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Larval Tapeworm Infections in Primates: Coenurosis, Cysticercosis, and Echinococcosis

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Neglected Diseases in Monkeys

Abstract

As globally distributed parasites of humans, livestock, and wildlife, taeniid parasites exploit predator–prey relationships across mammalian systems. Infections with the larval taeniid stage cause symptoms ranging from the neurological (e.g., paralysis, seizures) to the ocular (e.g., blindness) and muscular (e.g., atrophy), result in massive economic losses in livestock, and threaten wildlife populations. While taeniids were once considered to be relatively host-specific in their larval stage, reports of taeniid emergence in nontraditional hosts are increasing in frequency. In this chapter, I take a One-Health approach to examining cases of larval taeniid infections in primates, focusing on the infection of wild geladas (Theropithecus gelada) with the larval stage of Taenia serialis. By understanding how taeniid species emerge in nontraditional hosts, we can build useful frameworks for predicting and disrupting transmission and thereby protecting captive and wild NHP, domestic animals, and humans in a world with a broadening human–wildlife interface.

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References

  • Abuladze KI (1964) Taeniata of animals and man and diseases caused by them. In: Skrjabin KI (ed) Essentials of cestodology, vol 4. Akademiia Nauk SSSR, Gel’mintologicheskaia Laboratoriia, Izdatel’stvo Nauka, Moskva, (English translation, Israel Program for Scientific Translations, Jerusalem, 1970)

    Google Scholar 

  • Ambrosio JR, Valverde-Islas L, Nava-Castro KE, Palacios-Arreola MI, Ostoa-Saloma P, Reynoso-Ducoing O et al (2015) Androgens exert a cysticidal effect upon Taenia crassiceps by disrupting flame cell morphology and function. PLoS One 10(6):e0127928

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Arteaga-Silva M, Vargas-Villavicencio JA, Vigueras-Villaseñor RM, Rodríguez-Dorantes M, Morales-Montor J (2009) Taenia crassiceps infection disrupts estrous cycle and reproductive behavior in BALB/c female mice. Acta Trop 109(2):141–145

    Article  PubMed  Google Scholar 

  • Avcioglu H, Yildirim A, Duzlu O, Inci A, Terim KK, Balkaya I (2011) Prevalence and molecular characterization of bovine coenurosis from Eastern Anatolian region of Turkey. Vet Parasitol 176(1):59–64

    Article  CAS  PubMed  Google Scholar 

  • Bacciarini LN, Gottstein B, Pagan O, Rehmann P, Gröne A (2004) Hepatic alveolar echinococcosis in cynomolgus monkeys (Macaca fascicularis). Vet Pathol 41(3):229–234

    Google Scholar 

  • Bertolino P (1957) Studio clinico ed anatomo-patologico su due casi di cenurosi in Theropithecus gelada. Profilassi 30:3–10

    Google Scholar 

  • Borji H, Emami MR, Maleki MOHSEN, Razmi GH, Mehrjerdi HK, Moghaddas E (2012) Alveolar echinococcosis infection in a monkey (Ateles geoffroyi) in Mashhad, Iran. Iran J Public Health 41(2):111

    Google Scholar 

  • Boufana B, Stidworthy MF, Bell S, Chantrey J, Masters N, Unwin S et al (2012) Echinococcus and Taenia spp. from captive mammals in the United Kingdom. Vet Parasitol 190(1–2):95–103

    Google Scholar 

  • Bowman DD (2009) Georgis’ parasitology for veterinarians. Elsevier Health Sciences, St. Louis, MO

    Google Scholar 

  • Brack M, Conraths FJ, Rensing S (1997) Alveolar hydatidosis (Echinococcus multilocularis) in a captive rhesus monkey (Macaca mulatta) in Germany. Tropical Med Int Health 2(8):754–759

    Google Scholar 

  • Brooks DR, Glen DR (1982) Pinworms and primates: a case study in coevolution. Proc Helminthol Soc Wash 49(1):76–S5

    Google Scholar 

  • Brunet J, Pesson B, Chermette R, Regnard P, Grimm F, Deplazes P et al (2014) First case of peritoneal cysticercosis in a non-human primate host (Macaca tonkeana) due to Taenia martis. Parasit Vectors 7(1):422

