ABSTRACT

The island of Fernando de Noronha, belonging to the state of Pernambuco, Brazil, has several animal species introduced by man, such as the black rat (Rattus rattus) and the domestic cat (Felis catus), representing a risk to the ecological balance of the island and to the public health. This study aimed to report the occurrence of Strobilocercus fasciolaris in black rats (R. rattus) in this insular environment and to contribute with epidemiological data on this parasitosis. Rodents were captured using Tomahawk traps and sedated with an association of Ketamine Hydrochloride (40mg/kg/IM) and Xylazine Hydrochloride (2mg/kg/IM) for subsequent euthanasia and necroscopic evaluation. Of the 154 captured black rats, 54 (35.06%) had single or multiple cysts in the liver. The cysts were morphologically evaluated and the metacestodes were identified as Strobilocercus fasciolaris, the larval form of Hydatigera taeniformis. This is the first report of the occurrence of Strobilocercus fasciolaris in black rats (Rattus rattus) in an island environment in Brazil. The occurrence of this metacestode in rodents on the Island demonstrates the high environmental contamination, fast reproduction, and dispersion of this parasite, being a potential risk for the conservation of susceptible species and for public health.

Keywords:
exotic animals; rodents; Taenia taeniformis; Cysticercus fasciolaris; metacestodes

RESUMO

A Ilha de Fernando de Noronha, pertencente ao estado de Pernambuco, Brasil, possui diversas espécies animais introduzidas pelo homem, como o rato-preto (Rattus rattus) e o gato-doméstico (Felis catus), representando um risco ao equilíbrio ecológico da Ilha e à saúde pública. Objetivou-se relatar a ocorrência de Strobilocercus fasciolaris em ratos-pretos (R. rattus) nesse ambiente insular e contribuir com dados epidemiológicos sobre essa parasitose. Os roedores foram capturados utilizando-se armadilhas do tipo Tomahawk, sedados com uma associação de cloridrato de cetamina (40mg/kg/IM) e de cloridrato de xilazina (2mg/kg/IM) para posterior eutanásia e avaliação necroscópica. Dos 154 ratos-pretos capturados, 54 (35,06%) apresentavam cistos únicos ou múltiplos no fígado. Os cistos foram avaliados morfologicamente e os metacestódeos foram identificados como Strobilocercus fasciolaris, forma larval de Hydatigera taeniformis. Este é o primeiro relato da ocorrência de Strobilocercus fasciolaris em ratos-pretos (Rattus rattus) em ambiente insular no Brasil. A ocorrência desse metacestodeo em roedores na Ilha demonstra a alta contaminação ambiental, a rápida reprodução e a dispersão desse parasito, sendo um potencial risco para a conservação das espécies suscetíveis e para a saúde pública.

Palavras-chave:
animais exóticos; roedores; Taenia taeniformis; Cysticercus fasciolaris; metacestoide

INTRODUCTION

The Fernando de Noronha Archipelago belongs to the state of Pernambuco, Northeast Brazil, being considered the top of an underwater mountain of volcanic origin, consisting of 21 islands and islets, the main and only inhabited being the Fernando de Noronha Island (Plano…, 1990).

In this Island, several animal species were introduced by man, such as the black rat (Rattus rattus), mice (Mus musculus) and the domestic cat (Felis catus), representing a risk to the ecological balance (Antas, 1991ANTAS, P.T.Z. Status and conservation of seabirds breeding in Brazilian waters. ICBP Techn. Public., v.11, p.141-158, 1991.). The presence of these and other invasive species plays an important role in the introduction and dissemination of different parasites (Crowl et al., 2008CROWL, T.A.; CRIST, T.O.; PARMENTER, R.R. et al. The spread of invasive species and infectious disease as drivers of ecosystem change. Front. Ecol. Environ., v.6, p.238-246, 2008.).

