ROLE OF RATS IN TRANSMISSION OF SOME HELMINTHS IN BENI-SUEF GOVERNORATE

Document Type : Research article

Author

Animal Health Institute, Beni-Suef Branch.

Abstract

 
The population distribution and zoonotic potential of gastrointestinal helminths in naturally infected population of rats (Rattus rattus and Rattus frugivorus) in Beni-Suef are studied. One hundred and twenty rats were investigated, 30.00 % of R. rattus and 28.57 % of R. frugivorus were found infected by helminths. These helminths were 3 cestodes; Hymenolepis nana, Hymenolepis diminuta and Strobilocercus fasciolaris larva; 2 nematodes; Syphacia obvelata and Nippostrongylus braseliensis from both species of rats. The most prevalent helminth was Nippostrongylus braseliensis in rats. Experimental infection of free cats by larvae of Strobilocercus fasciolaris to obtain adult worms of Taenia taeniaeformis was done. The study revealed that rats act as reservoir of infection for human by Hymenolepis nana and H. diminuta and for cats by Taenia taeniaeformis

Keywords


Animal Health Institute, Beni-Suef Branch.

 

Role of rats in transmission of some helminths in Beni-Suef Governorate

(With 4 Tables and 4 Figures)

 

By

L.S. Hussien

(Received at 3/12/2008)

 

دور الجرذان فى نقل بعض الديدان فى محافظة بنى سويف

 

حسين سيد لطفى

 

لکثرة انتشارالجرذان فى أماکن التجمعات البشرية فان هذه الدراسة تلقى الضوء على الديدان التى تصيب الجرذان فى محافظة بنى سويف . تم فحص 120 جرذا حيث وجد ان 30 % من الجرذان من نوع راتس راتس و (28.57 %) من نوع راتس فراجيفورس مصابة بانواع مختلفة من الديدان. هذه الديدان هى 3 ديدان شريطية هى: هيمينوليبس نانا وهيمينوليبس دايمنيوتا ويرقات الاستروبيلوسرکس فاشيولاريس. وديدان اسطوانية هى سيفشيا اوبفيلاتا ونيبوستروجيلس برازيلينسس. وجد ان دودة نيبوسترونجيلس برازيلينسس هى الاکثر انتشارا فى الجرذان. وللتعرف على الطور البالغ ليرقة الاستروبيلوسرکس فاشيولاريس تم اجراء عدوى تجريبية فى القطط وتم الحصول على الاطوار البالغة لديدان التنيا تينيفورمس. من هذه الدراسة وجد ان الجرذان تعمل کعوائل خازنة لديدان هيمينوليبس نانا وهيمينوليبس دايمنيوتا والتى يمکن ان تنتقل الى الانسان وکذالک هى عوائل وسيطة لديدان التنيا تنيفورمس والتى تصيب القطط.

 

SUMMARY

 

The population distribution and zoonotic potential of gastrointestinal helminths in naturally infected population of rats (Rattus rattus and Rattus frugivorus) in Beni-Suef are studied. One hundred and twenty rats were investigated, 30.00 % of R. rattus and 28.57 % of R. frugivorus were found infected by helminths. These helminths were 3 cestodes; Hymenolepis nana, Hymenolepis diminuta and Strobilocercus fasciolaris larva; 2 nematodes; Syphacia obvelata and Nippostrongylus braseliensis from both species of rats. The most prevalent helminth was Nippostrongylus braseliensis in rats. Experimental infection of free cats by larvae of Strobilocercus fasciolaris to obtain adult worms of Taenia taeniaeformis was done. The study revealed that rats act as reservoir of infection for human by Hymenolepis nana and H. diminuta and for cats by Taenia taeniaeformis.

 

Key words: Rats, helminthes, cestodes, nematodes

Introduction

 

Rats carry several zoonotic pathogens and because rats and humans live in close proximity in urban environments, there exists potential risk for transmission (Easterbrook et al., 2007). It is important to survey the parasites of rats for understanding the source of the zoonotic infections, because rats can be natural reservoir of serious zoonotic parasitic infections (Seong et al., 1995).   

Many helminths were reported from rats as; Hymenolepis nana, Hymenolepis diminuta, Syphacia obvelata, Nippostrongylus brasiliensis and Strobilocercus  fasciolaris (Mafiana et al., 1997; Namue and Wongsawad, 1997; Abdel-Wahed et al., 1999; Ito and Itagaki, 2003; Syed-Arnez and  Mohd-Zain, 2006 and Waugh et al., 2006).