    Google Scholar 

  • Brunet J, Regnard P, Pesson B, Abou-Bacar A, Sabou M, Pfaff AW, Candolfi E (2015) Description of vertebral and liver alveolar echinococcosis cases in Cynomolgus monkeys (Macaca fascicularis). BMC Vet Res 11(1):198

    Google Scholar 

  • Clark JD (1969) Coenurosis in a gelada baboon (Theropithecus gelada). J Am Vet Med Assoc 155(7):1258–1263

    CAS  PubMed  Google Scholar 

  • Combes C (1991) Ethological aspects of parasite transmission. Am Nat 138(4):866–880

    Article  Google Scholar 

  • Combes C (2001) Parasitism: the ecology and evolution of intimate interactions. University of Chicago Press, Chicago

    Google Scholar 

  • Conn DB, Swiderski Z (2008) A standardised terminology of the embryonic envelopes and associated developmental stages of tapeworms (Platyhelminthes: Cestoda). Folia Parasitol 55(1):42

    Article  Google Scholar 

  • Cowlishaw G (1994) Vulnerability to predation in baboon populations. Behaviour 131(3):293–304

    Article  Google Scholar 

  • Craig PS, Macpherson CNL (2000) Dogs and cestode zoonoses. In: Macpherson CN, Mesli FX, Wandeler AI (eds) Dogs, zoonoses and public health. CAB International, Oxon, pp 149–211

    Google Scholar 

  • Craig P, Pawłowski Z (eds) (2002) Cestode zoonoses: echinococcosis and cysticercosis: an emergent and global problem, vol 341. IOS Press, Amsterdam

    Google Scholar 

  • De Liberato C, Berrilli F, Meoli R, Friedrich KG, Di Cerbo P, Cocumelli C, Eleni C (2014) Fatal infection with Taenia martis metacestodes in a ring-tailed lemur (Lemur catta) living in an Italian zoological garden. Parasitol Int 63(5):695–697

    Google Scholar 

  • Denk D, Boufana B, Masters NJ, Stidworthy MF (2016) Fatal echinococcosis in three lemurs in the United Kingdom—a case series. Vet Parasitol 218:10–14

    Article  PubMed  Google Scholar 

  • Deplazes P, Eckert J (2001) Veterinary aspects of alveolar echinococcosis—a zoonosis of public health significance. Vet Parasitol 98(1–3):65–87

    Article  CAS  PubMed  Google Scholar 

  • Deplazes P, Rinaldi L, Rojas CA, Torgerson PR, Harandi MF, Romig T, Antolova D, Schurer JM, Lahmar S, Cringoli G, Magambo J (2017) Global distribution of alveolar and cystic echinococcosis. In: Advances in parasitology, vol 95. Academic Press, Cambridge, MA, pp 315–493

    Google Scholar 

  • Dunbar RIM (1980) Demographic and life history variables of a population of gelada baboons (Theropithecus gelada). J Anim Ecol 49(2):485–506

    Article  Google Scholar 

  • Dunbar RIM, Dunbar EP (1977) Dominance and reproductive success among female gelada baboons. Nature 266(5600):351

    Article  CAS  PubMed  Google Scholar 

  • Eckert J, Thompson RCA (2017) Historical aspects of echinococcosis. In: Thompson RCA, Deplazes P, Lymbery AJ (eds) Advances in parasitology: Echinococcus and Echinococcosis, part A, vol 95, pp 1–64

    Google Scholar 

  • Elek SR, Finkelstein LE (1939) Multiceps serialis infestation in a baboon. Report of a case exhibiting connective tissue cystic masses. Zoologica 24:323–328

    Google Scholar 

  • Esch GW (1967) Some effects of cortisone and sex on the biology of coenuriasis in laboratory mice and jackrabbits. Parasitology 57(1):175–179

    Article  CAS  Google Scholar 

  • Escobedo G, Larralde C, Chavarria A, Cerbón MA, Morales-Montor J (2004) Molecular mechanisms involved in the differential effects of sex steroids on the reproduction and infectivity of Taenia crassiceps. J Parasitol 90(6):1235–1244

    Article  CAS  PubMed  Google Scholar 

  • Escobedo G, De León-Nava MA, Morales-Montor J (2010) Sex differences in parasitic infections: beyond the dogma of female-biased resistance. In: Klein SL, Roberts CW (eds) Sex hormones and immunity to infection. Springer, Berlin, pp 187–204

