Hostname: page-component-78c5997874-s2hrs Total loading time: 0 Render date: 2024-11-15T15:19:03.637Z Has data issue: false hasContentIssue false

Morphological, Molecular, and Pathological Appraisal of Hymenolepis nana (Hymenolepididae) Infecting Laboratory Mice (Mus musculus)

Published online by Cambridge University Press:  05 March 2020

Ebtsam Al-Olayan
Affiliation:
Department of Zoology, College of Science, King Saud University, Riyadh, Saudi Arabia
Maha Elamin
Affiliation:
Department of Zoology, College of Science, King Saud University, Riyadh, Saudi Arabia
Eman Alshehri
Affiliation:
Department of Zoology, College of Science, King Saud University, Riyadh, Saudi Arabia
Abeer Aloufi
Affiliation:
Department of Zoology, College of Science, King Saud University, Riyadh, Saudi Arabia Research Chair of Vaccines, Deanship of Scientific Research, King Saud University, Riyadh, Saudi Arabia
Zainab Alanazi
Affiliation:
Department of Zoology, College of Science, King Saud University, Riyadh, Saudi Arabia
Mina Almayouf
Affiliation:
Department of Zoology, College of Science, King Saud University, Riyadh, Saudi Arabia
Lamia Bakr
Affiliation:
Department of Zoology, Faculty of Science, Tanta University, Tanta, Egypt
Rewaida Abdel-Gaber*
Affiliation:
Department of Zoology, College of Science, King Saud University, Riyadh, Saudi Arabia Department of Zoology, Faculty of Science, Cairo University, Cairo, Egypt
*
*Author for correspondence: Rewaida Abdel-Gaber, E-mail: [email protected], [email protected]
Get access

Abstract

Hymenolepis nana, typically a parasite found in conventionally established mouse colonies, has zoonotic potential characterized by autoinfection and direct life cycle. The objective of this study was to determine the rate of parasite infection in laboratory mice. The hymenolepidide cestode infected 40% of the 50 mice sampled. The rate of infection in males (52%) was higher than in females (28%). Morphological studies on the cestode parasite showed that worms had a globular scolex with four suckers, a retractable rostellum with 20–30 hooks, and a short unsegmented neck. In addition, the remaining strobila consisted of immature, mature, and gravid proglottids, irregularly alternating genital pores, lobulated ovaries, postovarian vitelline glands, and uteri with up to 200 eggs in their gravid proglottids. The parasite taxonomy was confirmed by using molecular characterization based on the sequence analysis of the mitochondrial cytochrome c oxidase subunit 1 (mtCOX1) gene. The parasite recovered was up to 80% identical to other species in GenBank. High blast scores and low divergence were noted between the isolated parasite and previously described H. nana (gb| AP017666.1). The phylogenetic analysis using the COX1 sequence places this hymenolepidid species of the order Cyclophyllidea.

Type
Micrographia
Copyright
Copyright © Microscopy Society of America 2020

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Al Quraishy, S, Abdel-Gaber, R, Alajmi, R, Dkhil, MA, Al Jawher, M & Morsy, K (2019). Morphological and molecular appraisal of cyclophyllidean cestoda parasite Raillietina saudiae sp. Nov. infecting the domestic pigeon Columba livia domestica and its role as a bio-indicator for environmental quality. Parasitol Int 71, 5972. https://doi.org/10.1016/j.parint.2019.03.002CrossRefGoogle ScholarPubMed