Rats are a reservoir of many parasitic diseases specially zoonotic helminths as Hymenolepis nana which is the common zoonotic disease in children and institutionalized groups (El-Ridi et al., 1987, Mohamed et al., 1987, Rauch, 1993 and Alvez et al., 2003). H. diminuta has been reported from various areas of the world (El-Ridi et al., 1987, Mohamed et al., 1987 and Ishih et al., 2003).

Rodents are intermediate hosts for Taenia taeniaeformis and become infected by ingestion of eggs of this worm where they develop as Strobilocercus fasciolaris or Cysticercus fasciolaris (Sohn and Chai, 2005 and Mahesh Kumar et al. (2006). Strobilocercus fasciolaris were found in the liver and peritoneum of muskrat especially in adult rats (Borqsteede et al., 2003).

This work aimed to detect the parasitic helminths in rats in Beni-Suef Governorate and which of these parasites could be infectious to other hosts specially human.

 

Materials and methods

 

1. Animals.

A total of 120 rats (50 Rattus rattus and 70 Rattus frugivorus) were collected between April 2008 and August 2008 from different localities in Beni-Suef Governorate, Egypt. These animals were captured alive by metal trap, then transferred to the Lab of the institute. The animals were identified according to Osborn and Helmy (1980). They were anesthetized by diethyl ether inhalation after that the vertebral column was dislocated. Then they were dissected and gastrointestinal tract, liver, lungs, kidneys, gonads, body cavity and subcutaneous tissues were examined for helminths infections using stereomicroscope.

2. Parasites.

Adult worms and/or larvae of different helminths were collected. Cestodes were flattened, fixed in 10% formalin and stained with acetocarmine (Pritchard & Kruse, 1982), while nematodes were fixed in 70% glycerol alcohol and mounted in glycerol jelly. Taxonomic identification of helminths was based on Yamaguti (1958).

2.1. Experimental infection of cats for identification of larvae: 

Faeces of 3 cats (Felis catus) were examined to ensure that they were free from parasitic helminthic infection especially Taenia species. They were fed on the part of livers of rats that contained the obtained cysts. Each cat was infected by 5 cysts. After 5 weeks post infection, faeces of cats were examined weekly for the presence of T. taeniaeformis eggs by using floatation technique (Soulsby, 1982). Cats were sacrificed at 55 days post infection and the intestine was examined for the presence of the adult worms. Adult worms were collected, counted and identified.  

 

Results

 

1. Incidence of infection among the examined rat species

 In this work, 120 rats were examined, 35 (29.16%) were found harboring helminths. 50 R. rattus were examined and the infection rate was 30% while on examination of 70 R. frugivorus, 28.57 % were infected (Table 1).

Regarding the helminths infection among rat species, cestode helminths were recorded at highest rates, 24% and 21.43% in R. rattus and R. frugivorus respectively. The nematode infection was 16% and 21.43% in R. rattus and R. frugivorus respectively (Table 2).

Table (3) illustrated the helminths in R. rattus: Nippostrongylus brasiliensis was the most common type of infection among the infected rats (20%), followed by Hymenolepis nana (16%), H. diminuta, (14%) Syphacia obvelata, (10%) and lowest infection rate was Strobilocercus fasciolaris 6%.

Table (4) showed the detected helminths; the highest helminth infection rate in R. frugivorus was by N. brasiliensis (21.43%). followed by H. diminuta (20%)

2. Identification of helminths and larvae.

            The helminths of the infected R. rattus were three cestodes;       H. nana, H. diminuta (Fig. 1) and Strobilocercus fasciolaris larva     (Fig. 2), two nematodes; Syphacia obvelata (Fig 3) and N.  brasiliensis (Fig. 4), while those in R. frugivorus were: three cestodes, H. nana,      H. diminuta and Strobilocercus fasciolaris and two nematodes; Syphacia obvelata and  N. brasiliensis.

3- Complete identification of obtained larva by the experimental infection of cat.

