm wide) on the roosts and walls, especially around crack entrances. Unfed Argas ticks are able to survive without a new blood meal for several months or years.

Spirochetosis outbreaks have been reported in Californian turkey and chicken flocks where no ticks, lice or mites could be found (McNeil et al., 1949). These intriguing findings have been subject to several speculations about the transmission by mosquitoes or through contaminated faeces from wandering birds. Once introduced in a clean flock, spirochetosis can be transmitted from bird to bird by virtually any means whereby blood, excreta, or tissues from an infected live or recently dead bird come in contact with a susceptible bird (Barnes, 1997).

Impact: Economic

Most of the literature about spirochetosis was published before the 1980s, especially from the 1940s to the 1960s, when the poultry industry comprised several small enterprises, many of which could be categorized by poor sanitation conditions. New scientific reports about field spirochetosis have rarely been released. This contrast is certainly a result of modifications of poultry-rearing methods around the world in the past few decades. The industry today, as it is in most countries, is very advanced in response to globalization, industrialization, vertical integration and aggregation such that a few large agribusiness companies virtually control the poultry industry in different countries. A number of diseases that used to cause problems before this revolution in production systems no longer do so, among them avian spirochetosis. These modifications have diminished the possibilities of tick establishment into new intensively managed flocks. In many countries where spirochetosis was reported to be one of the most severe diseases affecting the poultry industry in the past, the disease became confined to small flocks kept for personal consumption of product (village chickens) or very limited local sale, with no significant economic impact to the country. Sa’idu et al. (1995) noted the drastic decline of cases of spirochetosis in Nigeria in the 1980s, when compared to the 1970s, and associated it with better housing of birds and improved management and tick control measures.

Nowadays, free-range egg production is becoming a trend in response to concerns about the welfare of poultry kept in large farm complexes. It will be interesting to see the impact of such management on the establishment of Argas populations in these modified flock systems.

Disease Treatment

B. anserina is sensitive to penicillin, tylosin, streptomycin, dihydrostreptomycin, oxytetracycline and aureomycin. Generally, a single intramuscular dose of any of these drugs is sufficient for a severely affected bird to recover (Hsiang and Packchanian, 1951; Singer, 1977; Kheir El Din et al., 1986).

Prevention and Control

Avoiding or eliminating Argas ticks from the pens are the best measures to control spirochetosis. Tick eradication through the use of acaricides is very difficult due to the particular behaviour of ticks, which hide in the pen. Vaccination has been shown to control the disease. Several formalin- or phenol-inactivated vaccines were tested in different countries (Aragão, 1911; Nóbrega and Reis, 1941; Morcos et al., 1946; Gorrie, 1950; Rao et al., 1954). In general, all these vaccines showed high immunizing power which lasted for at least 6 months.

Today, fowl spirochetosis is practically confined to small flocks kept for subsistence or very limited local sale. In this context, the disease assumes endemic levels in which sick birds are seldom observed. Newborn chicks are resistant to the disease due to maternal antibodies and develop acquired immunity as they follow up. In these flocks the disease is practically confined to recently introduced susceptible birds. This particular context has aroused little or no interest from veterinary laboratories to trade spirochetosis vaccines. Regular acaricide applications on the pen and antibiotic therapy of sick birds should be adopted in these endemic spirochetosis flocks. Alternatively, attempts to 'tick-proof' roosts by suspending them from wire and keeping grease spread on the wire, or by placing roost legs in oil-filled containers, require almost constant attention to be effective (Barnes, 1997). Owners of clean flocks must be aware of the origin of new introduced birds to avoid importation of ticks or the disease.

References

Abdu PA, 1987. Infectious bursal disease and spirochetosis in pullet chicks. Avian Diseases, 31(1):204-205; 4 ref.

Aragão HB, 1911. Soroterapia e vacinação na espiroquetoze das galinhas. Memórias do Instituto Oswaldo Cruz, 3:3-39.