Andrews, RH & Chilton, NB (1999). Multilocus enzyme electrophoresis: A valuable technique for providing answers to problems in parasite systematics. Int J Parasitol 29, 213253. https://doi.org/10.1016/s0020-7519(98)00168-4Google ScholarPubMed
Ariola, V (1899). II gen. Scyphocephalus Rigg. E proposta di una nuova classificazione dei cestodi. Atti Soc Ligust Sci Nat Geogr 10, 160167.Google Scholar
Awwad, MH, Lashien, GH, Abou, E & Kheir, SM (2001). Using restriction-site variation of PCR-amplified 18S ribosomal RNA gene for phylogenetic analysis of Hymenolepis spp. Egypt J Hosp Med 5, 3848. https://doi.org/10.12816/EJHM.2001.18861Google Scholar
Baylis, HA (1924) The range of variation of Hymenolepis nana in rats and mice. Parasitology XVI, 415418. https://doi.org/10.1017/S0031182000020308CrossRefGoogle Scholar
Bazzano, T, Restel, TI, Pinto, RM & Gomes, DC (2002). Patterns of infection with the nematodes Syphacia obvelata and Aspiculuris tetraptera in conventionally maintained laboratory mice. Mem Inst Oswaldo Cruz 97, 847853. https://doi.org/10.1590/s0074-02762002000600017CrossRefGoogle ScholarPubMed
Bhuiyan, AI, Ahmed, ATA & Khanum, H (1996). Endoparasitic helminths in Rattus Linnaeus and Bendicota bengalensis Gray. J Asiat Soc Bangladesh Sci 22, 189194.Google Scholar
Brooks, DR & Mayes, MA (2011). Hymenolepis asketus sp. n. (Cestoidea: Hymenolepididae) from the short-tailed shrew, Blarina brevicauda Say, from Nebraska. Proc Helminthol Soc Wash 44, 6062.Google Scholar
Bush, AO, Lafferty, KD, Lotz, J & Shostak, AW (1997). Parasitology meets ecology on its own terms: Margolis et al. revised. J Parasitol 83, 575583.10.2307/3284227CrossRefGoogle Scholar
Campbell, RA & Beveridge, I (1994) Order trypanorhyncha diesing, 1863. In Keys to the Cestode Parasites of Vertebrates, Khalil, LF, Jones, A & Bray, RA (Eds.), pp. 51148. Wallingford: CAB International.Google Scholar
Cheng, T, Liu, GH, Song, HQ, Lin, RQ & Zhu, XQ (2016). The complete mitochondrial genome of the dwarf tapeworm Hymenolepis nana — A neglected zoonotic helminth. Parasitol Res 115, 12531262. https://doi.org/10.1007/s00436-015-4862-8CrossRefGoogle ScholarPubMed
Coleman, AW (2003). ITS-2 is a double-edged tool for eukaryotic evolutionary comparisons. Trends Genet 19, 370375. https://doi.org/10.1016/S0168-9525(03)00118-5CrossRefGoogle Scholar
Coomansingh, C, Pinckney, RD, Bhaiyat, MI, Chikweto, S, Bitner, A, Baffa, A & Sharma, R (2009). Prevalence of endoparasites in wild rats in Grenada. West Indian Vet J 9, 1721.Google Scholar
Cummingham, LJ & Olson, PD (2010). Description of Hymenolepis microstoma (Nottingham: strain): a classical tapeworm model for research in the genomic era. Parasites and Vectors 3, 123.10.1186/1756-3305-3-123CrossRefGoogle Scholar
Czaplinski, B & Vaucher, C (1994) Family hymenolepididae ariola, 1899. In Keys to the Cestode Parasites of Vertebrates, Khalil, LF, Jones, A & Bray, RA (Eds), pp. 595663. Wallingford: CAB International.Google Scholar
D'Ovidio, D, Noviello, E, Pepe, P, Del Prete, L, Cringoli, G & Rinaldi, L (2015). Survey of Hymenolepis spp. in pet rodents in Italy. Parasitol Res 114, 43814384. https://doi.org/10.1007/s00436-015-4675-9CrossRefGoogle ScholarPubMed
Fedorko, JM (1999). Schistosoma japonicum in the black rat, Rattus mindanensis, from Leyte, Philippines, in relation to Oncomelania snail colonies with reference to other endoparasites. Southeast Asian J Trop Med Public Health 30, 343349.Google ScholarPubMed