    Chapter  Google Scholar 

  • Ewald PW (1995) The evolution of virulence: a unifying link between parasitology and ecology. J Parasitol 81(5):659

    Article  CAS  PubMed  Google Scholar 

  • Fain A (1956) Coenurus of Taenia brauni in Man and Animals in the Belgian Congo and Ruanda-Urundi. I. Coenurus in Wild Animals, with Cerebral Localization. Annales de la Société Belge de Médecine Tropicale 36(5):673–677. Société Belge de Médecine Tropicale

    Google Scholar 

  • Flisser A (1991) Taeniasis-cysticercosis: an introduction. Southeast Asian J Trop Med Public Health 22:233–235

    PubMed  Google Scholar 

  • Garcia HH, Nash TE, Del Brutto OH (2014) Clinical symptoms, diagnosis, and treatment of neurocysticercosis. Lancet Neurol 13(12):1202–1215

    Article  PubMed  PubMed Central  Google Scholar 

  • Gemmell MA, Lawson JR, Roberts MG (1987) Population dynamics in echinococcosis and cysticercosis: evaluation of the biological parameters of Taenia hydatigena and T. ovis and comparison with those of Echinococcus granulosus. Parasitology 94(01):161–180

    Article  PubMed  Google Scholar 

  • Gourbal BEF, Gabrion C (2004) A study of mate choice in mice with experimental cysticercosis: can males choose? Can J Zool 82(4):635–643

    Article  Google Scholar 

  • Gourbal BEF, Lacroix A, Gabrion C (2002) Behavioural dominance and Taenia crassiceps parasitism in BALB/c male mice. Parasitol Res 88(10):912–917

    Article  CAS  PubMed  Google Scholar 

  • Gregory GG (1976) Fecundity and proglottid release of Taenia ovis and T. hydatigena. Aust Vet J 52(6):277–279

    Article  CAS  PubMed  Google Scholar 

  • Guerra-Silveira F, Abad-Franch F (2013) Sex bias in infectious disease epidemiology: patterns and processes. PLoS One 8(4):e62390

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Heath DD (1971) The migration of oncospheres of Taenia pisiformis, T. serialis and Echinococcus granulosus within the intermediate host. Int J Parasitol 1(2):145–150

    Article  CAS  PubMed  Google Scholar 

  • Hobbes TR, Colgin L, Maginnis GM, Lewis AD (2003) Abdominal cysticercosis in a rhesus macaque (Macaca mulatta). Comp Med 53(5):545–547

    Google Scholar 

  • Hoberg EP (2002) Taenia tapeworms: their biology, evolution and socioeconomic significance. Microbes Infect 4(8):859–866

    Article  PubMed  Google Scholar 

  • Hoberg EP, Jones A, Rausch RL, Eom KS, Gardner SL (2000) A phylogenetic hypothesis for species of the genus Taenia (Eucestoda: Taeniidae). J Parasitol 86(1):89–98

    Article  CAS  PubMed  Google Scholar 

  • Hoberg EP, Alkire NL, Queiroz AD, Jones A (2001) Out of Africa: origins of the Taenia tapeworms in humans. Proc R Soc Lond B Biol Sci 268(1469):781–787

    Article  CAS  Google Scholar 

  • Howard EB, Gendron AP (1980) Echinococcus vogeli infection in higher primates at the Los Angeles zoo. Proceedings of the Symposia of the National Zoological Park, Smithsonian Institution, pp 379–382

    Google Scholar 

  • Hugot JP (1999) Primates and their pinworm parasites: the Cameron hypothesis revisited. Syst Biol 48(3):523–546

    Article  CAS  PubMed  Google Scholar 

  • Ibarra-Coronado EG, Escobedo G, Nava-Castro K, Ramses CRJ, Hernández-Bello R, García-Varela M et al (2011) A helminth cestode parasite express an estrogen-binding protein resembling a classic nuclear estrogen receptor. Steroids 76(10):1149–1159

    Article  CAS  PubMed  Google Scholar 

  • Ing MB, Schantz PM, Turner JA (1998) Human coenurosis in North America: case reports and review. Clin Infect Dis 27(3):519–523

    Article  CAS  PubMed  Google Scholar 

  • Iwamoto T, Mori A, Kawai M, Bekele A (1996) Anti-predator behavior of gelada baboons. Primates 37(4):389–397

