Abstract
In the present work, a morphological and biometrical study of whipworms Trichuris Roederer, 1761 (Nematoda: Trichuridae) parasitizing Colobus guereza kikuyensis has been carried out. Biometrical and statistical data showed that the mean values of individual variables between Trichuris suis and Trichuris sp. from C. g. kikuyensis differed significantly (P < 0.001) when Student’s t test was performed: seven male variables (width of esophageal region of body, maximum width of posterior region of body, width in the place of junction of esophagus and the intestine, length of bacillary stripes, length of spicule, length of ejaculatory duct, and distance between posterior part of testis and tail end of body) and three female variables (width of posterior region of body, length of bacillary stripes, and distance of tail end of body and posterior fold of seminal receptacle). The combination of these characters permitted the discrimination of T. suis with respect to Trichuris sp. from C. g. kikuyensis, suggesting a new species of Trichuris. Furthermore, males of Trichuris sp. from C. g. kikuyensis showed a typical subterminal pericloacal papillae associated to a cluster of small papillae that were absent in males of T. suis, while females of Trichuris from Colobus appeared with a vulval region elevated/over-mounted showing a crater-like appearance. The everted vagina showed typical triangular sharp spines by optical microscopy and SEM. Thus, the existence of a new species of Trichuris parasitizing C. g. kikuyensis has been proposed.
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References
Barus V, Kotrla B, Tenora F (1978) Scanning electron microscopic study of vulva of some trichurids (Nematoda). Folia Parasitol 25:31–34
Beer RJS (1976) The relationship between T. trichiura (Linnaeus 1758) of man and Trichuris suis (Schrank 1788) of the pig. Res Vet Sci 20:47–54
Callejón R, Nadler S, De Rojas M, Zurita A, Petrášová J, Cutillas C (2013) Molecular characterization and phylogeny of whipworm nematodes inferred from DNA sequences of cox1 mtDNA and 18S rDNA. Parasitol Res 112(11):3933–3949
Chandler AC (1930) Specific characters in the genus Trichuris with a description of the new species Trichuris tenuis from a camel. J Parasitol 16:198–206
Creplin FCH (1825) Observationes de Entozois (Gryphisw) 86
Cutillas C, Callejón R, De Rojas M, Tewes B, Ubeda JM, Ariza C, Guevara DC (2009) Trichuris suis and T. trichiura are different nematode species. Acta Trop 11:299–307
Dinnik NN (1938) Differences between Trichocephalus trichiura and Trichocephalus suis (Schrank, 1788). Med Parazitol Parazit Bolezn 1:907–908
Dujardin MF (1845) Histoire naturelle des Helminthes ou vers Intestinaux. Paris, pp 564
Dunn JJ, Columbus ST, Aldeen WE, Davis M, Carroll KC (2002) Trichuris vulpis recovered from a patient with chronic diarrhea and five dogs. J Clin Microbiol 40:2703
Elliot DE, Summers RW, Weinstock JV (2007) Helminths as governors of inmune-mediated inflammation. Int J Parasitol 37:457–464
Feliú C, Spakulová M, Casanova JC, Renaud F, Morand S, Hugot JP, Santalla F, Durand P (2000) Genetic and morphological heterogeneity in small rodent whipworms in southwestern Europe: characterization of Trichuris muris and description of Trichuris arvicolae n. sp. (Nematoda: Trichuridae). J Parasitol 86:442–449
Flynn RJ (1973) Parasites of laboratory animals. Iowa state University Press, Ames
Gibbons LM (1986) SEM guide to the morphology of nematode parasites of vertebrates. CAB, Stough
Horii Y, Usui M (1985) Experimental transmission of Trichuris ova from monkeys to man. Trans R Soc Trop Med Hyg 79:423
Itoh K, Oku M, Okamoto M, Ohbayashi M, Kitamura Y, Shibahara T (1988) Helminth parasites of Japanese monkey Macaca fuscata fuscata in Ehime Prefecture, Japan. J Vet Res 36:235–247
Jessee MT, Schilling PW, Stunkard JA (1970) Identification of intestinal helminth eggs in old world primates. Lab Anim Care 20:83–87
Knight RA (1971) Redescription of Trichuris discolor (Von Listow, 1906) and T. skrjabini (Baskakov, 1924) from domestic ruminants in the United States and comparisons with T. ovis (Abildgaard, 1795). J Parasitol 57:302–310
Knight RA (1984) Morphological differences in Trichuris ovis associated with different host species. J Parasitol 70:842–843
Konno S (1958) On Trichuris trichiura in Macaca fuscata fuscata and Papio papio. Med Biol 48:21–24
Lanfredi RM, De Souza W, Correa Gomes D (1995) Comparative study of four species of Trichuris Roederer, 1761 (Nematoda, Trichurinae) by scanning electron microscopy. Mem Inst Oswaldo Cruz Rio de Janeiro 90:489–496
Leuckart R (1876) Cited by Schwartz (1926)
Liu GH, Gasser RB, Su A, Nejsum P, Peng L, Lin RQ, Li MW, Xu MJ, Zhu XQ (2012) Clear genetic distinctiveness between human- and pig-derived Trichuris based on analysis of mitochondrial datasets. PLoS Negl Trop Dis 6:e1539
