Molecular characterization and histo-physiological alterations induced by concurrent helminthosis in the liver of urban commensal rodents in Punjab, India

Document Type : Full paper (Original article)


1 Department of Zoology, College of Basic Sciences and Humanities, Punjab Agricultural University, Ludhiana-141004, India

2 Department of Veterinary Parasitology, College of Veterinary Science, Guru Angad Dev Veterinary and Animal Sciences University, Ludhiana-141004, India



Background: Rodents harbour a number of parasites of public health importance, thus, they threaten human health and livestock. Aims: The present study aimed to characterize two helminthic species found in commensal rodents and record histo-physiological alterations induced by them. Methods: A total of 300 synanthropic rodents of three species: Rattus rattus (n=201), Bandicota bengalensis(n=90), and Mus musculus(n=09) were live trapped and necropsied in different seasons during November 2017 to October 2019 at Ludhiana, Punjab, India. Results: Liver of two species B. bengalensis (72.22%) and R. rattus (65.67%) were found infected with two helminthic parasites Taenia taeniaeformis, and Calodium hepaticum. These endoparasites were present either alone (4.33-6.33%) or as mixed infection (65.55%). The level of total proteins and liver marker enzymes including aspartate aminotransferase (AST) and alanine aminotransferase (ALT) were found significantly higher in the liver of rodent species infected with single and mixed infection compared to those with no infection. In histopathological assay, granulomatous liver lesions and necrosis of hepatocytes were seen which were associated with eggs and adults of C. hepaticum and inflammatory reaction in hepatic parenchyma adjoining to cysts of T. taeniaeformis. Based upon scanning electron microscopy (SEM) identification and molecular characterization using mitochondrial cytochrome oxidase I (COI) region, the metacestodes in whitish cysts were confirmed to be of T. taeniaeformis for the first time in Punjab, India. Conclusion: The study highlights an alarmingly high infection of rodents with zoonotic parasites and suggests immediate pest (rodent) control to check the dissemination of zoonotic diseases by helminth species under study.