    Article  Google Scholar 

  • Jabbar A, Swiderski Z, Mlocicki D, Beveridge I, Lightowlers MW (2010) The ultrastructure of taeniid cestode oncospheres and localization of host-protective antigens. Parasitology 137(03):521–535

    Article  CAS  PubMed  Google Scholar 

  • Jeon HK, Chai JY, Kong Y, Waikagul J, Insisiengmay B, Rim HJ, Eom KS (2009) Differential diagnosis of Taenia asiatica using multiplex PCR. Exp Parasitol 121(2):151–156

    Article  CAS  PubMed  Google Scholar 

  • Jia WZ, Yan HB, Guo AJ, Zhu XQ, Wang YC, Shi WG et al (2010) Complete mitochondrial genomes of Taenia multiceps, T. hydatigena and T. pisiformis: additional molecular markers for a tapeworm genus of human and animal health significance. BMC Genomics 11(1):447

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kondo H, Wada Y, Bando G, Kosude M, Yagi K, Oku Y (1996) Alveolar hydatidosis in a gorilla and a ring-tailed lemur in Japan. J Vet Med Sci 58(5):447–449

    Article  CAS  PubMed  Google Scholar 

  • Kuntz RE, Myers BJ (1967) Primate cysticercosis: Taenia hydatigena in Kenya vervets (Cercopithecus aethiops Linnaeus, 1758) and Taiwan macaques (Macaca cyclopis Swinhoe, 1864). Primates 8(1):83–88

    Google Scholar 

  • Lafferty KD (1999) The evolution of trophic transmission. Parasitol Today 15(3):111–115

    Article  CAS  PubMed  Google Scholar 

  • Lafferty KD, Thomas F, Poulin R (2000) Evolution of host phenotype manipulation by parasites and its consequences. In: Poulin R, Morand S, Skorping A (eds) Evolutionary biology of host–parasite relationships: theory meets reality. Elsevier, Amsterdam

    Google Scholar 

  • Larralde C, Morales J, Terrazas I, Govezensky T, Romano MC (1995) Sex hormone changes induced by the parasite lead to feminization of the male host in murine Taenia crassiceps cysticercosis. J Steroid Biochem Mol Biol 52(6):575–580

    Article  CAS  PubMed  Google Scholar 

  • Lawson JR, Gemmell MA (1990) Transmission of taeniid tapeworm eggs via blowflies to intermediate hosts. Parasitology 100(01):143–146

    Article  PubMed  Google Scholar 

  • Lefèvre T, Lebarbenchon C, Gauthier-Clerc M, Missé D, Poulin R, Thomas F (2009) The ecological significance of manipulative parasites. Trends Ecol Evol 24(1):41–48

    Article  PubMed  Google Scholar 

  • Leiby PD, Dyer WG (1971) Cyclophyllidean tapeworms of wild carnivora. In: Davis JW, Anderson RC (eds) Parasitic diseases of wild animals. Iowa State University Press, Iowa City, pp 174–234

    Google Scholar 

  • Lescano AG, Zunt J (2013) Other cestodes: sparganosis, coenurosis and Taenia crassiceps cysticercosis. In: Handbook of clinical neurology, vol 114. Elsevier, Amsterdam, pp 335–345

    Google Scholar 

  • Lin YC, Rikihisa Y, Kono H, Gu Y (1990) Effects of larval tapeworm (Taenia taeniaeformis) infection on reproductive functions in male and female host rats. Exp Parasitol 70(3):344–352

    Article  CAS  PubMed  Google Scholar 

  • Loos-Frank B (2000) An up-date of Verster’s (1969) ‘Taxonomic revision of the genus Taenia Linnaeus’ (Cestoda) in table format. Syst Parasitol 45(3):155–184

    Article  CAS  PubMed  Google Scholar 

  • Luzón M, De La Fuente-López C, Martínez-Nevado E, Fernández-Morán J, Ponce-Gordo F (2010) Taenia crassiceps cysticercosis in a ring-tailed lemur (Lemur catta). J Zoo Wildl Med 41(2):327–330

    Article  PubMed  Google Scholar 

  • Lymbery AJ (2017) Phylogenetic pattern, evolutionary processes and species delimitation in the genus Echinococcus. In: Thompson RCA, Deplazes P, Lymbery AJ (eds) Advances in parasitology: echinococcus and echinococcosis, part A, vol 95. Academic Press, London, pp 111–145