Mirdha BR, Singh YG, Samantray JC, Mishra B (1998) Trichuris vulpis infection in slum children. Indian J Gastroenterol 17:154
Nissen S, Al-Jubury A, Hansen TV, Olsen A, Christensen H (2012) Genetic analysis of Trichuris suis and T. trichiura recovered from humans and pigs in a sympatric setting in Uganda. Vet Parasitol 188:68–77
Oliveros R, Cutillas C, Arias P, Guevara D (1998) Morphologic, biometric and isoenzyme characterization of Trichuris suis. Parasitol Res 84:513–515
Ooi HK, Tenora F, Itoh K, Kamiya M (1993) Comparative study of Trichuris trichiura from non-human primates and from man and their difference with T. suis. J Vet Med Sci 55:363–366
Pavlovsky EN, Sondak VA (1951) On the specific differences between the whipworm of man and swine. Parazitol Sbo Zool Inst AN SSSR 13:35–44
Pedersen S, Saeed I, Michaelsen KF, Friis H, Murrell KD (2002) Impact of protein energy malnutrition on Trichuris suis infection in pigs concomitantly infected with Ascaris suum. Parasitology 124(05):561–568
Ravasi DF, O’Riain MJ, Davids F, Illing N (2012) Phylogenetic evidence that two distinct Trichuris genotypes infect both humans and nonhuman primates. PLoS ONE 7:e44187
Reddy A, Fried B (2007) The use of Trichuris suis and other helminthes therapies to treat Crohn’s disease. Parasitol Res 100:921–927
Reddy A, Fried B (2009) An update on the use of helminths to treat Crohn’s and other autoimmunune diseases. Parasitol Res 104(2):217–221
Rickard LG, Bishop JK (1991) Redescription of Trichuris tenuis Chandler, 1930, from llamas (Lama glama) in Oregon with a key to the species of Trichuris present in North American ruminants. J Parasitol 71:70–75
Sarwar MM (1959) Reconstruction of the genus Trichuris and a short review of its taxonomy and morphology. Biología (Lahore) 5:19–35
Schneider A (1866) Cited by Schwartz (1926)
Schwartz B (1926) A possible new source of infection of man with Trichuris, with a consideration of the question of physiological varieties among helminths. Archiv Schiffs-u Trophyg 9:544–577
Singh S, Samantaray JC, Singh N, Das GB, Verma IC (1993) Trichuris vulpis infection in an Indian tribal population. J Parasitol 79:457
Skrjabin KI, Shikhobalova NP, Orlow IV (1957) Trichocephalidae and Capillariidae of animals and the man and the diseases caused by them. Essentials of Nematodology, vol. VI. Translated by Dr. A. Birron. Edited by D. Greenberg Israel Program for Scientific Translations Ltd. Keter Press Wiener Binder Ltd., Jerusalem
Sondak VA (1948) On the question of species independence of whipworms of man and swine. Parazitol Sbo Zool Inst AN SSSR 10:195–204
Soulsby EJL (1982) Helminths, arthropods and protozoa of domesticated animals, 7th edn. Bailliere Tindall, London
Spakulová M (1994) Discriminant analysis as a method for the numerical evaluation of taxonomic characters in male trichurid nematodes. Syst Parasitol 29:113–119
Spakulová M, Lýsek H (1981) A biometric study of two populations of Tricocephalus suis Schrank, 1788 from swine and wild boars. Helminthologia 18:91–98
Summers RW, Elliott DE, Qadir K, Urban JF, Thompson R, Weinstock JV (2003) Trichuris suis seems to be safe and possibly effective in the treatment of inflammatory bowel disease. Am J Gastroenterol 98:2034–2041
Summers RW, Elliott DE, Urban JF Jr, Thompson R, Weinstock JV (2005) Trichuris suis therapy in Crohn’s disease. Gut 54:87–90
Suriano DM, Navone GT (1994) Three new species of the genus Trichuris Roederer, 1761 (Nematoda: Trichuridae) from Cricetidae and Octodontidae rodents in Argentina. Res Rev Parasitol 54:39–46
Tenora F, Hovorka I, Hejlková D (1988) A supplement to the scanning electron microscopy of some Trichocephalus spp. (Nematoda). Helminthologia 25:227–234
Tenora F, Kamiya M, Spakulová M, Stanek M, Ooi HK (1993) Scanning electron microscopy of Trichuris suis and Trichuris vulpis from Slovakia and Japan. Helminthologia 30:93–98
Vásquez O, Martínez I, Romero R, Valencia S, Tay J (1997) Infección Mixta por Trichuris trichiura y por Trichuris vulpis. Rev Gastroenterol Peru 17:1
Zaman V (1984) Scanning electron microscopy of Trichuris trichiura (Nematoda). Acta Trop 41:287–292
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The present work has been supported by a grant of the V Plan Propio de investigación of the University of Seville, Spain.
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Cutillas, C., de Rojas, M., Zurita, A. et al. Trichuris colobae n. sp. (Nematoda: Trichuridae), a new species of Trichuris from Colobus guereza kikuyensis . Parasitol Res 113, 2725–2732 (2014). https://doi.org/10.1007/s00436-014-3933-6
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DOI: https://doi.org/10.1007/s00436-014-3933-6