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Aboel-Hadid, SM and Allam, GA (2007). Investigation of helminth parasitic infection oflaboratory animals (rats & mice) with specialreference to control of Hymenolepis nana as azoonotic parasite. Egypt. J. Exp. Biol. (Zool.), 3: 83-89.
Aghdam, MK; Karimi, A; Amanati, A; Ghoroubi, J; Khoddami, M; Shamsian, BS and Shamsizadeh Far, SZ (2015). Capillaria hepatica, A case report and review of the literatures. Arch. Pediatr. Infect. Dis., 3: e19398. doi: 10.5812/pedinfect.19398.
Bacigalupo, J (1922). Sobreunanuevae specie de Taenia, Taenia infantis. Semana Med., 26: 726-729.
Bergmeyer, HU (1974). Methods of enzymatic analysis. 2nd Edn., Vol. 2, New York, Academic Press. PP: 727-733.
Bhelonde, JJ and Ghosh, RC (2002). Incidence of Cysticercus fasciolaris in laboratory rats. Indian J. Vet. Pathol., 26: 69.
Botros, M and Sikaris, KA (2013). The deritis ratio: the test of time. Clin. Biochem. Rev., 34: 117-130.
Bowles, J; Blair, D and McManus, DP (1995). A molecular phylogeny of the human schistosomes. Mol. Phylogenet. Evol., 4: 103-109. doi: 10.1006/mpev.1995.1011.
Ceruti, R; Sonzogni, O; Origgi, F; Vezzoli, F; Cammarata, S; Giusti, AM and Scanziani, E (2001). Capillaria hepatica infection in wild brown rats (Rattus norvegicus) from the urban area of Milan, Italy. J. Vet. Med. B. 48: 235-240. doi: 10.1046/j.1439-0450.2001.00436.x.
Easterbrook, JD; Kaplan, JB; Glass, GE; Watson, J and Klein, SL (2008). A survey of rodent-borne pathogens carried by wild-caught Norway rats: a potential threat to laboratory rodent colonies. Lab. Anim., 42: 92-98. doi: 10.1258/la.2007.06015e.
Easterbrook, JD; Kaplan, JB; Vanasco, NB; Reeves, WK; Purcell, RH; Kosoy, MY; Glass, GE; Watson, J and Klein, SL (2007). A survey of zoonotic pathogens carried by Norway rats in Baltimore, Maryland, USA. Epidemiol. Infect., 135: 1192-1199. doi: 10.1017/s0950268806007746.
Ekanayake, S; Warnasuriya, ND; Samarakoon, PS; Abewickrama, H; Kuruppuarachchi, ND and Dissanaike, AS (1999). An unusual ‘infection’ of a child in Sri Lanka, with Taenia taeniaeformis of the cat. Ann. Trop. Med. Parasitol., 93: 869-873. doi: 10.1080/00034983.1999. 11813494.
El-Demerdash, FM (2004). Antioxidant effect of vitamin E and selenium on lipid peroxidation, enzyme activities and biochemical parameters in rats exposed to aluminium. J. Trace. Elem. Med. Biol., 18: 113-121.
Fagir, DM and El-Rayah, EA (2009). Parasites of the Nile rat in rural and urban regions of Sudan. Integr. Zool., 4: 179-187. doi: 10.1111/j.1749-4877.2009.00148.x.
Felsenstein, J (1985). Confidence limits on phylogenies: An approach using the bootstrap. Evolution. 39: 783-791.
Fuehrer, HP; Baumann, TA; Riedl, J; Treiber, M; Igel, P; Swoboda, P; Joachim, A and Noedl, H (2012). Endoparasites of rodents from the Chittagong Hill Tracts in Southeastern Bangladesh. Wien. Klin. Wochenschr., 124: 27-30. doi: 10.1007/s00508-012-0237-7.
Fuehrer, HP; Igel, P and Auer, H (2011). Capillaria hepatica in man: an overview of hepatic capillariosis and spurious infections. Parasitol. Res., 109: 969-979.
Herawati, NA and Sudarmaji (2019). Prevalence of infection of endoparasites and its intensity in small mammals’ liver captured from irrigated rice crop area and villages. Adv. Health Sci. Res., 24: 141-147.
Jithendran, KP and Somvanshi, R (1999). Studies on occurrence and pathology of spontaneous Cysticercus fasciolaris in laboratory mice and rats. J. Vet. Parasitol., 13: 61-62.
Kasarala, G and Tillmann, HL (2016). Standard liver tests. Clin. Liver Dis., 8: 13-18. doi: 10.1002/cld.562.
Kataranovski, D; Kataranovski, M and Deljanin, I (2010). Helminth fauna of Rattus norvegicus Berkenhout, 1769 from the Belgrade area, Serbia. Arch. Biol. Sci., 62: 1091-1100.
Kobayashi, K; Nakamura-Uchiyama, F; Nishiguchi, T; Isoda, K; Kokubo, Y; Ando, K; Katurahara, M; Sako, Y; Yanagida, T; Ito, A; Iwabuchi, S and Ohnishi, K (2013). Rare case of disseminated cysticercosis and taeniasis in a Japanese traveler after returning from India. Am. J. Trop. Med. Hyg., 89: 58-62. doi: 10.4269/ajtmh.12-0355.
Kumar, S; Stecher, G; Li, M; Knyaz, C and Tamura, K (2018). MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol. Biol. Evol., 35: 1547-1549.
Lowry, OH; Rosebrough, NJ; Farr, AL and Randall, AJ (1951). Protein measurement with folin phenol reagent. J. Biol. Chem., 193: 265-275.
MacArthur, WP (1924). A case of infestation of human liver with Hepaticola hepatica (Bancroft, 1893) Hall, 1916; with sections from the liver. Proc. R. Soc. Med., 17: 83-84.
Mcinnes, E; Kohn, H and Carmichael, I (2014). Larvae of Taenia taeniaeformis in the liver of a laboratory rat (Rattus norvegicus). Ann. Clin. Pathol., 2: 2-5.