Several studies on the occurrence of parasites in animals on the Fernando de Noronha Island have already been reported, in particular on the occurrence of coccidian protozoa (Melo et al., 2020MELO, R.P.B.; ALMEIDA J.C.; LIMA D.C.V. et al. Atypical Toxoplasma gondii genotype from a sheep and a pigon Fernando de Noronha Island, Brazil, showed different mousevirulence profiles. Parasitol. Res., v.119, p.351-356. 2020.; Lima et al., 2019aLIMA, D.C.V.; MELO, R.P.B.; ANDRADE, M.R. et al. Low frequency of antibodies anti-Neospora caninum in rodents in Fernando de Noronha Island, Brazil. An. Acad. Bras. Ciênc., v.91, p.e20190439, 2019a.; Lima et al., 2019b; Lima et al., 2018, Silva et al., 2017SILVA, J.C.R.; FERREIRA, F.; DIAS R.A. et al. Cat-rodent Toxoplasma gondii Type Iivariant circulation and limited genetic diversity on the Island of Fernando de Noronha, Brazil. Parasit. Vectors, v.10, p.1-6, 2017.; Magalhães et al., 2016MAGALHÃES, F.J.R.; ANDRADE M.R.; ALCÂNTARA A.M. et al. Risk factors for Toxoplasma gondii infection in sheep and cattle from Fernando de Noronha Island, Brazil. Rev. Bras. Parasitol. Vet., v.25, p.511-515, 2016., Melo et al., 2016; Magalhães et al., 2017; Lima-Filho, 2015; Vitaliano et al., 2014VITALIANO, S.N.; SOARES, H.S.; MINERVINO, A.H.H. et al. Genetic characterization of Toxoplasma gondii from Brazilian wildlife revealed abundant new genotypes. Int. J. Parasitol. Parasites Wildl., v.3, p.276-283, 2014.; Costa et al., 2012COSTA, D.G.C.; MARVULO, M.F.V.; SILVA, J.S.A. et al. Seroprevalence of Toxoplasma gondii in domestic and wild animals from the Fernando de Noronha, Brazil. J. Parasitol., v.98, p.679-680, 2012.; Dubey et al., 2010DUBEY, J.P.; RAJENDRAN, C.; COSTA, D.G.C. et al. New Toxoplasma gondii genotypes isolated from free-range chickens from the Fernando de Noronha, Brazil: unexpected findings. J. Parasitol., v.96, p.709-712, 2010.). However, studies on the occurrence and dispersion of helminths are scarce in this island environment.

Strobilocercus fasciolaris (also known as Cysticercus fasciolaris) is termed as the larval stage of Hydatigera taeniaeformis (also known as Taenia taeniaeformis), a cestode (Order: Cyclophyllidea) of cosmopolitan distribution that develops in the small intestine with the release of proglottids in feces of domestic and wild felines, which are considered its definitive hosts (Stuti et al., 2012STUTI, V.; SWAID, A.; DEEPESH, S.; MIR, M. Parasitic ova and oocysts observed in in testinal contents of a leopard (Panthera pardus) - a case report. J. Vet. Parasitol., v.26, p.170-171, 2012.; Krone et al., 2008KRONE, O.; GUMINSKY, O.; MEINIG, H. et al. Endopar asite spectrum of wild cats (Felis silvestris Schreber, 1777) and domestic cats (Felis catus L.) from the Eifel, Pfalz region and Saarland, Germany. Eur. J. Wildli. Res., v.54, p.95-100, 2008.). Felines become infected by ingesting the liver of intermediate hosts containing the larval form of this parasite (Singla et al., 2009SINGLA, L.D.; AULAKH, G.S.; SHARMA, R. et al. Concurrent infection of Taenia taeniaeformis and Isospora felis in a stray kitten: a case report. Vet. Med., v.54, p.81-83. 2009.), being synanthropic rodents (R. norvegicus, R. rattus and M. musculus) the main intermediate hosts that become infected through the ingestion of embryonated eggs present in the environment (Sharma et al., 2017SHARMA, R.; TIWARI, K.; BIRMINGHAM, K. et al. Cysticercus fasciolaris in Brown Rats (Rattus norvegicus) in Grenada, West Indies. J. Parasitol. Res., v.2017, p.1723406, 2017.; Parkdel et al., 2013).