Folstad, I & Karter, AJ (1992). Parasites, bright males, and the immunocompetence handicap. Am Nat 139, 603622.10.1086/285346CrossRefGoogle Scholar
Francisco, CJ, Almeida, A, Castro, AM & Santos, MJ (2010). Development of a PCR RFLP marker to genetically distinguish Prosorhynchus crucibulum and Prosorhynchus aculeatus. Parasitol Int 59, 4043. https://doi.org/10.1016/j.parint.2009.09.004CrossRefGoogle ScholarPubMed
Gardner, SL & Schmidt, GD (1987). Cestodes of the genus Hymenolepis Weinland, 1858 sensu stricto from pocket gophers Geomys and Thomomys spp. (Rodentia: Geomyidae) in Colorado and Oregon, with a discriminant analysis of four species of Hymenolepis. Can J Zool 66, 896903. https://doi.org/10.1139/z88-132CrossRefGoogle Scholar
Garedaghi, Y & Khaki, A (2014). Prevalence of gastrointestinal and blood parasites of rodents in Tabriz, Iran, with emphasis on parasitic zoonoses. Crescent J Med Biol Sci 1, 912.Google Scholar
Ghatani, S, Shylla, JA, Tandon, V, Chatterjee, A & Roy, B (2012). Molecular characterization of pouched amphistome parasites (Trematoda: Gastrothylacidae) using ribosomal ITS-2 sequence and secondary structures. J Helminthol 86, 117124. https://doi.org/10.1017/S0022149X11000125CrossRefGoogle Scholar
Gofur, MA, Khanum, H, Podder, MP & Nessa, Z (2010). Parasitic infestation in laboratory rat strain, Long-Evans (Rattus norvegicus Berkenhout, 1769). Univ J Zool Rajshahi 29, 4146. https://doi.org/10.3329/ujzru.v29i1.9464CrossRefGoogle Scholar
Gonçalves, L, Pinto, RM, Vicente, JJ, Noronha, D & Gomes, DC (1998). Helminth parasites of conventionally maintained laboratory mice — II. Inbred strains with an adaptation of the anal swab technique. Mem Inst Oswaldo Cruz 93, 121126. https://doi.org/10.1590/s0074-02761998000100023CrossRefGoogle ScholarPubMed
Gudissa, T, Mazengia, H, Alemu, S & Nigussie, H (2011). Prevalence of gastrointestinal parasites of laboratory animals at Ethiopian Health and Nutrition Research Institute (EHNRI). Addis Ababa J Infect Dis Immun 3, 15.Google Scholar
Guimarães, AO, Valenca, FM, Sousa, JBS, Souza, SA, Madi, RR & de Melo, CM (2014). Parasitic and fungal infections in synanthropic rodents in an area of urban expansion, Aracaju, Sergipe state, Brazil. Acta Sci Biol Sci 36, 113120.10.4025/actascibiolsci.v36i1.19760CrossRefGoogle Scholar
Guo, A (2016). The complete mitochondrial genome of the tapeworm Cladotaenia vulturi (Cestoda: Paruterinidae): Gene arrangement and phylogenetic relationships with other cestodes. Parasit Vectors 9, 475484. https://doi.org/10.1186/s13071-016-1769-xCrossRefGoogle ScholarPubMed
Hämäläinen, A, Heistermann, M & Kraus, C (2015). The stress of growing old: Sex-and season-specific effects of age on allostatic load in wild grey mouse lemurs. Oecologia 178, 10631075. https://doi.org/10.1007/s00442-015-3297-3CrossRefGoogle ScholarPubMed
Haukisalmi, V, Hardman, LM, Foronda, P, Feliu, C, Laakkonen, J, Niemimaa, J, Lehtonen, JT & Henttonen, H (2010). Systematic relationships of hymenolepidid cestodes of rodents and shrews inferred from sequences of 28S ribosomal RNA. Zool Scr 39, 631641. https://doi.org/10.1111/j.1463-6409.2010.00444.xCrossRefGoogle Scholar
Haukisalmi, V, Heino, M & Kaitala, V (1998). Body size variation in tapeworms (Cestoda): Adaptation to intestinal gradients? OIKOS 83, 152160. https://doi.org/10.2307/3546556CrossRefGoogle Scholar