The obtained larva was Strobilocercus fasciolaris (Cysticercus fasciolaris), the cysts were found on the liver of both rats. It was white cyst located on the parietal surface of liver containing the larvae (0.5cm in diameter). When the cyst was ruptured the segmented white larvae appeared (5cm in length) in which the scolex was evaginated and connected to the bladder by a segmented strobila, resembling a small tapeworm and also was known as a strobilocercus. The scolex carries hooks in two rows as adult worm (Fig. 2).

A group of 3 cats each was infected with 5 cysts. After 48 days post infection eggs of Taenia taeniaeformis were detected in the faeces of all infected cats. All cats were sacrificed at one week post eggs detection in their faeces. The mean adult T. taeniaeformis was 3 + 1 in the infected cats. Adult T. taeniaeformis is about 50cm in length, has a scolex armed with hooks in two rows, mature segment contained bilobed ovary and numerous testes scattered in the segment and gravid segment had several lateral branches (5-8 branches)  (Fig. 2).

 

Table 1: Rate of infection among examined rat species.

 

Rat species/

Exam. No.

Infect. No.

% of infection

Rattus rattus

50

15

30.00

R. frugivorus

70

20

28.57

Total

120

35

29.16

 

Table 2: Incidence of infection with helminths in infected rat species.

 

              Rat spp.

Helminth

Rattus rattus (n=50)

R. frugivorus (n= 70)

Inf. No.

%

Inf. No.

%

Cestodes

12

24

15

21.43

Nematodes

8

16

15

21.43

 

Table 3: The helminth parasites in the examined R. rattus.

 

Helminths

Exam. No.

Inf. No.

Prevalence of infection (%)

Hymenolepis nana

50

8

16

H. diminuta

50

7

14

Strobilocercus fasciolaris

50

3

6

Syphacia obvelata

50

5

10

Nippostrongylus braziliensis

50

10

20

Table 4: The helminth parasites in the examined R. frugivorus

 

Helminths

Exam. No.

Inf. No.

Prevalence of infection (%)

Hymenolepis nana

70

10

14.29

H. diminuta

70

14

20

Strobilocercus fasciolaris

70

8

11.43

Syphacia obvelata

70

7

10

Nippostrongylus braziliensis

70

15

21.43

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

Fig. 1: (X10) A1. Scolex of H. diminutaB1. Scolex of H. nana

    A2. Mature segments of H. diminuta   B2. Mature segment of H. nana

     A3. Gravid segments of H. diminuta    B3. Gravid segment H. nana

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

Fig. 2: A. Whole larva of Strobilocercus fasciolaris

           B. Scolex of Adult Taenia taeniformis.

           C. Mature segment of Taenia taeniformis.      

           D. Gravid segment of Taenia taeniformis (X 4).

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

Fig. 3: A. Anterior end of Syphacia obvelata.

           B. Posterior end of S. obvelata (male). 

           C. Posterior end of S. obvelata (Female) (X 100).

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

Fig. 4: Nippostrongylus braziliensis(X 100)

          A- Anterior end   B- Female posterior en

 

Discussion

 

            Rats have an important role in transmission and dissemination of serious pathogens to man and animals (Shoukry et al, 1986). Also they are considered as reservoir hosts for many parasitic diseases (Morsy et al., 1982).

The data of the present study showed that 29.16% of the rats that collected from Beni-Suef Governorate, Egypt were infected with helminths also 30.00 % of R. rattus and 28.57 % of R. frugivorus were infected with helminths. These helminths are Hymenolepis nana, H. diminuta, Strobilocercus fasciolaris, S. obvelata and N. brazilinsis.

The most prevalent type of infection was cestodal worms 21.43% (Hymenolepis nana, H. diminuta and Strobilocercus fasciolaris). These species in the present study were similar to the results of other authors like; Samaha and Otify, 1991, Abdel Salam et al., 1994, El Shazly et al., 1994, Seong et al., 1995, Mafiana et al., 1997,Abdel Wahed et al., 1999 and Waugh et al., 2006.

Regarding the nematodes infection, N. braziliensis was the most common infection in the infected rats. The same result was reported by Uga et al. (1983); Udonsi (1989); Antolin et al. (2006) and Syed-Arnez and Mohd-Zain (2006).

S. obvelata (the pin worm of rodents) is widely distributed all over the world and its presence in this study goes parallel with other studies (Abel Salam et al., 1994; Mafiana et al., 1997; Shaheen et al., 1999; Syed-Arnez and Mohd-Zain 2006).