Mohd Zain, SN; Behnke, JM and Lewis, JW (2012). Helminth communities from two urban rat populations in Kuala Lumpur, Malaysia. Parasit. Vectors. 5: 47-70. doi: 10.1186/1756-3305-5-47.
Moudgil, AD; Singla, LD; Gupta, K; Daundkar, PS and Vemu, B (2013). Histopathological and morphological studies on natural Cysticercus fasciolaris infection in liver of Wistar rats. J. Parasit. Dis., 40: 255-258.
Mowat, V; Turton, J; Stewart, J; Lui, KC and Pilling, AM (2009). Histopathological features of Capillaria hepatica infection in laboratory rabbits. Toxicol. Pathol., 37: 661-666. doi: 10.1177/0192623309339501.
Okoye, CI and Obiezue, RNN (2008). A survey of the gut parasites of rodents in Nsukka ecological zone. Anim. Res. Int., 5: 846-847. doi: 10.4314/ari.v5i2.48744.
Paramasvaran, S; Sani, RA; Hassan, L; Hanjeet, K; Krishnasamy, M; John, J; Santhana, R; Sumarni, MG and Lim, KH (2009). Endo-parasite fauna of rodents caught in five wet markets in Kuala Lumpur and its potential zoonoticimplications. Trop. Biomed., 26: 67-72.
Reperant, LA and Deplazes, P (2005). Cluster of Capillaria hepatica infections in non-commensal rodents from the canton of Geneva, Switzerland. Parasitol. Res., 96: 340-342. doi: 10.1007/s00436-005-1358-y.
Resendes, AR; Amaral, AF; Rodrigues, A and Almeria, S (2009). Prevalence of Calodium hepaticum (syn. Capillaria hepatica) in house mice (Mus musculus) in the Azores archipelago. Vet. Parasitol., 160: 340-343. doi: 10.1016/j. vetpar.2008.11.001.
Rocha, EJ; BasanoSde, A; Souza, MM; Honda, ER; Castro, MB; Colodel, EM; Silva, JC; Barros, LP; Rodrigues, ES and Camargo, LM (2015). Study of the prevalence of Capillaria hepatica in humans and rodents in an urban area of the city of Porto Velho, Rondônia, Brazil. Rev. Inst. Med. Trop. Sao Paulo. 57: 39-46. doi: 10.1590/S0036-46652015000100006.
Singh, YD and Arya, RS (2015). Clinico-pathology, diagnosis and management of Cysticercus fasciolaris and Hymenolepis diminuta co-infection in wistar rats. Vet. World. 8: 116-120. doi: 10.14202/vetworld.2015.116-120.
Singla, LD; Aulakh, GS; Sharma, R; Juyal, PD and Singh, J (2009). Concurrent infection of Taenia taeniaeformis and Isospora felis in a stray kitten: a case report. Vet. Med., 54: 81-83.
Singla, N; Dhar, P; Singla, LD and Gupta, K (2016). Patho-physiological observations in natural concurrent infections of helminth parasites of zoonotic importance in the wild rodents, Bandicota bengalensis. J. Parasit. Dis., 40: 1435-1442. doi: 10.1007/s12639-015-0709-6.
Singla, LD and Singla, N (2019). Transmission potential of parasitic diseases by rodents to animals and humans. In: Tripathi, RS and Chaudhary, V (Eds.), Compendium of model training course on management of vertebrate pests in drylands for enhancing farmers income. Central Arid Zone Research Institute, Jodhpur. PP: 161-174.
Singla, N; Singla, LD; Gupta, K and Sood, NK (2013). Pathological alterations in natural cases of Capillaria hepatica infection alone and in concurrence with Cysticercus fasciolaris in Bandicota bengalensis. J. Parasit. Dis., 37: 16-20. doi: 10.1007/s12639-012-0121-4.
Singla, N; Singla, LD and Kaur, R (2008a). Rodents as museum of helminth parasites of public health importance in Punjab, India. Int. J. Infect. Dis., 12: 381-382. doi: 10.1016/j.ijid.2008.05.1007.
Singla, LD; Singla, N; Parshad, VR; Sandhu, B and Singh, J (2003). Occurrence and pathomorphological observations on Cysticercus fasciolaris in bandicoot rats in India. In: Singleton, GR; Hinds, LA; Krebs, CJ and Spratt, DM (Eds.), Rats, mice and people: rodent biology and management. Australian Centre of International
Agricultural Research, Canberra, Monograph No. 96, PP: 57-59.
Spratt, DM and Singleton, GR (2001). Hepatic capillariasis. In: Davis, JW; Samuel, WM; Pybus, MJ and Alan Kocan, A (Eds.), Parasitic diseases of wild animals. (2nd Edn.), Ames, Iowa State University Press. PP: 365-379.
Sterba, J; Blazek, K and Barus, V (1977). Contribution to the pathology of strobilocercosis (Strobilocercus fasciolaris) in the liver of man and some animals. Folia. Parasit., 24: 41-46.
Stojcevic, D; Mihaljevic, Z and Marinculic, A (2004). Parasitological survey of rats in rural regions of Croatia. Vet. Med. Czech., 49: 70-74. doi: 10.17221/5679-VETMED.
Tijjani, M; Majida, RA; Abdullahia, SA and Unyaha, NZ (2020). Detection of rodent-borne parasitic pathogens of wild rats in Serdang, Selangor, Malaysia: A potential threat to human health. Int. J. Parasitol. Parasite. Wildl., 11: 174-182. doi: 10.1016/j.ijppaw.2020.01.008.
Zamini, G; Khadem-Erfan, MB and Faridi, A (2017). Capillaria hepatica in Rattus spp. captured in Sanandaj and orally uninfected Balb/C mice with embryonated eggs. Int. J. Basic. Sci. Med., 2: 133-138. doi: 10.15171/ijbsm.2017. 25.