Hayward, AD (2013). Causes and consequences of intra- and inter-host heterogeneity in defence against nematodes. Parasite Immunol 35, 362373. https://doi.org/10.1111/pim.12054Google ScholarPubMed
Hillis, DM & Bull, JJ (1993). An empirical test of bootstrapping as a method for assessing confidence in phylogenetic analysis. Syst Biol 42, 182192. https://doi.org/10.1093/sysbio/42.2.182CrossRefGoogle Scholar
Hilmy, IS (1936). Parasites from Liberia and French Guinea. Part 3: Cestodes from Liberia, 72 p. Le Caire: The Egyptian University.Google Scholar
Hoberg, EP, Jones, A & Bray, RA (1999). Phylogenetic analysis among the families of the Cyclophyllidea (Eucestoda) based on comparative morphology, with new hypotheses for co-evolution in vertebrates. Syst Parasitol 42, 5173. https://doi.org/10.1023/a:1006100629059CrossRefGoogle ScholarPubMed
Huda-Thaher, A (2012). Prevalence of Hymenolepis nana infections in Abu Ghraib City (Baghdad/Iraq). Iraqi Postgraduate Med J 11, 581584.Google Scholar
Illiger, JK (1811). Prodromus Systematis Mammalium et Avium additis terminis zoographicis utriudque classis. C. Salfeld, Berlin, i-xviii, 1-301.Google Scholar
Ito, A (2003). Immunology in cestode infection (2). Immunity to the larval cestodes. In Progress of Parasitology Research in Japan, Tokyo, Otsuru, M, Kamegai, S & Hayashi, S (Eds), p. 327337. Tokyo: Meguro Parasitological Museum.Google Scholar
Ito, A (2015). Basic and applied problems in developmental biology and immunobiology of cestode infections: Hymenolepis, Taenia and Echinococcus. Parasite Immunol 37, 5369. https://doi.org/10.1111/pim.12167CrossRefGoogle ScholarPubMed
Ito, A & Yamamoto, M (1976). The mode of active protection against Hymenolepis nana reinfection in mice inoculated with different doses of shell-free eggs. Jpn J Parasitol 25, 247253.Google Scholar
Janicki, C (1904). Zur Kenntniss einiger Saügetiercestoden. Zool Anzeig XXVII, 770782.Google Scholar
Joyeux, PC & Kobozieff, NI (1928). Recherches sur L’ Hymenolepis microstoma (Dujardin, 1845). Annales de Parasitologie 6, 5979.10.1051/parasite/1928061059CrossRefGoogle Scholar
Kandil, OM, Mahmoud, MS, Allam, NAT & El Namaky, AH (2010). Mitochonderial cytochrome c oxidase subunit 1 (cox 1) gene sequence of the Hymenolepis species. J Am Sci 6, 13461353.Google Scholar
Kataranovski, M, Zolotarevski, L, Belij, S, Mirkov, I, Stošić, J, Popov, A & Kataranovski, D (2010). First record of Calodium hepaticum and Taenia taeniaeformis liver infection in wild Norway rats (Rattus norvegicus) in Serbia. Arch Biol Sci 62, 431440. https://doi.org/10.2298/ABS1002431KCrossRefGoogle Scholar
Khatoon, N, Bilqees, FM, Shahwar, D & Rizwana, AG (2004). Histopathological alterations associated with Syphacia spp. (Nematode) in the intestine of Nesokia indica. Turk J Zool 28, 345351.Google Scholar
Kim, BJ, Song, KS, Kong, HH, Cha, HJ & Ock, M (2014). Heavy Hymenolepis nana infection possibly through organic foods: Report of a case. Korean J Parasitol 52, 8587. https://doi.org/10.3347/kjp.2014.52.1.85CrossRefGoogle ScholarPubMed
Klein, SL (2004). Hormonal and immunological mechanisms mediating sex differences in parasite infection. Parasite Immunol 26, 247264. https://doi.org/10.1111/j.0141-9838.2004.00710.xCrossRefGoogle ScholarPubMed