  The resulted adult cestode from the experimental infection was identified as Taenia taeniaeformis based on its typical taenoid hooks and structure of mature segments and branches of gravid segments. The adult worm was similar to that obtained by Williams and Shearer (1981) and Rossin et al. (2004). Also Mahesh Kumar et al. (2006) confirmed that the obtained tapeworm cysts from liver of Wistar rats in India as Strobilocercus fasciolaris by PCR linked mitochondrial DNA sequencing.

From this study, Hymenolepis nana was reported from both species of rats and this worm is a zoonotic parasite, so rats are considered as reservoir and maintaining hosts for spreading of the infection to man by this helminth. This was stated by many studies; Samaha and Otify (1991), Abdel-Salam et al. (1994) and Easterbrook et al. (2007).

H. diminuta was recorded from examined rats in this study. Many studies considered it as a zoonotic parasite, so rats act as reservoirs and source for human infection by that worm. This view was shown by many works; Samaha and Otify (1991), Abel Salam et al. (1994), El Shazly et al. (1994), Abd El-Wahed et al. (1999) and Waugh et al. (2006).

From this study it could be concluded that R. rattus and R. frugivorus were found infected by many helminths. Moreover the study recorded two parasites as a common zoonotic parasites for human; H. nana and H. diminuta. Also rats are source of infection for cats by Taenia taeniaeformis

 

References

 

Abdel-Salam, F.A.; Galal, A.A. and Ali, M.K. (1994): The role of rodents as a reservoir of zoonotic intestinal parasites at Sohag Governorate, Egypt. Assuit Vet. Med. J., 30(60):124-138.

Abd el-Wahed, M.M.; Salem, G.H. and El-Assaly, T.M. (1999): The role of wild rats as a reservoir of some internal parasites in Qalyobia Governorate. J. Egypt. Soc. Parasitol., 29(2): 495-503.

Alvez, J.R.; Macedo, H.W.; Ramos, A.N.; Ferreira, L.F.; Goncalves, M.L. and Araujo, A. (2003): Intestinal parasite infections in a semiarid area of Northeast Brazil: Preliminary findings differ from expected prevalence rates. Cad Saude Publica., 19 (2): 667-670.

Antolin, M.M.; Joshi, R.C.; Sebastian, L.S.; Marquez, L.V.; Duque, U.G. and Domingo, C.J.  (2006): Endo- and ectoparasites of the Philippine rice field rat, Rattus tanezumi Temminck, on PhilRice farms.  International-Rice-Research-Notes; 31(1): 26-27.

Borqsteede, F.H.; Tibben, J.H. and Vander Giessen, J.W. (2003): The muskrat (Ondatra zibethicusas) intermediate host of cestodes in the Netherlands. Vet. Parasitol., 117(1-2): 29-36.

Easterbrook, J.D.; Kaplan, J.B.; Vanasco, N.B.; Reeves, W.K.; Purcell, R.H.; Kosoy, M.Y.; Glass, G.E.; Watson, J. and Klein, S.L. (2007): A survey of zoonotic pathogens carried by Norway rats in Baltimore, Maryland, USA. Epidemiology and Infection, 135(7): 1192-1199

El-Ridi, A.M.S.; Ismail, M.M.; El-Gamal, R.L.R. and Abd El-Fattah, M.E.M. (1987): Helminthic infections in rodents in Sharkiyia Governorate. J. Egypt. Soc. Parasitol., 17(1): 281-288.

El Shazly, A.M.; Morsy, T.A.; El Kady, G.A.; Ragheb, D.A.; Handousa, A.E.; Ahmed, M.M.; Younis, T.A. and Habib, K.S. (1994): The helminthic parasites of rodents in Dakahlia Governorate, with reference to their Egyptian helminth fauna. J. Egypt. Soc. Parasitol., 24(2): 413-28.

Ishih, A.; Sekijima, T.; Asakawa, M.; Tenora, F. and Uchikawa, R. (2003): Hymenolepis pseudodiminuta Tenora et al. 1994 from Apodemus speciosus and H. diminuta: a comparison of experimental infections in rats. Parasitol. Res., 89(4): 297-301.

Ito, M. and Itagaki, T. (2003): Survey on wild rodents for endoparasites in Iwate Prefecture, Japan. J. Vet. Med. Sci., 65(10):1151-1153.