    Google Scholar 

  • Marty AM, Neafie RC (2000) Helminthiases. In: Meyers WM, Neafie RC, Marty AM, Wears DJ (eds) Pathology of infectious diseases, vol 1. Armed Forces Institute of Pathology, Washington, DC, pp 185–196

    Google Scholar 

  • McManus DP (2006) Molecular discrimination of taeniid cestodes. Parasitol Int 55:S31–S37

    Article  CAS  PubMed  Google Scholar 

  • McManus DP, Zhang W, Li J, Bartley PB (2003) Echinococcosis. Lancet 362(9392):1295–1304

    Article  PubMed  Google Scholar 

  • Moore J (2002) Parasites and the behavior of animals. Oxford University Press, Oxford

    Google Scholar 

  • Morales J, Larralde C, Arteaga M, Govezensky T, Romano MC, Morali G (1996) Inhibition of sexual behavior in male mice infected with Taenia crassiceps cysticerci. J Parasitol 82(5):689–693

    Article  CAS  PubMed  Google Scholar 

  • Morales-Montor J, Larralde C (2005) The role of sex steroids in the complex physiology of the host-parasite relationship: the case of the larval cestode of Taenia crassiceps. Parasitology 131(3):287–294

    Article  CAS  PubMed  Google Scholar 

  • Morales-Montor J, Rodríguez-Dorantes M, Mendoza-Rodríguez CA, Camacho-Arroyo I, Cerbón MA (1998) Differential expression of the estrogen-regulated proto-oncogenes c-fos, c-jun, and bcl-2 and of the tumor-suppressor p53 gene in the male mouse chronically infected with Taenia crassiceps cysticerci. Parasitol Res 84(8):616–622

    Article  CAS  PubMed  Google Scholar 

  • Morales-Montor J, Gamboa-Dominguez A, Rodriguez-Dorantes M, Cerbon MA (1999a) Tissue damage in the male murine reproductive system during experimental Taenia crassiceps cysticercosis. J Parasitol 85(5):887–890

    Article  CAS  PubMed  Google Scholar 

  • Morales-Montor J, Rodríguez-Dorantes M, Cerbon MA (1999b) Modified expression of steroid 5α-reductase as well as aromatase, but not cholesterol side-chain cleavage enzyme, in the reproductive system of male mice during (Taenia crassiceps) cysticercosis. Parasitol Res 85(5):393–398

    Article  CAS  PubMed  Google Scholar 

  • Morales-Montor J, Baig S, Mitchell R, Deway K, Hallal-Calleros C, Damian RT (2001) Immunoendocrine interactions during chronic cysticercosis determine male mouse feminization: role of IL-6. J Immunol 167(8):4527–4533

    Article  CAS  PubMed  Google Scholar 

  • Morales-Montor J, Hallal-Calleros C, Romano MC, Damian RT (2002a) Inhibition of P-450 aromatase prevents feminisation and induces protection during cysticercosis. Int J Parasitol 32(11):1379–1387

    Article  CAS  PubMed  Google Scholar 

  • Morales-Montor J, Baig S, Kabbani A, Damian RT (2002b) Do interleukin-6 and macrophage-migration inhibitory factor play a role during sex-associated susceptibility in murine cysticercosis? Parasitol Res 88(10):901–904

    Article  PubMed  Google Scholar 

  • Morales-Montor J, Chavarria A, De Leon MA, Del Castillo LI, Escobedo EG, Sanchez EN et al (2004) Host gender in parasitic infections of mammals: an evaluation of the female host supremacy paradigm. J Parasitol 90(3):531–546

    Article  CAS  PubMed  Google Scholar 

  • Nakao M, Lavikainen A, Yanagida T, Ito A (2013) Phylogenetic systematics of the genus Echinococcus (Cestoda: Taeniidae). Int J Parasitol 43(12–13):1017–1029

    Google Scholar 

  • Nguyen N, Fashing PJ, Boyd DA, Barry TS, Burke RJ, Goodale CB, Jones SC, Kerby JT, Kellogg BS, Lee LM, Miller CM (2015) Fitness impacts of tapeworm parasitism on wild gelada monkeys at Guassa, Ethiopia. Am J Primatol 77(5):579–594