Lapage, G (1951). Parasitic Animals. UK: The University Press.Google Scholar
Lecanidou, R, Douris, V & Rodakis, GC (1994). Novel features of metazoan mtDNA revealed from sequence analysis of three mitochondrial DNA segments of the land snail Albinaria turrita (Gastropoda: Clausiliidae). J Mol Evol 38, 369382.10.1007/BF00163154CrossRefGoogle Scholar
Lichtenfels, JR, Hoberg, EP & Zarlenga, DS (1997). Systematics of gastrointestinal nematodes of domestic ruminants: Advances between 1992 and 1995 and proposals for future research. Nucleic Acids Res 18, 41234130. https://doi.org/10.1016/s0304-4017(97)00099-xGoogle Scholar
Linnaeus, C (1758). Systema naturæ per regna tria naturæ, secundum classes, ordines, genera, species, cum characteribus, differentiis, synonymis, locis, vol. 1, 10th ed, pp. 14, 1–824. Stockholm: Laurentius Salvius.Google Scholar
Macnish, MG, Morgan-Ryan, UM, Monis, PT, Behnke, JM & Thompson, RCA (2002). A molecular phylogeny of nuclear and mitochondrial sequences in Hymenolepis nana (Cestoda) supports the existence of a cryptic species. Parasitology 125, 567575. https://doi.org/10.1017/s0031182002002366CrossRefGoogle ScholarPubMed
Macy, RW (1931). A key to the species of Hymenolepis found in bats and the description of a new species, H. christensoni, from Myotis lucifugus. Trans Am Microsc Soc 50, 344347. https://doi.org/10.2307/3222075CrossRefGoogle Scholar
Macy, RW (1947). Parasites found in certain Oregan bats with the description of a new cestode, Hymenolepis genschi. Am Midl Nat 37, 375378.10.2307/2421660CrossRefGoogle Scholar
Macy, RW & Rausch, RL (1946). Morphology of a new species of bat cestode, Hymenolepis roudabushi, and a note on Hymenolepis christensoni Macy. Trans Am Microsc Soc 65, 173175. https://doi.org/10.2307/3223178CrossRefGoogle Scholar
Mahami-Oskouei, M, Dalimi, A, Forouzandeh-Moghadam, M & Rokni, M (2011). Molecular identification and differentiation of Fasciola isolates using PCR-RFLP method based on internal transcribed spacer ITS-1 58S rDNA ITS-2. Iran J Parasitol 6, 3542.Google Scholar
Makarikov, AA, Tkach, VV & Bush, SE (2013). Two new species of Hymenolepis (Cestoda: Hymenolepididae) from murid rodents (Rodentia: Muridae) in the Philippines. Journal of Parasitology 99, 847855.10.1645/12-173.1CrossRefGoogle Scholar
Makarikova, TA, Gulyaev, VD, Tiunov, MP & Feng, J (2010). Cestodes Paramilina nishidai (Sawada 1982) gen. n., comb. n. and Hymenolepis magna sp. n. (Cyclophyllidea: Hymenolepididae) from Chiroptera in China. Zoolgicheskii Zhurnal 89, 131139.Google Scholar
Mariaux, J (1998). A molecular phylogeny of the Eucestoda. J Parasitol 84, 114124. https://doi.org/10.2307/3284540CrossRefGoogle ScholarPubMed
Mayhew, RL (1925). Studies on the avian species of the cestode family Hymenolepididae. Illinois Biol Monogr 10, 125.Google Scholar
McLeod, JA (1933). A parasitological survey of the genus Citellus in Manitoba. Can J Res 9, 108127. https://doi.org/10.1139/cjr33-072CrossRefGoogle Scholar
Mehlhorn, H, Schmahl, G & Mevissen, I (2005). Efficacy of a combination of imidacloprid and moxidectin against parasites of reptiles and rodents: Case reports. Parasitol Res 97, S97101. https://doi.org/10.1007/s00436-005-1451-2CrossRefGoogle ScholarPubMed
Mohammad, MA & Hegazi, MA (2007). Intestinal permeability in Hymenolepis nana as reflected by non-invasive lactulosa/manitol dual permeability test and its impaction on nutritional parameters of patients. J Egypt Soc Parasitol 37, 877891.Google ScholarPubMed