Ataliba AC; Resende JS; Yoshinari N; Labruna MB, 2007. Isolation and molecular characterization of a Brazilian strain of Borrelia anserina, the agent of fowl spirochaetosis. Research in Veterinary Science, 83(2):145-149. http://www.sciencedirect.co./science/journal/00345288

Bandopadhyay AC; Vegad JL, 1983. Observations on the pathology of experimental avian spirochaetosis. Research in Veterinary Science, 35:138-144.

Barnes HJ, 1997. Spirochetosis (Borreliosis). In: amek BW, Barnes HJ, Beard CW, McDougald LR, Saif YM, eds. Disease of Poultry. Ames, USA: Iowa State University Press, 318-324.

Boero JJ, 1957. Las garrapatas de la Republica Argentina (Acarina-Ixodoidea). Buenos Aires, Argentina:Universidad de Buenos Aires, 113pp.

Burroughs AL, 1947. Fowl spirochetosis transmitted by Argas persicus (Oken, 1818) from Texas. Science, 105:577.

Cooper GL; Bickford AA, 1993. Spirochetosis in California game chickens. Avian Diseases, 37(4):1167-1171; 16 ref.

DaMassa AJ; Adler HE, 1979. Avian spirochetosis:natural transmission by Argas (Persicargas) sanchezi (Ixodoidea:Argasidae) and existence of different serologic and immunologic types of Borrelia anserina in the United States. American Journal of Veterinary Research, 40(1):154-157.

Dhawedkar RG; Dhanesar NS, 1983. Preservation of Borrelia anserina by liquid nitrogen refrigeration. Indian. Journal of Animal Sciences, 53(10):1124-1127.

Diab FM; Soliman ZR, 1977. An experimental study of Borrelia anserina in four species of Argas ticks. 1. Spirochete localization and densities. Zeitschrift fur Parasitenkunde, 53:201-212.

Fabbi M; Sambri V; Marangoni A; Magnino S; Basano FS; Cevenini R; Genchi C, 1995. Borrelia in pigeons: no serological evidence of Borrelia burgdorferi infection. Journal of Veterinary Medicine. Series B, 42(8):503-507; 20 ref.

Francis DW, 1956. A case of spirochetosis in New Mexico. Poultry Science, 35:1142-1143.

Ginawi MA; Shommein AM, 1980. Preservation of Borrelia anserina at different temperatures. Bulletin of Animal Health and Production in Africa, 28:221-223.

Gorrie CJR, 1950. Vaccination against spirochetosis in fowls. Australian Veterinary Journal, 26:308-315.

Gothe R; Buchheim C; Schrecke W, 1981. Argas (Persicargas) persicus und Argas (Argas) africolumbae als natürliche biologische Überträger von Borrelia anserina und Aegyptianella pullorum in Obervolta. Berliner und Munchener Tierarztliche Wochenschrift, 94:280-285.

Gothe R; Schrecke W, 1972. Zur epizootiologischen Bedeutung von Persicargas - Zecken der Hühner in Transvaal. Berliner und Munchener Tierarztliche Wochenschrift, 85(1):9-11.

Hart L, 1963. Spirochetosis in fowls:studies on immunity. Australian Veterinary Journal, 39:187-191.

Henry JN, 1950. Vaccination against spirochetosis in fowls. Australian Veterinary Journal, 26:301-307.

Higgins AR, 1986. Demonstrating Borrelia anserina: "a can of worms". Veterinary Record, 119(5):120; 1 ref.

Hoffman HA; Jackson TW, 1956. Spirochetosis in turkeys. Journal of the American Veterinary Medical Association, 109:481-486.

Hoogstraal H, 1985. Argasid and Nuttalliellid ticks as parasites and vectors. Advances in Parasitology, 24:135-238.

Hovind-Hougen K, 1995. A morphological characterization of Borrelia anserina. Microbiology (Reading), 141(1):79-83; 21 ref.