Mafiana, C.F.; Osho, M.B. and Sam-Wobo, S. (1997): Gastrointestinal helminth parasites of the black rat (Rattus rattus) in Abeokuta, southwest Nigeria. J. Helminth.; 71(3): 217-220

Mahesh-Kumar, J.; Reddy, P.L.; Aparna, V.; Srinivas, G.; Nagarajan, P.; Venkatesan, R.; Sreekumar, C. and Sesikaran, B. (2006): Strobilocercus fasciolaris infection with hepatic sarcoma and gastroenteropathy in a Wistar colony. Vet. Parasitol., 5;141(3-4):362-7.

Mohamed, S.E.; Tosson, A.M.; Mohamed, A.B.; Mohamed, A.S.; Arafa, A.S. and Salam, M.M. (1987): Rodents as reservoir of zoonotic intestinal helminthes in Suez Canal zone with the possible immunological changes. J. Egypt. Soc. Parasit., 17(1): 259-273. 

Morsy, T.A, Michael, S.A.; Bassili, W.R. and Saleh, M.S. (1982): Studies on rodents and their zoonotic parasites, particularly Leishmania, in Ismailiya Governorate, A.R. Egypt. J. Egypt. Soc. Parasitol., 12(2): 565-85.

Namue, C. and Wongsawad, C. (1997): A survey of helminth infection in rats (Rattus spp) from Chiang Mai Moat. Southeast Asian J. Trop. Med. Public Health., 28 Suppl 1:179-83

Osborn, D.J. and Helmy, J. (1980): The contemporary land mammals of Egypt. FieldMuseum, Natural History, USA.

Pritchard, M.H. and Kruse, G.O.W. (1982): The collection and preservation of animal parasites. Univ. of Nebraska, Lincoln and London.

Rauch, R. (1993): The biology of Echinococcus. In Compendium on Cystic Hydatid Disease with special reference to the Xinjiang Uygur Autonomous region, the people's Republic of China (Andersen, F. L., ed.), 27-56. provo: BrighamYoungUniversity Print Services.

Rossin, A.; Malizia, A.I. and Denegri, G.M. (2004): The role of the subterranean rodent Ctenomys talarum (Rodentia: Octodontidae) in the life cycle of T. taeniaeformis (Cestoda: Taeniidae) in urban environments. Vet. Parasitol., 10; 122(1): 27-33.

Samaha, H. and Otify, Y. (1991): Role of rodents as a reservoir of some enteric parasites. Assiut. Vet. Med. J., 34(48): 171-175.

Seong, J.K.; Huh, S.; Lee, J.S. and Oh, Y.S. (1995): Helminths in Rattus norvegicus captured in Chunchon, Korea. Kor. J. Parasitol., 33(3): 235-7.

Shaheen, S.I.; Sayed, G.; Hamza, I. and Abdel Rahman, S.M. (1999): Two new species and a new locality record of a zoonotic cestode (Mathevotaenia) among intestinal helminths of rats in Assiut. Assiut Vet. Med. J., 41(82): 43-62.

Shoukry, A.; Morsy, T.A.; Abu Hashish, T.A.; El Kady, G.A. (1986): Seasonal activities of two commensal rats and flea index in North Sinai Governorate, Egypt. J. Egypt. Soc. Parasitol., 16(2): 385-93.

Syed-Arnez, A.S.K and Mohd Zain, S.N. (2006): A study on wild rats and their endoparasite fauna from the EndauRompinNational Park, Johor.  Malay. J. Sci., 25(2): 19-39.

Sohn, W.M. and Chai, J.Y. (2005): Infection status with helminths in feral cats purchased from a market in Busan, Republic of Korea. Kor. J. Parasitol. 43(3): 93-100.

Soulsby, E.J.L. (1982): Helminths, Arthropodes and Protozoa of domestic Animals. 7th Ed. The English Language Book society and Baillers. Tindall school.

Udonsi, J.K.  (1989): Helminth parasites of wild populations of the black rat, Rattus rattus (L.), from urban, rural residential and other ecological areas of Nigeria.  Acta Parasitol. Pol., 34(2): 107-116

Uga, S.; Matsumura, T.; Araki, K.; Gondo, M.; Murata, K.; Kagei, N.  (1983): A survey of the parasitic helminths of wild rats at a zoo in HyogoPrefecture. Jap. J. Parasitol., 32(6): 597-600

Waugh, C.A.; Lindo, J.F.; Foronda, P.; Angeles-Santana, M.; Morales, J. and Robinson, R.D. (2006): Population distribution and zoonotic potential of gastrointestinal helminths of wild rats Rattus rattus and R. norvegicus from Jamaica. J. Parasitol., 92(5): 1014-8.