Mohd Zain, SNM, Behnke, JM & Lewis, JW (2012). Helminth communities from two urban rat populations in Kuala Lumpur, Malaysia. Parasit Vectors 5, 47. https://doi.org/10.1186/1756-3305-5-47.CrossRefGoogle ScholarPubMed
Moniez, R (1880). Essai monographique sur les cysticerques (Thèse Méd. Lille). In-4° de 190 pl. Travaux de l'Institut Zoologique de Lille, III; p. 3.Google Scholar
Nicoll, W & Minchin, EA (1910). On two species of cysticercoides from the rat flea (Ceratophyllus fasciatus). Proc Zool Soc London 1013.Google Scholar
Niwa, A, Asano, K & Ito, A (1998). Eosinophil chemotactic factors from cysticercoids of Hymenolepis nana. J Helminthol 72, 273275. https://doi.org/10.1017/s0022149(00016552CrossRefGoogle ScholarPubMed
Nkouawa, A, Haukisalmi, V, Li, T, Nakao, M, Lavikainen, A, Chen, X, Henttonen, H & Ito, A (2016). Cryptic diversity in hymenolepidid tapeworms infecting humans. Parasitol Inter 65, 8386. https://doi.org/10.1016/j.parint.2015.10.009CrossRefGoogle ScholarPubMed
Okamoto, K (2003). Immunology in cestode infection (1). Adult worm parasitism in the intestine. In Progress of Parasitology Research in Japan, vol. 8, Otsuru, M, Kamegai, S & Hayashi, S (Eds), pp. 319325. Tokyo: Meguro Parasitological Museum.Google Scholar
Okamoto, M, Bessho, Y, Kamiya, M, Kurosawa, T & Horii, T (1995). Phylogenetic relationships within Taenia taniaeformis variants and other Taeniid cestodes inferred from the nucleotide sequences of the cytochrome C oxidase subunit I gene. Parasitol Res 81, 451458. https://doi.org/10.1007/bf00931785CrossRefGoogle ScholarPubMed
Okoye, CI & Obiezue, RNN (2008). A survey of the gut parasites of rodents in Nsukka ecological zone. Anim Res Inter 5, 846847. https://doi.org/10.4314/ari.v5i2.48744Google Scholar
Pakdel, N, Naem, S, Rezaei, F & Chalehchaleh, AA (2013). A survey on helminthic infection in mice (Mus musculus) and rats (Rattus norvegicus and Rattus rattus) in Kermanshah, Iran. Vet Res Forum 4, 105109.Google Scholar
Palm, HW (2004). The Trypanorhyncha Diesing, 1863, 710 p. Bogor: IPB-PKSPL Press.Google Scholar
Panti-May, JA, Digiani, MC, Palomo-Arjona, EE, Gurubel-gonzÁlez, YM, Navone, GT, Williams, CM, HernÁndez-Betancourt, SF & Robles, MDR (2018). A checklist of the helminthparasites of sympatric rodents from two Mayan villages in Yucatán, México. Zootaxa 4403(3), 495512.10.11646/zootaxa.4403.3.4CrossRefGoogle ScholarPubMed
Perec-Matysiak, A, Okulewicz, A, Hildebrand, J & Zalesny, G (2006). Helminth parasites of laboratory mice and rats. Wiad Parazytol 52, 99102.Google ScholarPubMed
Rahdar, M, Roointan, EAS, Vazirianzadeh, B & Alborzi, A (2017). Study of internal parasites of rodents in Ahvaz, South-West of Iran. Jundishapur J Health Sci 9, e29067.Google Scholar
Rausch, RL (1975). Cestodes of the genus Hymenolepis Weinland, 1858 (sensu lato) from bats in North America and Hawaii. Can J Zool 53, 15371551. https://doi.org/10.1139/z75-189CrossRefGoogle ScholarPubMed
Rehbinder, C, Baneux, P, Forbes, D & Winker, GC (1996). FELASA recommendations for the health monitoring of mouse, rat, hamster, gerbil, guinea pig and rabbit experimental units. Report of the Federation of European Laboratory Animal Science Associations (FELASA) Working Group on Animal Health accepted by the FELASA Board of Management, November 1995. Lab Anim 30, 193208. https://doi.org/10.1258/002367796780684881CrossRefGoogle Scholar
