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Intestinal Parasites in Wild Rats

Introduction

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Mauritius is a small island of 1865 km2 situated 900 km east of the Malagasy Republic in the southern Indian Ocean. The island was found to be suitable as a port of call for traders travelling along the famous Spice Route from Europe round the Cape of Good Hope to the East Indies and was named East India trade route. The Dutch introduced sugarcane, orange trees, mango trees, rice and tobacco during their stay in Mauritius. They also brought deer from Java, rabbits, sheep, chickens and ducks. (http://mauritius.genosy.com)

The island has been much altered under various colonial powers. The Dutch, French and British cleared the dense forests that covered the island leaving very few areas of intact forest which are found in the highland and in the south-west and these have been invaded by exotic species such as wild plants and various introduced species (e.g. black rats and pigs). (John A. N. Parnell et al., 1989; http:// know-britain.com) Black rats were introduced in Mauritius probably by the Europeans in the 15th century when they were visiting the island. These rats were found in their vessels and they escaped and invaded the forests. (http://books.google.mu)

Plague was introduced in Mauritius by rats which were in Indian vessels trading with the island. The first case of genuine plague in Mauritius was discovered in Port-Louis and was confirmed by blood analysis. The victim died 24 hours after having been attacked. In February 1899 an outbreak of bubonic plague was reported in Port-Louis. This affected badly the island as the victims’ houses were burnt, affected people were sent to the segregated ranches outside of town. Suspects were put in quarantine in the suburbs of Port-Louis. This had a very bad effect on the economy and the local inhabitants. (John C. Campbell., 1899)

Recently in Mauritius, two employees of the airport of Plaisance died on 17 July 2013 and 14 August 2013 of leptospirosis. Another patient suspected of having contracted leptospirosis was admitted to a hospital in Mahebourg. The latter was working in a security company at Plaisance airport.These cases have aroused as the airport was under construction, forcing the wild rats to leave their natural habitats and live in proximity to humans. The three patients exhibited the same symptoms namely, muscle aches, vomiting and high fever.(http://en.indian-ocean-times.com)

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Types of rats

Rats are highly opportunistic, prolific, mobile, troublesome and damaging rodents that have capitalized on human movements to conquer most continents and a variety of habitats. They are considered as pests in many countries as they destroy crops, eat and contaminate food, damage structures and properties, disturb the ecological cycle and transmit diseases and parasites to other animals and humans. (Andrea Paparini et al., 2012; R. M. Timm et al., 2011)

There are two main rat speciesworldwide and these are:

  1. Rattus norvegicus, also known as the Norway or brown rat.
  2. Rattus rattus, also known asthe roof or black rat.( http://pestcontrol)
Classification
  Norway rats Black rats
Kingdom Animalia Animalia
Phylum Chordata Chordata
Subphylum Vertebrata Vertebrata
Class Mammalia Mammalia
Order Rodentia Rodentia
Family Muridae Muridae
Genus Rattus Rattus
Species Rattus norvegicus Rattus rattus

Table 1.1: Classification of the Norway and Black rats (http://biologycorner.com)

Characteristics Norway rats Black rats
General appearance Large and robust Sleek and agile
Color Grey Grey to white
Weight 198 – 510 grams 141 – 283 grams
Tail Shorter than body Longer than their heads and bodies combined
Head Blunt muzzle Pointed muzzle
Ears Small Long enough to reach eyes if folded over
Habitat They usually live in the basement or ground floor of buildings, in moist areas especially in gardens and fields, for example in sugarcane fields and near rivulets, and beneath rubbish or woodpiles. Their nests are found above the ground in shrubs, trees and dense vegetation. They can be found in enclosed or elevated spaces in buildings. They prefer ocean-influenced, warmer climates.
Picture Norway rat. Adult roof rat.

Table 1.2: Characteristics of Norway and Black rats (R. M. Timm et al., 2011; http://ipm.ucdavis.edu)

Rats as disease carriers

Rats are rodents that spread diseases to humans and animals as they act as reservoir hosts for many zoonotic pathogens. (Siti Shafiyyah et al., 2012; Jesse Adams) They transmit a number of zoonoses as they harbor and disseminate the pathogens involved, either through their biological materials or via their ectoparasites. (Antoniou M et al., 2010) Some of the diseases transmitted by rats to humans and other animals are rabies, leptospirosis, murine typhus, spotted fever, lassa fever, polio, meningitis, trichinosis, rat-bite fever, salmonellosis, plague, and toxoplasmosis. (http://cowleys)

Helminthes

Helminthes are worm-like parasites characterized by elongated, flat or round bodies. They are also known as triploblastic metazoans. They fall under two main phyla: Platyhelminthes and Nemathelminthes. Platyhelminthes comprise the classes Cestoda (tapeworms) and Trematoda (flukes) whereas Nemathelminthes comprise the class Nematoda (roundworms). Helminths involved in the intestines of rats are cestodes and nematodes.