Hsiang CM; Packchanian A, 1951. A comparison of eleven antibiotics in the treatment of Borrelia anserina infection (spirochetosis) in young chicks. Texas Reports on Biology and Medicine, 9:34-45.

Joshi AG; Soni JL; Khan AG, 1982. Note on erythrophagocytosis in acute avian spirochaetosis. Indian Journal of Animal Sciences, 52(6):477-481.

Joshi AG; Soni JL; Khan AG, 1985. Resistance of dwarf chickens to Borrelia anserina infection as compared to that of White Leghorn and broilers. Indian Journal of Animal Sciences, 55(8):654-655; 2 ref.

Kanth MAH, 2006. Spirochaetosis - a devastating tick borne poultry disease in the trans Himalayas. Vet Scan, 1(2):16-18. http://www.kashvet.org/vetscan.htm

Kelly RT, 1984. Borrelia Swellengrebel, 1907. In:Krieg NR, Holt JG, eds. Bergey's Manual of Systematic Bacteriology v.1. Baltimore, USA:Willians & Wilkins, 57-62.

Kheir El Din AW; Hassan NR; Hatem ME, 1986. Clinical and pathological investigations on avian spirochaetosis following experimental infection and treatment. Veterinary Medical Journal, 34(3):327-335.

Knowles R; Gupta BM; Basu BC, 1932. Studies in avian spirochetosis. Indian Medical Research Memoirs, 22:1-122.

Labruna MB; Resende JS; Martins NRS; Jorge MA, 1999. Cryopreservation of an avian spirochete strain in liquid nitrogen. Arquivo Brasileiro de Medicina Veterinária e Zootecnia, 51(6):551-553; 7 ref.

Levine JF; Dykstra MJ; Nicholson WL; Walker RL; Massey G, 1990. Attenuation of Borrelia anserina by serial passage in liquid medium. Research in Veterinary Science, 48(1):64-69; 20 ref.

Loomis EC, 1953. Avian spirochetosis in California turkeys. American Journal of Veterinary Research, 14:612-615.

Marchoux E; Salimbeni A, 1903. La spirillose des poules. Annales de l'Institute Pasteur, 17(9):569-580.

McNeil E; Hinshaw WR; Kissling RE, 1949. A study of Borrelia anserina infections (spirochaetosis) in turkeys. Journal of Bacteriology, 57:191-206.

Morcos Z; Zaki AO; Zaki R, 1946. A concise investigation of fowl spirochetosis in Egypt. Journal of the American Veterinary Medical Association, 109:102-116.

Nóbrega P; Reis AS, 1947. O diagnóstico da espiroquetose aviária em animais mortos. Arquivos do Instituto Biológico (São Paulo), 18:91-96.

Nóbrega P; Reis J, 1941. Produção de vacina contra espiroquetose aviária em ovos embrionados. Arquivos do Instituto Biológico (São Paulo), 12:87-92.

OIE Handistatus, 2002. World Animal Health Publication and Handistatus II (dataset for 2001). Paris, France: Office International des Epizooties.

OIE Handistatus, 2003. World Animal Health Publication and Handistatus II (dataset for 2002). Paris, France: Office International des Epizooties.

OIE Handistatus, 2004. World Animal Health Publication and Handistatus II (data set for 2003). Paris, France: Office International des Epizooties.

OIE Handistatus, 2005. World Animal Health Publication and Handistatus II (data set for 2004). Paris, France: Office International des Epizooties.

Popova T, 2008. Spirochaetosis in aviary breaded partridges (Perdix perdix). In: Sbornik dokladi ot nauchnata konferentsiya: Traditsii i s'vremenhost v'v veterinarnata meditsina. Sofia, Bulgaria: Lesotekhnicheski Universitet, 197-202.

Prowazek SV, 1909. Contribuição para o estudo do desenvolvimento do Spirochaeta gallinarum. Memórias do Instituto Oswaldo Cruz, 1(2):79-80.