    Google Scholar 

  • O’Grady JP (1982) Ultrasonic evaluation of echinococcosis in four lowland gorillas. J Am Vet Med Assoc 181(11):1348

    PubMed  Google Scholar 

  • Ohsawa H (1979) The local gelada population and environment of the Gish area. In: Kawai M (ed) Ecological and sociological studies of gelada baboons. Karger Publishers, Tokyo, pp 4–45

    Google Scholar 

  • Padgett KA, Nadler SA, Munson L, Sacks B, Boyce WM (2005) Systematics of Mesocestoides (Cestoda: Mesocestoididae): evaluation of molecular and morphological variation among isolates. J Parasitol 91(6):1435–1443

    Article  CAS  PubMed  Google Scholar 

  • Pappano DJ, Beehner JC (2014) Harem-holding males do not rise to the challenge: androgens respond to social but not to seasonal challenges in wild geladas. R Soc Open Sci 1(1):140081

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Parker GA, Ball MA, Chubb JC (2015) Evolution of complex life cycles in trophically transmitted helminths. II. How do life-history stages adapt to their hosts? J Evol Biol 28(2):292–304

    Article  CAS  PubMed  Google Scholar 

  • Peña N, Morales J, Morales-Montor J, Vargas-Villavicencio A, Fleury A, Zarco L et al (2007) Impact of naturally acquired Taenia solium cysticercosis on the hormonal levels of free ranging boars. Vet Parasitol 149(1):134–137

    Article  PubMed  CAS  Google Scholar 

  • Plesker R, Bauer C, Tackmann K, Dinkel A (2001) Hydatid echinococcosis (Echinococcus granulosus) in a laboratory colony of pig-tailed macaques (Macaca nemestrina). J Vet Med B 48(5):367–372

    Google Scholar 

  • Plesker R, Nadler T, Dinkel A, Romig T (2009) A case of an Echinococcus ortleppi infestation in a red-shanked douc langur (Pygathrix nemaeus) in northern Vietnam. Vietnam J Primatol 3:75

    Google Scholar 

  • Poulin R (1997) Species richness of parasite assemblages: evolution and patterns. Annu Rev Ecol Evol Syst 28(1):341–358

    Article  Google Scholar 

  • Poulin R (2007) Evolutionary ecology of parasites. Princeton University Press, Princeton

    Book  Google Scholar 

  • Poulin R (2010) Parasite manipulation of host behavior: an update and frequently asked questions. Adv Study of Behav 41:151–186

    Article  Google Scholar 

  • Poulin R, Fredensborg BL, Hansen EK, Leung TL (2005) The true cost of host manipulation by parasites. Behav Process 68(3):241–244

    Article  Google Scholar 

  • Rabiela MT, Rivas A, Flisser A (1989) Morphological types of Taenia solium cysticerci. Parasitol Today 5(11):357–359

    Article  CAS  PubMed  Google Scholar 

  • Rehmann P, Gröne A, Lawrenz A, Pagan O, Gottstein B, Bacciarini LN (2003) Echinococcus multilocularis in two lowland gorillas (Gorilla g. gorilla). J Comp Pathol 129(1):85–88

    Google Scholar 

  • Rietschel W, Kimmig P (1994) Alveolar echinococcosis in a cynomolgus monkey. Tierarztl Prax 22(1):85–88

    CAS  PubMed  Google Scholar 

  • Robar N, Burness G, Murray DL (2010) Tropics, trophics and taxonomy: the determinants of parasite-associated host mortality. Oikos 119(8):1273–1280

    Article  Google Scholar 

  • Rodhain J, Wanson M (1954) Un nouveau cas de coenurose chez le babouin, Theropithecus gelada RUPPELL. Riv Parassitol 15(4):613–620

    Google Scholar 

  • Rogan MT, Marshall I, Reid GDF, Macpherson CNL, Craig PS (1993) The potential of vervet monkeys (Cercopithecus aethiops) and baboons (Papio anubis) as models for the study of the immunology of Echinococcus granulosus infections. Parasitology 106(5):511–517

    Google Scholar 

  • Romig T, Dinkel A, Mackenstedt U (2006) The present situation of echinococcosis in Europe. Parasitol Int 55:S187–S191