Helminthes classification
Kingdom Animalia
Phylum Platyhelminthes Nemathelminthes
Class Cestoda Nematoda
Order Pseudophyllidea Cyclophyllidea

Caryophyllidea

Diphyllidea

Rhabditida

Trichinellida

Dioctophymatida

Muspiceida

Mermithidia

Table 1.3: Brief phylogenic classification of helminthes (FEG Cox, 1982, 1983)

The full classification of cestodes and nematodes can be found in the appendix.  

  Cestodes Nematodes
Shape
  • Ribbon-like.
  • Segmented.
  • Elongated.
  • Cylindrical.
  • Unsegmented.
Sexes
  • Not separate (monoecious/ hermaphrodite).
  • Separate (dioecious).
“Head” End
  • Suckers are present.
  • Scolex with hooks and rostellum.
  • No suckers and no hooks.
  • Well developed buccal cavity armed with teeth or cutting plates.
Alimentary

canal

  • Absent.
  • Absorption by microvilli on the cuticle’s surface.
  • Present and complete.
Body cavity
  • Absent.
  • Present.

Table 1.4: Characteristics of helminthes. (Dawit Assafa et al., 2004)

Chapter Two

Literature Review

Little is known concerning the intestinal parasites living in the locally available wild rats. The prevalence of parasites among wild rats (Rattus norvegicus and Rattus rattus) throughout the world is well documented. A study conducted by Tung et al. (2009) showed that 93.7% parasites prevailed on 95 rodents from different localities in Taiwan. Nippostrongylus braziliensis and Hymenolepis diminuta were the main endoparasites detected in a study done by Easterbrook et al. (2008) in 162 rats in Baltimore, Maryland, USA. In 2008, Elshazly et al. found that the commonest cestode was H. diminuta and the commonest nematode was Capillaria hepatica in rodents in Egypt. 999 feral rats were examined by Singh and Chee-Hock in 1971 and 450 were positive for nematode parasites. Capillaria hepatica was reported in wild rodents collected from different states in peninsular Malaysia by Liat et al. in 1977. From 151 house rats, Rattus rattus diardii collected from five different localities, examined in Kuala Lumpur, Leong et al. (1979) recovered nineteen species of parasites, H. diminuta and N. brasiliensis being the predominant species. (Siti Shafiyyah et al., 2012)

In a study conducted on 41 Norway and Black rats collected from two regions of Gaza, the prevalence ofintestinalparasites was 58.5%, consisting of Strongyloides eggs, G. lamblia, Hymenolepis diminuta, E. histolytica/dispar, Syphacia obvelata, Isospora, Acanthocephala and Heligmonoides josephi. (Al Hindi AI,Abu-Haddaf E., 2013)

In a surveillance programme conducted in625 wildrodents in 51 different areas of Cyprus, 92 animals were detected with Cysticercus fasciolaris, Hymenolepis diminuta, and Physalloptera spp. 12 different Salmonella spp. and serotypes were also detected in the intestine of 56rats.(Antoniou M et al., 2010)

Two species of cestodes (H. nana, H. diminuta), two genera (Raillietina species I, Raillietina species II) and one unidentified Hymenolepididae and the nematodes Streptopharagus species and Monanema nilotica were demonstrated on 220 Nilerats caughtin different regions of Sudan during the period January 2003-January 2006. (Fagir DM,El-Rayah el-A., 2009)

Rats and mice are known to be carriers of at least 35 diseases. They transmit swine and poultry diseases which also affect humans. The following are reservoirs of rodents:

  • Bacterial zoonoses such as leptospirosis, salmonellosis, salmonella typhimurium, tularaemina, yersiniosis, rat-bite fever plague, meliodosis and lyme disease.
  • Rickettsial zoonoses such as Siberian tick typhus, rickettsial pox and flea-borne typhus.
  • Viral zoonoses such as Argentinian haemorrhagic fever, Venezuelan equine encephalitus, lymphocytic choriomeningitis, haemorrhagic fever with renal syndrome and lassa fever.
  • Parasitic zoonoses such as echinococcossis due to E. multilocularis, leishmaniasis, schistosomiasis, angio strongyliasis, toxoplasmosis and Trichinelliosis.
  • Mycotic zoonoses such as histoplasmosis. (Jesse Adams)

So far there is no record available on these intestinal helminths and the other organisms in wild rats in Mauritius.

Dog ownership, dog behaviour and transmission ofEchinococcusspp. in the Alay Valley, southern Kyrgyzstan

Bioinformatic prediction of epitopes in the Emy162 antigen ofEchinococcus multilocularis

Cestodes (Tapeworms)

Characteristics of Cestodes
Shape Tapeworms are flattened, elongated organisms, and consist of segments called proglottids. They are usually 2 to 3 mm long and may reach up to 10 m. They may have three to several thousand proglottids.
Sexes Cestodes are hermaphroditic. Pseudophyllidean tapeworms’ eggs exit through a uterine pore found in the center of the ventral surface. The female system of cyclophyllidean tapeworms includes a uterus without a uterine pore.