Rao SBV; Thakral BM; Dhanda MR, 1954. Studies on fowl spirochetosis with special reference to penicillin therapy and the development of an egg-adapted vaccine for its control. Indian Veterinary Journal, 31(1):1-14.

Rashid J; Ali A, 1991. Comparative study of pathogenicity of experimentally produced Borrelia anserina infection in commercial broiler and Desi chicks. Pakistan Journal of Zoology, 23(4):361-362.

Rockey NW; Snell VN, 1958. Avian spirochetosis (Borrelia anserina) epizootics in Arizona poultry. Journal of the American Veterinary Medical Association, 138:648-652.

Sa'idu L; Agbede RIS; Abdu AP, 1995. Prevalence of avian spirochaetosis in Zaria (1980-1989). Israel Journal of Veterinary Medicine, 50(1):39-40; 12 ref.

Sakharoff MN, 1891. Spirochaeta anserina et la septicemie des oies. Annales de l'Institute Pasteur, 5:564-566.

Sambri V; Marangoni A; Olmo A; Storni E; Montagnani M; Fabbi M; Cevenini R, 1999. Specific antibodies reactive with the 22-kilodalton major outer surface protein of Borrelia anserina Ni-NL protect chicks from infection. Infection and Immunity, 67(5):2633-2637; 29 ref.

Singer N, 1977. An outbreak of spirochaetosis in a flock of white pekin ducks. Refuah Veterinarith, 34(3):104-106.

Soni JL; Adaval SC; Kolte GN, 1980. Preliminary observations on anaemia, splenomegaly and cold agglutinin production during acute avian spirochaetosis. Indian Journal of Animal Sciences, 50(12):1110-1113.

Soni JL; Joshi AG, 1980. A note on strain variation in Akola and Jabalpur strains of Borrelia anserina. Zentralbl Veterinaermed Reibe B, 27:70-72.

Verma RK; Rao KNP, 1988. Some observations on the response of Borrelia anserina in chemically and surgically bursectomized chicks. Indian Veterinary Journal, 65(10):864-867; 7 ref.

Zaher MA; Soliman ZR; Diab FM, 1977. An experimental study of Borrelia anserina in four species of Argas ticks. 1. Transsstadial survival and transovarial transmission. Zeitschrift fur Parasitenkunde, 53:213-223.

Distribution References

Abdu P A, 1987. Infectious bursal disease and spirochetosis in pullet chicks. Avian Diseases. 31 (1), 204-205. DOI:10.2307/1590797

Ataliba A C, Resende J S, Yoshinari N, Labruna M B, 2007. Isolation and molecular characterization of a Brazilian strain of Borrelia anserina, the agent of fowl spirochaetosis. Research in Veterinary Science. 83 (2), 145-149. http://www.sciencedirect.co./science/journal/00345288 DOI:10.1016/j.rvsc.2006.11.014

Burroughs AL, 1947. Fowl spirochetosis transmitted by Argas persicus (Oken, 1818) from Texas. In: Science, 105 577.

CABI, Undated. CABI Compendium: Status as determined by CABI editor. Wallingford, UK: CABI

Cooper G L, Bickford A A, 1993. Spirochetosis in California game chickens. Avian Diseases. 37 (4), 1167-1171. DOI:10.2307/1591932

Francis DW, 1956. A case of spirochetosis in New Mexico. In: Poultry Science, 35 1142-1143.

Ginawi M A, Shommein A M, 1980. Preservation of Borrelia anserina at different temperatures. Bulletin of Animal Health and Production in Africa. 28 (3), 221-223.

GORRIE C J R, 1950. Vaccination against spirochaetosis in fowls. Australian Veterinary Journal. 308-315. DOI:10.1111/j.1751-0813.1950.tb04839.x

Gothe R, Schrecke W, 1972. On the epizootiological significance of Persicargas ticks of hens in the Transvaal. (Zur epizootiologischen Bedeutung von Persicargas-Zecken der Huhner in Transvaal.). Berliner und Münchener Tierärztliche Wochenschrift. 85 (1), 9-11.