Hydatigera taeniaeformis is a parasite with zoonotic potential, considered to be accidental in humans, and its occurrence has been reported in several countries such as Argentina, Czech Republic, Denmark, Taiwan, and Sri Lanka (Oryan and Alidadi, 2015ORYAN, A.; ALIDADI, S. Public health concerns of Taenidae and their metacestodes. Trop. Med. Surg., v.3, p.e123, 2015.; Ekanayake et al., 1999EKANAYAKE, S.; WARNASURIYA, N.D.; SAMARAKOON, P.S. et al. An unusual ‘infection’ of a child in Sri Lanka, with Taenia taeniaeformis of the cat. Ann. Trop. Med. Parasitol., v.93, p.869-873, 1999.; Miyazaki, 1991MIYAZAKI, I. An illustrated book of Helminthic zoonoses. Tokio: International Medical Foundation of Japan, 1991. 503p.).

Reports of these and other helminths in free-living animals are still scarce in the scientific literature, especially regarding invasive species in island environments. In this sense, the objective was to report the occurrence of Strobilocercus fasciolaris in black rats (Rattus rattus) on Fernando de Noronha Island and contribute epidemiological data on this parasitosis.

MATERIAL AND METHODS

The project was approved by the Committee on Ethics in the Use of Animals - CEUA/UFRPE (License nº 101/2015) and by the Authorization and Information System on Biodiversity - SISBIO (License nº 49198-1).

The research was carried out on Fernando de Noronha Island, located in the Fernando de Noronha Archipelago (3° 50'25 S, 32° 24'38 W), PE, Brazil.

Tomahawk traps were used to capture rodents of the Rattus rattus species. The captured rats were subsequently sedated with a combination of Ketamine Hydrochloride (40mg/kg/IM) and Xylazine Hydrochloride (2mg/kg/IM). Then, the animals were euthanized by members of the Island's Rodent Control Program following the protocol described by Silva et al. (2017SILVA, J.C.R.; FERREIRA, F.; DIAS R.A. et al. Cat-rodent Toxoplasma gondii Type Iivariant circulation and limited genetic diversity on the Island of Fernando de Noronha, Brazil. Parasit. Vectors, v.10, p.1-6, 2017.) and the necropsy stage was performed.

The captured animals were submitted to euthanasia, necropsy, and collection of tissue samples. After euthanasia, a macroscopic examination of all organs in the abdominal and thoracic cavity of the animals was performed to observe possible changes. The cysticerci found during the necropsy of the rodents were removed and placed in containers containing 0.9% saline solution, refrigerated for the relaxation of their structures and subsequent morphological analysis and identification of the parasite. A small incision was made on the wall of each cyst to remove the metacestode (Bomfim, 2001BOMFIM, T.C.B. Some observations about natural infection in Rattus norvegicus for Cysticercus fasciolaris (Eucestoda: Taeniidae). Rev. Bras. Parasitol. Vet., v.10, p.79-82. 2001.).

RESULTS

154 rats of the Rattus rattus species were captured and the macroscopic evaluation of the livers showed the presence of one or multiple whitish-yellow cysts in 54 animals (35.06%), measuring between 2-8mm (Figure 1 - A, B and C). When cut, each cyst contained a small portion of whitish fluid that characterized the color of the parasitic structure in addition to a larva (Medina-Pinto et al., 2019). The metacestode of each cyst was evaluated macroscopically, observing a large scolex, with a long neck, a body with pseudo-segments and a rounded terminal portion (Zhang et al., 2012ZHANG, X.; ZHANG, J.; HUANG, H. et al. Taenia taeniaeformis in rat favors protracted skin lesions caused by Sporothrix schenckii infection: Dectin-1 and IL-17 are dispensable for clearance of this fungus. PLoS One, v.7, p.e52514, 2012.). Thus, it was possible to identify the structure as Strobilocercus fasciolaris, the larval form of Hydatigera taeniformis.

Besides the presence of cysts, no macroscopic lesions were observed in the hepatic parenchyma. In the evaluation of other organs and tissues, no noteworthy alterations were identified.

DISCUSSION

So far, this is the first report of the occurrence of Strobilocercus fasciolaris in black rats (Rattus rattus) in an island environment in Brazil.

Figure 1
Strobilocercus fasciolaris in black rat (Rattus rattus) livers. A: Presence of multiple cysts in the liver of a rodent (R. rattus). B: Presence of a cyst measuring about 0.7cm in the liver of a rodent (R. rattus). C: S. fasciolaris measuring about 6cm removed from the interior of a rodent liver cyst (R. rattus).