Richard, FO (2008). Diphyllobothrium, dipylidium, and hymenolepsis species. In Principles and Practice of Pediatric Infectious Diseases, 3rd ed., Long, SS, Pickering, LK and Prober, CG (Eds), chapter 279. Philadelphia: Churchill Livingstone Elsevier.Google Scholar
Roberts, L & Janovy, J (2000). Foundations of Parasitology, 6th ed.Boston, MA: Mcgraw-Hill Higher Education.Google Scholar
Robles, MR & Navone, GT (2007). A new species of Syphacia (Nematoda: Oxyuridae) from Oligoryzomys nigripes (Rodentia: Cricetidae) in Argentina. Parasitol Res 101, 10691075.10.1007/s00436-007-0595-7CrossRefGoogle Scholar
Rokni, MB, Mirhendi, H, Mizani, A, Mohebali, M, Sharbatkhori, M, Kia, EB, Abdoli, H & Izadi, S (2010). Identification and differentiation of Fasciola hepatica and Fasciola gigantica using a simple PCR restriction enzyme method. Exp Parasitol 124, 209213. https://doi.org/10.1016/j.exppara.2009.09.015CrossRefGoogle ScholarPubMed
Rosas, GA (1997). Diagnóstico: Parasitosis intestinal por Aspiculuris tetraptera. Anim Experim 2, 911.Google Scholar
Sadaf, HS, Khan, SS, Kanwal, N, Tasawer, BM & Ajmal, SM (2013). A review of diarrhoea causing Hymenolepis nana-Dwarf tapeworm. Int Res J Pharmacy 4, 3235.Google Scholar
Sawada, I & Harada, M (1990). A new Himenolepis species (Cestoda: Hymenolepididae) from Lesser Japanese Shrew-mole Dymecodon pilirostris of Nagano Prefecture, Japan. Proc Jap Soc Systemat Zool 42, 1013.Google Scholar
Sawada, I & Mohammad, KM (1989). Two new species of Hymenolepidid cestodes from Iraqi Bats, with record of a species of Davainidid cestode. Proc Jap Soc Syst Zool 39, 17.Google Scholar
Schantz, PM (2006). Tapeworms (Cestodiasis). Gastroenterol Clin North Am 25, 637653.10.1016/S0889-8553(05)70267-3CrossRefGoogle Scholar
Schiller, EL (1959). Experimental studies on morphological variation in the cestode genus Hymenolepis. III. X-irradiation as a mechanism for facilitating analyses in H. nana. Exp Parasitol 8, 427470. https://doi.org/10.1016/0014-4894(59)90033-5CrossRefGoogle ScholarPubMed
Schmidt, GD, Janovy, J & Roberts, LS (2009). Foundations of Parasitology, 8th ed. Boston, MA: McGraw-Hill.Google Scholar
Schultz, J, Maisel, S, Gerlach, D, Müller, T & Wolf, M (2005). A common core of secondary structure of the internal transcribed spacer 2 (ITS-2) throughout the Eukaryota. RNA 11, 361364. https://doi.org/10.1261/rna.7204505CrossRefGoogle Scholar
Sharma, D, Joshi, S, Vatsya, S & Yadav, CL (2013). Prevalence of gastrointestinal helminth infections in rodents of Tarai region of Uttarakhand. J Parasit Dis 37, 181184. https://doi.org/10.1007/s12639-012-0158-4CrossRefGoogle ScholarPubMed
Sharma, S, Lyngdoh, D, Roy, B & Tandon, V (2016). Differential diagnosis and molecular characterization of Hymenolepis nana and Hymenolepis diminuta (Cestoda: Cyclophyllidea: Hymenolepididae) based on nuclear rDNA ITS-2 gene marker. Parasitol Res 115, 42934298. https://doi.org/10.1007/s00436-016-5210-3CrossRefGoogle Scholar
Smyth, JD & McManus, DP (1989). The Physiology and Biochemistry of Cestodes. Cambridge: Cambridge University Press. https://doi.org/10.1017/CBO9780511525841CrossRefGoogle Scholar