    Article  PubMed  Google Scholar 

  • Romig T, Deplazes P, Jenkins D, Giraudoux P, Massolo A, Craig PS et al (2017) Ecology and life cycle patterns of Echinococcus species. In: Thompson RCA, Deplazes P, Lymbery AJ (eds) Advances in parasitology: echinococcus and echinococcosis, part A, vol 95. Academic Press, London, pp 213–314

    Google Scholar 

  • Sandground JH (1937) On a coenurus from the brain of a monkey. J Parasitol 23(5):482–490

    Article  Google Scholar 

  • Sato C, Kawase S, Yano S, Nagano H, Fujimoto S, Kobayashi N et al (2005) Outbreak of larval Echinococcus multilocularis infection in Japanese monkey (Macaca fuscata) in a zoo, Hokkaido: western blotting patterns in the infected monkeys. J Vet Med Sci 67(1):133–135

    Google Scholar 

  • Schneider-Crease I (2017) Predictors, costs, and consequences of larval tapeworm infection in Geladas (Theropithecus gelada). [ProQuest Dissertations Publishing]. http://search.proquest.com/docview/1934334130/

  • Schneider-Crease I, Snyder-Mackler N, Jarvey JC, Bergman TJ (2013) Molecular identification of Taenia serialis coenurosis in a wild Ethiopian gelada (Theropithecus gelada). Vet Parasitol 198(1):240–243

    Google Scholar 

  • Schneider-Crease I, Griffin RH, Gomery MA, Bergman TJ, Beehner JC (2017a) High mortality and low reproductive success associated with parasitism in geladas (Theropithecus gelada) in the Simien Mountains National Park, Ethiopia. Am J Primatol 77:579–594

    Google Scholar 

  • Schneider-Crease I, Griffin RH, Gomery MA, Dorny P, Noh JC, Handali S, Chastain HM et al (2017b) Identifying wildlife reservoirs of neglected taeniid tapeworms: non-invasive diagnosis of endemic Taenia serialis infection in a wild primate population. PLoS Negl Trop Dis 11(7):e0005709

    Google Scholar 

  • Schwartz B (1926) A subcutaneous tumor in a baboon due to Multiceps larvae. J Parasitol 12:159

    Google Scholar 

  • Schwartz B (1927) A subcutaneous tumor in a primate caused by tapeworm larvae experimentally reared to maturity in dogs. J Agric Res 35(5):471–480

    Google Scholar 

  • Sciutto E, Fragoso G, Diaz ML, Valdez F, Montoya RM, Govezensky T et al (1991) Murine Taenia crassiceps cysticercosis: H-2 complex and sex influence on susceptibility. Parasitol Res 77(3):243–246

    Article  CAS  PubMed  Google Scholar 

  • Scott HH (1926) Report on deaths occurring in the society’s gardens during the year 1925. Proc Zool Soc London 96(1):231–244

    Article  Google Scholar 

  • Shahar R, Horowitz IH, Aizenberg I (1995) Disseminated hydatidosis in a ring-tailed lemur (Lemur catta): a case report. J Zoo Wildl Med 26:119–122

    Google Scholar 

  • Simpson ER, Mahendroo MS, Means GD, Kilgore MW, Hinshelwood MM, Graham-Lorence S et al (1994) Aromatase cytochrome P450, the enzyme responsible for estrogen biosynthesis. Endocr Rev 15(3):342–355

    CAS  PubMed  Google Scholar 

  • Spangelo BL, Judd AM, Call GB, Zumwalt J, Gorospe WC (1995) Role of the cytokines in the hypothalamic-pituitary-adrenal and gonadal axes. Neuroimmunomodulation 2(5):299–312

    Article  CAS  PubMed  Google Scholar 

  • Sulaiman S, Williams JF, Wu D (1986) Natural infections of vervet monkeys (Cercopithecus aethiops) and African red monkeys (Erythrocebus patas) in Sudan with taeniid cysticerci. J Wildl Dis 22(4):586–587

    Google Scholar 

  • Taniyama H (1996) A natural case of larval echinococcosis caused by Echinococcus multilocularis in a zoo orangutan (Pongo pygmaeus). In: Uchino J, Sat N (eds) Alveolar echinococcosis. Strategy for eradication of alveolar echinococcosis of the liver, Fuji Shoin, Sapporo, pp 65–67