Williams, J.F. and Shearer, A.M. (1981): Longevity and productivity of Taenia taeniaeformis in cats. Am. J. Vet. Res., 42(12): 2182-3.

Yamaguti, S. (1958): Systema Heminthum. Vol. I, the digenetic trematodes of Vertebrates- Part I.

 

 

 

Abdel-Salam, F.A.; Galal, A.A. and Ali, M.K. (1994): The role of rodents as a reservoir of zoonotic intestinal parasites at Sohag Governorate, Egypt. Assuit Vet. Med. J., 30(60):124-138.
Abd el-Wahed, M.M.; Salem, G.H. and El-Assaly, T.M. (1999): The role of wild rats as a reservoir of some internal parasites in Qalyobia Governorate. J. Egypt. Soc. Parasitol., 29(2): 495-503.
Alvez, J.R.; Macedo, H.W.; Ramos, A.N.; Ferreira, L.F.; Goncalves, M.L. and Araujo, A. (2003): Intestinal parasite infections in a semiarid area of Northeast Brazil: Preliminary findings differ from expected prevalence rates. Cad Saude Publica., 19 (2): 667-670.
Antolin, M.M.; Joshi, R.C.; Sebastian, L.S.; Marquez, L.V.; Duque, U.G. and Domingo, C.J.  (2006): Endo- and ectoparasites of the Philippine rice field rat, Rattus tanezumi Temminck, on PhilRice farms.  International-Rice-Research-Notes; 31(1): 26-27.
Borqsteede, F.H.; Tibben, J.H. and Vander Giessen, J.W. (2003): The muskrat (Ondatra zibethicusas) intermediate host of cestodes in the Netherlands. Vet. Parasitol., 117(1-2): 29-36.
Easterbrook, J.D.; Kaplan, J.B.; Vanasco, N.B.; Reeves, W.K.; Purcell, R.H.; Kosoy, M.Y.; Glass, G.E.; Watson, J. and Klein, S.L. (2007): A survey of zoonotic pathogens carried by Norway rats in Baltimore, Maryland, USA. Epidemiology and Infection, 135(7): 1192-1199
El-Ridi, A.M.S.; Ismail, M.M.; El-Gamal, R.L.R. and Abd El-Fattah, M.E.M. (1987): Helminthic infections in rodents in Sharkiyia Governorate. J. Egypt. Soc. Parasitol., 17(1): 281-288.
El Shazly, A.M.; Morsy, T.A.; El Kady, G.A.; Ragheb, D.A.; Handousa, A.E.; Ahmed, M.M.; Younis, T.A. and Habib, K.S. (1994): The helminthic parasites of rodents in Dakahlia Governorate, with reference to their Egyptian helminth fauna. J. Egypt. Soc. Parasitol., 24(2): 413-28.
Ishih, A.; Sekijima, T.; Asakawa, M.; Tenora, F. and Uchikawa, R. (2003): Hymenolepis pseudodiminuta Tenora et al. 1994 from Apodemus speciosus and H. diminuta: a comparison of experimental infections in rats. Parasitol. Res., 89(4): 297-301.
Ito, M. and Itagaki, T. (2003): Survey on wild rodents for endoparasites in Iwate Prefecture, Japan. J. Vet. Med. Sci., 65(10):1151-1153.
Mafiana, C.F.; Osho, M.B. and Sam-Wobo, S. (1997): Gastrointestinal helminth parasites of the black rat (Rattus rattus) in Abeokuta, southwest Nigeria. J. Helminth.; 71(3): 217-220
Mahesh-Kumar, J.; Reddy, P.L.; Aparna, V.; Srinivas, G.; Nagarajan, P.; Venkatesan, R.; Sreekumar, C. and Sesikaran, B. (2006): Strobilocercus fasciolaris infection with hepatic sarcoma and gastroenteropathy in a Wistar colony. Vet. Parasitol., 5;141(3-4):362-7.
Mohamed, S.E.; Tosson, A.M.; Mohamed, A.B.; Mohamed, A.S.; Arafa, A.S. and Salam, M.M. (1987): Rodents as reservoir of zoonotic intestinal helminthes in Suez Canal zone with the possible immunological changes. J. Egypt. Soc. Parasit., 17(1): 259-273. 