Hart L, 1963. Spirochetosis in fowls:studies on immunity. In: Australian Veterinary Journal, 39 187-191.

HENRY J N, 1950. Vaccination against spirochaetosis in fowls. Australian Veterinary Journal. 301-307. DOI:10.1111/j.1751-0813.1950.tb04838.x

Higgins A R, 1986. Demonstrating Borrelia anserina: "a can of worms". Veterinary Record, 119 (5), 120.

Hoffman HA, Jackson TW, 1956. Spirochetosis in turkeys. In: Journal of the American Veterinary Medical Association, 109 481-486.

Joshi A G, Soni J L, Khan A G, 1985. Resistance of Dwarf chickens to Borrelia anserina infection as compared to that of White Leghorn and broilers. Indian Journal of Animal Sciences. 55 (8), 654-655.

Knowles R, Gupta BM, Basu BC, 1932. Studies in avian spirochetosis. In: Indian Medical Research Memoirs, 22 1-122.

Labruna M B, Resende J S, Martins N R S, Jorge M A, 1999. Cryopreservation of an avian spirochete strain in liquid nitrogen. Arquivo Brasileiro de Medicina Veterinária e Zootecnia. 51 (6), 551-553. DOI:10.1590/S0102-09351999000600008

LOOMIS E C, 1953. Avian spirochetosis in California turkeys. American Journal of Veterinary Research. 612-615.

Marchoux E, Salimbeni A, 1903. (La spirillose des poules). In: Annales de l'Institute Pasteur, 17 (9) 569-580.

MCNEIL E, HINSHAW W R, KISSLING R E, 1949. A study of Borrelia anserina infection (spirochetosis) in turkeys. Journal of Bacteriology. 191-206.

Nóbrega P, Reis AS, 1947. (O diagnóstico da espiroquetose aviária em animais mortos). In: Arquivos do Instituto Biológico (São Paulo), 18 91-96.

OIE Handistatus, 2005. World Animal Health Publication and Handistatus II (dataset for 2004)., Paris, France: Office International des Epizooties.

Popova T, 2008. Spirochaetosis in aviary breaded partridges (Perdix perdix). In: Sbornik dokladi ot nauchnata konferentsiya: Traditsii i s'vremenhost v'v veterinarnata meditsina. Sofia, Bulgaria: Lesotekhnicheski Universitet. 197-202.

Prowazek SV, 1909. (Contribuição para o estudo do desenvolvimento do Spirochaeta gallinarum). In: Memórias do Instituto Oswaldo Cruz, 1 (2) 79-80.

RAO S B V, THAKRAL B M, DHANDA M R, 1954. Studies on fowl spirochaetosis with special reference to penicillin therapy and the development of an egg-adapted vaccine for its control. Indian Veterinary Journal. 1-14.

Rashid J, Ali A, 1991. Comparative study of pathogenicity of experimentally produced Borrelia anserina infection in commercial broiler and Desi chicks. Pakistan Journal of Zoology. 23 (4), 361-362.

Rockey NW, Snell VN, 1958. Avian spirochetosis (Borrelia anserina) epizootics in Arizona poultry. In: Journal of the American Veterinary Medical Association, 138 648-652.

Sa'idu L, Agbede R I S, Abdu A P, 1995. Prevalence of avian spirochaetosis in Zaria (1980-1989). Israel Journal of Veterinary Medicine. 50 (1), 39-40.

Sakharoff MN, 1891. (Spirochaeta anserina et la septicemie des oies). In: Annales de l'Institute Pasteur, 5 564-566.

Singer N, 1977. An outbreak of spirochaetosis in a flock of White Pekin ducks. Refuah Veterinarith. 34 (3), 104-106.

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Distribution Maps