Figure 2(a): Structure of tapeworms. (http://pathobio.sdu.edu.cn)

Head –end Cestodes possess a scolex bearing the organs of attachment, a neck which is the region of segment proliferation, and a strobila which is a chain of proglottids. Elongation of the strobila occurs when new proglottids add in the neck region. The immature segments are nearest to the neck and the sex organs are not fully developed. The more posterior segments are mature. The terminal segments are termed gravid as the uterus is egg-filled.

The scolex contains the brain or cephalic ganglion. Externally, the scolex consists of a bothria, rostellum or acetabula. A rostellum is a retractable, cone-like structure found on the anterior end of the scolex and it may be hooked. Bothria are long and narrow with weakly muscular grooves that are present in pseudophyllidean tapeworms. Acetabula are characteristic of cyclophyllideans.

Alimentary canal Adult tapeworms do not have an alimentary canal. Substances enter the tapeworm across the tegument which possesses numerous microvilli.
Body cavity A body cavity is absent.
Eggs Pseudophyllidean tapeworms’ eggs are operculated, whereas those of cyclophyllideans are not. All tapeworm eggs contain an oncosphere. That of pseudophyllidean tapeworms is called a coracidium as it is ciliated externally. The eggs of cyclophyllideans are released only when gravid proglottids are shed into the intestine. Some proglottids disintegrate to release eggs that are voided in the feces whereas other proglottids are passed intact.
Life cycle The egg develops into a procercoid stage in its first immediate host and in its next intermediate host it develops into a plerocercoid larva. It becomes an adult worm in the definitive host. Depending on the species, the oncosphere of cyclophyllidean tapeworms develops into a cysticercus larva, cysticercoid larva, coenurus larva, or hydatid cyst in specific intermediate hosts and finally become adults in the definitive host.

Figure 2(b): Generalized life cycle of tapeworms. (http://skola.okuladocs)

Table 2.5: Characteristics of Cestodes (Gilbert A. Castro: http://ncbi.nlm.nih.gov)

Nematodes (Roundworms)

Characteristics of Nematodes
Shape Nematodes are cylindrical organisms. The body wall consists of an outer cuticle which may have longitudinal ridges called alae.
Sexes Nematodes are usually bisexual. Males are smaller than females. They have a curved posterior end, and some species possess copulatory structures, such as spicules or a bursa, or both. The males possess one or two testes that lead into a seminal vesicle and eventually into the cloaca. The female system is made up of reflexed ovaries where each ovary is continuous, with an oviduct and uterus. The uteri join to form the vagina that opens to the exterior through the vulva.

During copulation, sperm is transferred into the vulva of the female and it enters the ovum. The zygote secretes a fertilization membrane which gradually thickens to form the chitinous shell.

Figure 3(a): Structure of nematodes. (A) Female. (B) Male. (http://pathobio.sdu.edu.cn)

Head –end They possess neither suckers nor hooks. The buccal cavity may be absent or minuteto spaciousthat may be armed with teethor jaws.
Alimentary canal The alimentary canal is complete, with both mouth and anus. The lips bear bristles which are sensory papillae. The esophagus has a different shape in different species. The intestine is composed of a layer of columnar cells with microvilli on their luminal surface.
Body cavity The body cavity, pseudocoelom, is enclosed by a body wall containing longitudinally-arranged muscles It contains the flattened gut and various reproductive organs.
Eggs Below the shell is a second membrane that acts as a selective barrier so that the egg is impervious to all substances except oxygen and carbon dioxide. A third proteinaceous membrane is secreted in some species as the egg passes down the uterus and is deposited outside the shell.
Life cycle Females lay eggs that are passed into the external environment. They undergo three developmental stages, L1, L2, and L3, before the nematode is again infective to another host. A first stage larva develops inside the egg which hatches. The hatching process is controlled by several factors such as temperature and moisture levels of the environment which stimulate the enclosed larvae to hatch by secreting enzymes to digest the egg membranes, and exerting pressure against the weakened membranes to rupture them and escape. The newly hatched L1 feeds on bacteria and grows. The molting process allows further growth of the larva. During each life cycle nematodes molt four times, each occurring at the end of every larval stage. Moulting separates the first and second larval stages (L1 and L2), the second and third larval stages (L2 and L3), the third and fourth larval stages (L3 and L4) and the fourth larval stages and immature adults (L4 and L5). The L5 grows to the limit of its new cuticle and develops into a sexually mature adult.

Figure 3(b): Generalized life cycle of intestinal nematodes. (http://pathobio.sdu.edu.cn)

Table 2.7: Characteristics of Nematodes (Gilbert A. Castro: http://ncbi.nlm.nih.gov; http://cal.vet.upenn.edu; http://pml-nematode.org.uk; http://userwww.sfsu.edu)

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