Soares Magalhães, JR, Fançony, C, Gamboa, D, Langa, AJ, Sousa-Figueiredo, JC, Clements, ACA & Vaz Nery, S (2013). Extanding helminths control beyond STH and schistosomiaisis: The case of human hymenolepiasis. PLoS Negl Trop Dis 7, e2321. https://doi.org/10.1371/journal.pntd.0002321CrossRefGoogle Scholar
Steinmann, P, Cringoli, G, Bruschi, F, Matthys, B, Lohourignon, LK, Castagna, B, Maurelli, MP, Morgoglione, ME, Utzinger, J & Rinaldi, L (2012). FLOTAC for the diagnosis of Hymenolepis spp. infection: Proof-of-concept and comparing diagnostic accuracy with other methods. Parasitol Res 111, 749754. https://doi.org/10.1007/s00436-012-2895-9CrossRefGoogle Scholar
Stojcevic, D, Mihaljevic, Z & Marinculic, A (2004). Parasitological survey of rats in rural regions of Croatia. Vet Med 49, 7074. https://doi.org/10.17221/5679-VETMEDCrossRefGoogle Scholar
Tanideh, N, Sadiiadi, SM, Mohammadzadeh, T & Mehrabani, D (2010). Helminthic infections of laboratory animals in animal house of Shiraz University of Medical Sciences and the potential risks of Zoonotic infections for researches. Iran Red Crescent Med J 12, 151157.Google Scholar
Teodoro, TM, Jannotti-Passos, LK, Carvalho-Odos, S, Grijalva, MJ, Baús, EG & Caldeira, RL (2011). Hybridism between Biomphalaria cousin and Biomphalaria amazonica and its susceptibility to Schistosoma mansoni. Mem Inst Oswaldo Cruz 106, 851855. https://doi.org/1590/s0074-02762011000700011CrossRefGoogle Scholar
Thompson, JD, Gibson, TJ, Plewniak, F, Jeanmougin, F & Higgins, DG (1997). The CLUSTAL-X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25, 48764882. https://doi.org/10.1093/nar/25.24.4876.CrossRefGoogle ScholarPubMed
Thompson, RC (2015). Neglected zoonotic helminthes Hymenolepis nana, Echinococcus canadensis and Ancylostoma ceylanicum. Clin Microbiol Infect 21, 426432. https://doi.org/10.1016/j.cmi.2015.01.004CrossRefGoogle Scholar
Tubangui, MA (1931). Worm parasites of the brown rat (Mus norvegicus) in the Philippine Islands, with special reference to those forms that may be transmitted to human beings. Philippine J Sci 46, 537591.Google Scholar
Von Nickisch-Rosenegk, M, Lucius, R & Loos-Frank, B (1999). Contributions to the phylogeny of the Cyclophyllidea (Cestoda) inferred from mitochondrial 12S rDNA. J Mol Evol 48, 586596. https://doi.org/10.1007/pl00006501CrossRefGoogle ScholarPubMed
Wardle, MA & McLeod, JA (1952). The Zoology of Tapeworms, 780 p. Minneapolis, MN: University of Minnesota Press.Google Scholar
Weinland, DF (1858). Human Cestoides. An Essay on the Tapeworms of Man, p. 93. Cambridge: Metcalf & Co.Google Scholar
Yamaguti, S (1959). “Systema Helminth”. Cestodes of Vertebrates, vol. II. 860 p. New York, NY: Interscience Science Publisher Inc.Google Scholar
Yang, D, Zhao, W, Zhang, Y & Liu, A (2017). Prevalence of Hymenolepis nana and H. diminuta from Brown Rats (Rattus norvegicus) in Heilongiiang Province, China. Korean J Parasitol 55, 351355. https://doi.org/10.3347/kjp.2017.55.3.351CrossRefGoogle Scholar
Yoisefi, A, Eslami, A, Mobedi, I, Rahbari, S & Ronaghi, H (2014). Helminth infections of house mouse (Mus musculus) and wood mouse (Apodemus sylvaticus) from the suburban areas of Hamadan City, Western Iran. Iran J Parasitol 9, 511518.Google Scholar
Zhang, DX & Hewitt, GM (1996). Nuclear integrations: Challenges for mitochondrial DNA markers. Trends Eco Evol 11, 247251. https://doi.org/10.1016/0169-5347(96)10031-8CrossRefGoogle ScholarPubMed