    Google Scholar 

  • Tappe D, Brehm K, Frosch M, Blankenburg A, Schrod A, Kaup FJ, Mätz-Rensing K (2007) Echinococcus multilocularis infection of several old-world monkey species in a breeding enclosure. Am J Trop Med Hyg 77(3):504–506

    Google Scholar 

  • Tappe D, Berkholz J, Mahlke U, Lobeck H, Nagel T, Haeupler A et al (2016) Molecular identification of zoonotic tissue-invasive tapeworm larvae other than Taenia solium in suspected human cysticercosis cases. J Clin Microbiol 54(1):172–174

    Google Scholar 

  • Terrazas LI, Bojalil R, Govezensky T, Larralde C (1994) A role for 17-β-estradiol in immunoendocrine regulation of murine cysticercosis (Taenia crassiceps). J Parasitol 80:563–568

    Article  CAS  PubMed  Google Scholar 

  • Thompson RCA (2017) Biology and systematics of echinococcus. In: Thompson RCA, Deplazes P, Lymbery AJ (eds) Advances in parasitology: echinococcus and echinococcosis, part A, vol 95. Academic Press, London, pp 65–109

    Google Scholar 

  • Torgerson PR, Gulland FMD, Gemmell MA (1992) Observations on the epidemiology of Taenia hydatigena in Soay sheep on St Kilda. Vet Rec 131(10):218–219

    Article  CAS  PubMed  Google Scholar 

  • Torgerson PR, Pilkington J, Gulland FMD, Gemmell MA (1995) Further evidence for the long-distance dispersal of taeniid eggs. Int J Parasitol 25(2):265–267

    Article  CAS  PubMed  Google Scholar 

  • Torgerson PR, Keller K, Magnotta M, Ragland N (2010) The global burden of alveolar echinococcosis. PLoS Negl Trop Dis 4(6):e722

    Article  PubMed  PubMed Central  Google Scholar 

  • Tsubota K, Nakatsuji S, Matsumoto M, Fujihira S, Yoshizawa K, Okazaki Y, Murakami Y, Anagawa A, Oku Y, Oishi Y (2009) Abdominal cysticercosis in a cynomolgus monkey. Vet Parasitol 161(3–4):339–341

    Google Scholar 

  • Urbain A, Bullier P (1935) Un cas de cenurose conjonctive chez un gelada. Bull Acad Vet Fr 8(6):322–324

    Google Scholar 

  • Vargas-Villavicencio JA, Larralde C, De León-Nava MA, Morales-Montor J (2005) Regulation of the immune response to cestode infection by progesterone is due to its metabolism to estradiol. Microbes Infect 7(3):485–493

    Article  CAS  PubMed  Google Scholar 

  • Vickers JH, Penner LR (1968) Cysticercosis in four rhesus brains. J Am Vet Med Assoc 153(7):868–871

    CAS  PubMed  Google Scholar 

  • Walker AE (1936) Cysticercosis cellulosæ in the monkey: a case report. J Comp Pathol Ther 49:141–145

    Article  Google Scholar 

  • Zhang L, Hu M, Jones A, Allsopp BA, Beveridge I, Schindler AR, Gasser RB (2007) Characterization of Taenia madoquae and Taenia regis from carnivores in Kenya using genetic markers in nuclear and mitochondrial DNA, and their relationships with other selected taeniids. Mol Cell Probes 21(5):379–385

    Article  CAS  PubMed  Google Scholar 

  • Zuk M (2009) The sicker sex. PLoS Pathog 5(1):e1000267

    Article  PubMed  PubMed Central  CAS  Google Scholar 

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Acknowledgments

Schneider-Crease acknowledges funding from a Postdoctoral Research Fellowship awarded by the NSF’s Directorate for Social, Behavioral, and Economic Sciences in 2017. She also acknowledges support from the Snyder-Mackler lab at the University of Washington and Arizona State University, particularly from N Snyder-Mackler and KL Chiou, from the Simien Mountains Gelada Research Project field team, and from RH Griffin and the Nunn lab at Duke University.

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Schneider-Crease, I. (2020). Larval Tapeworm Infections in Primates: Coenurosis, Cysticercosis, and Echinococcosis. In: Knauf, S., Jones-Engel, L. (eds) Neglected Diseases in Monkeys. Springer, Cham. https://doi.org/10.1007/978-3-030-52283-4_14

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