Fernando de Noronha Island is considered an environment with a high occurrence of domestic felines with feral habits (Felis silvestris catus), which leads to several ecological problems, due to predation and competition with the local fauna, in addition to the maintenance and dissemination of pathogenic agents (Lima et al., 2019bLIMA, D.C.V.; MELO, R.P.B.; ALMEIDA, J.C. et al. Toxoplasma gondii in invasive animals on the Island of Fernando de Noronhain Brazil: Molecular characterization and mouse virulence studies of newgenotypes. Comp. Immunol. Infect. Dis., v.67, p.101347, 2019b., Magalhães et al., 2017MAGALHÃES, F.J.R.; ANDRADE, M.R.; SOUZA, F.M. et al. Seroprevalence and spatial distribution of Toxoplasma gondii infection in cats, dogs, pigs and equines of the Fernando de Noronha Island, Brazil. Parasitol. Int., v.66, p.43-46, 2017., 2016). Rats and mice are considered the most common intermediate hosts of S. fasciolaris and are usually asymptomatic (Abuladze, 1970ABULADZE, K.I. Taeniata of animals and mandiseases caused by them. In: SKRJABIN, K.I. (Ed.). Essencials of cestodology, v.4. Jerusalem: Israel Program for Scientific Translation, 1970. 549p.). Although this parasite can cause liver changes such as chronic irritation, liver necrosis, inflammatory reactions, neoplasms (Mahesh et al., 2006MAHESH, K.J.; REDDY P.L.; APARNA V. et al. Strobilocercus fasciolaris infection with hepatic sarcoma and gastroenteropathy in a Wistar colony. Vet. Parasitol., v.141, p.362-367, 2006.) and sarcomas (Irizarry-Rovira et al., 2007), these findings were not evidenced in this study, corroborating with Hasanpour et al. (2017HASANPOUR, H.; NAJAFI, F.; GHARAGOZLOU, M.J. et al. Cysticercus fasciolaris (Taenia taeniaeformis Larval Stage) in urban rats with illustration of histopathological changes in the liver. J. Med. Microbiol. Infect. Dis., v.5,p.43-46, 2017.), who suggest that the absence of these findings may indicate an infection in the acute phase.

The presence of multiple S. fasciolaris cysts in the liver of rats has been previously described by Bomfim (2001BOMFIM, T.C.B. Some observations about natural infection in Rattus norvegicus for Cysticercus fasciolaris (Eucestoda: Taeniidae). Rev. Bras. Parasitol. Vet., v.10, p.79-82. 2001.) and the difference observed between the sizes of these structures may suggest a more recent or later infection (Hasanpour et al., 2017HASANPOUR, H.; NAJAFI, F.; GHARAGOZLOU, M.J. et al. Cysticercus fasciolaris (Taenia taeniaeformis Larval Stage) in urban rats with illustration of histopathological changes in the liver. J. Med. Microbiol. Infect. Dis., v.5,p.43-46, 2017.; Moudgil et al., 2016MOUDGIL, A.D.; DAS-SIGLA, L.; GUPTA, K. et al. Histopathological and morphological studies on natural Cysticercus fasciolaris infection in liver of Wistar rats. J. Parasit. Dis., v.40, p.255-258, 2016.).

According to Lee et al. (2016), cysts can be found in different organs and tissues. The presence of ectopic larvae can occur due to their migration through the central hepatic vein and may affect other organs such as the lung and kidneys, however, ectopic larvae do not find adequate conditions for survival outside the liver, leading to their degeneration. In addition, these authors also found a frequency of 33.8% (97/287) of positivity for S. fasciolaris among rodents of the Rattus norvegicus species with the presence of cysts in different organs besides the liver, which disagrees with what was observed in the present study.