Morsy, T.A, Michael, S.A.; Bassili, W.R. and Saleh, M.S. (1982): Studies on rodents and their zoonotic parasites, particularly Leishmania, in Ismailiya Governorate, A.R. Egypt. J. Egypt. Soc. Parasitol., 12(2): 565-85.
Namue, C. and Wongsawad, C. (1997): A survey of helminth infection in rats (Rattus spp) from Chiang Mai Moat. Southeast Asian J. Trop. Med. Public Health., 28 Suppl 1:179-83
Osborn, D.J. and Helmy, J. (1980): The contemporary land mammals of Egypt. FieldMuseum, Natural History, USA.
Pritchard, M.H. and Kruse, G.O.W. (1982): The collection and preservation of animal parasites. Univ. of Nebraska, Lincoln and London.
Rauch, R. (1993): The biology of Echinococcus. In Compendium on Cystic Hydatid Disease with special reference to the Xinjiang Uygur Autonomous region, the people's Republic of China (Andersen, F. L., ed.), 27-56. provo: BrighamYoungUniversity Print Services.
Rossin, A.; Malizia, A.I. and Denegri, G.M. (2004): The role of the subterranean rodent Ctenomys talarum (Rodentia: Octodontidae) in the life cycle of T. taeniaeformis (Cestoda: Taeniidae) in urban environments. Vet. Parasitol., 10; 122(1): 27-33.
Samaha, H. and Otify, Y. (1991): Role of rodents as a reservoir of some enteric parasites. Assiut. Vet. Med. J., 34(48): 171-175.
Seong, J.K.; Huh, S.; Lee, J.S. and Oh, Y.S. (1995): Helminths in Rattus norvegicus captured in Chunchon, Korea. Kor. J. Parasitol., 33(3): 235-7.
Shaheen, S.I.; Sayed, G.; Hamza, I. and Abdel Rahman, S.M. (1999): Two new species and a new locality record of a zoonotic cestode (Mathevotaenia) among intestinal helminths of rats in Assiut. Assiut Vet. Med. J., 41(82): 43-62.
Shoukry, A.; Morsy, T.A.; Abu Hashish, T.A.; El Kady, G.A. (1986): Seasonal activities of two commensal rats and flea index in North Sinai Governorate, Egypt. J. Egypt. Soc. Parasitol., 16(2): 385-93.
Syed-Arnez, A.S.K and Mohd Zain, S.N. (2006): A study on wild rats and their endoparasite fauna from the EndauRompinNational Park, Johor.  Malay. J. Sci., 25(2): 19-39.
Sohn, W.M. and Chai, J.Y. (2005): Infection status with helminths in feral cats purchased from a market in Busan, Republic of Korea. Kor. J. Parasitol. 43(3): 93-100.
Soulsby, E.J.L. (1982): Helminths, Arthropodes and Protozoa of domestic Animals. 7th Ed. The English Language Book society and Baillers. Tindall school.
Udonsi, J.K.  (1989): Helminth parasites of wild populations of the black rat, Rattus rattus (L.), from urban, rural residential and other ecological areas of Nigeria.  Acta Parasitol. Pol., 34(2): 107-116
Uga, S.; Matsumura, T.; Araki, K.; Gondo, M.; Murata, K.; Kagei, N.  (1983): A survey of the parasitic helminths of wild rats at a zoo in HyogoPrefecture. Jap. J. Parasitol., 32(6): 597-600
Waugh, C.A.; Lindo, J.F.; Foronda, P.; Angeles-Santana, M.; Morales, J. and Robinson, R.D. (2006): Population distribution and zoonotic potential of gastrointestinal helminths of wild rats Rattus rattus and R. norvegicus from Jamaica. J. Parasitol., 92(5): 1014-8.
Williams, J.F. and Shearer, A.M. (1981): Longevity and productivity of Taenia taeniaeformis in cats. Am. J. Vet. Res., 42(12): 2182-3.
Yamaguti, S. (1958): Systema Heminthum. Vol. I, the digenetic trematodes of Vertebrates- Part I.