The presence of S. fasciolaris has been described in free-living rodents by several authors. Zhao et al. (2020ZHAO, F.; ZHOU, Y.; WU, Y. et al. Prevalence and genetic characterization of two mitochondrial gene sequences of Strobilocercus Fasciolaris in the livers of brown rats (Rattus norvegicus) in Heilongjiang Province in Northeastern China. Front. Cell Infect., v.10, p.588107, 2020.) described a frequency of 11.8% (13/110) of positivity for this agent in free-ranging brown rats (R. norvegicus) in China. In other studies, Sinniah et al. (2014SINNIAH, B.; HASSAN A, K.R.; SABARIDAH, I. et al. Prevalence of intestinal parasitic infections among communities living in different habitats and its comparison with one hundred and one studies conducted over the past 42 years (1970 to 2013) in Malaysia. Trop. Biomed. v.31, p.190-206. 2014.) reported 39.3% positivity in free-living rodents of different species (R. norvegicus, R. rattus and M. musculus) in Malaysia. Sharma et al. (2017SHARMA, R.; TIWARI, K.; BIRMINGHAM, K. et al. Cysticercus fasciolaris in Brown Rats (Rattus norvegicus) in Grenada, West Indies. J. Parasitol. Res., v.2017, p.1723406, 2017.) described a high percentage of positivity (70.7%) for S. fasciolaris in R. norvegicus in India, where they attributed this value to the proximity of these rodents to urban areas, which can also be inferred in the present research.

In a rural area in Mexico, Medina-Pinto et al. (2019) described a low frequency of S. fasciolaris infection in R. Rattus in the peridomestic environment, with a percentage of 7.8% (12/153) and, for the captured free-living rodent species, the presence of cysts was not observed. These findings corroborate with those found by Rodriguez-Vivas et al. (2011) also in Mexico, where rodents of different species were evaluated and a low frequency of positivity among the analyzed species (7.5% - 31/411) were found. Of this total of positives animals, 3.5% were black rats of the species R. rattus; and in wild rodent species, no animal was positive. These results may infer that environmental contamination by feline feces is low in this environment when compared to the environment on the island studied, which is a risk factor to be considered.

A high frequency of S. fasciolaris in free-living rodents may be related to the age of the animals, since younger ones are more susceptible and, consequently, more frequently infected with this parasite (Medina-Pinto et al., 2019, Lee et al., 2016), in addition to being related to warmer periods of the year (summer, spring), when there are more hosts in the environment due to the reproductive season (Mcinnes et al., 2014MCINNES, E.; KOHN, H.; CARMICHAEL, I. et al. Larvae of Taenia Taeniaformis in the liver of a laboratory rat (Rattus norvegicus). Ann. Clin. Pathol., v.2, p.1028, 2014.).

Sinniah et al. (2014SINNIAH, B.; HASSAN A, K.R.; SABARIDAH, I. et al. Prevalence of intestinal parasitic infections among communities living in different habitats and its comparison with one hundred and one studies conducted over the past 42 years (1970 to 2013) in Malaysia. Trop. Biomed. v.31, p.190-206. 2014.) add that the presence of many rodents and, consequently, a higher frequency of S. fasciolaris, is greater in environments with a tropical climate and places with less basic sanitation and public health policies, such as the inefficiency in combating synanthropic rodents.

Contamination of the environment by H. taeniformis eggs is reported not only in natural environments, but also in laboratory environments such as rodent breeding facilities, where parasite transmission can occur through contamination of wood shavings and/or water and food by infected felines feces (Singh and Arya, 2015; Oliveira et al., 2014OLIVEIRA, C.B.; FERRONATO, J.A.; GIACOMETI, M. et al. Presença de Cysticercus fasciolaris em Ratos do Biotério da Universidade do Oeste de Santa Catarina (Unoesc) de Xanxerê. In: CONGRESSO REGIONAL DE MEDICINA VETERINÁRIA, 2., 2014, Joaçaba. Anais... Joaçaba: Unoesc, 2014. 29p.; Mcinnes et al., 2014MCINNES, E.; KOHN, H.; CARMICHAEL, I. et al. Larvae of Taenia Taeniaformis in the liver of a laboratory rat (Rattus norvegicus). Ann. Clin. Pathol., v.2, p.1028, 2014.). Although S. fasciolaris infection is considered asymptomatic in most cases, in vivarium animals there is a greater susceptibility and a more severe clinical picture, with a high parasite load (Singh and Arya, 2015).

The high frequency of S. fasciolaris in rodents on Fernando de Noronha Island demonstrates an important environmental contamination and rapid reproduction and dispersion of parasitic agents in this environment. The permanence of invasive animals on the Island represents a high risk not only to the conservation of endemic species but has a harmful effect on public health in the maintenance of pathogens in the environment, and measures for the prevention and control of rodents and other exotic species should be encouraged in this island environment.

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History