Gastrointestinal nematodes in dogs from Debre Zeit, Ethiopia

Veterinary Parasitology 148 (2007) 144–148 www.elsevier.com/locate/vetpar

Gastrointestinal nematodes in dogs from Debre Zeit, Ethiopia H.T. Yacob, T. Ayele, R. Fikru, A.K. Basu * Department of Pathology and Parasitology, Faculty of Veterinary Medicine, Addis Ababa University, PO Box 34, Debre Zeit, Ethiopia Received 7 March 2007; received in revised form 28 May 2007; accepted 3 June 2007

Abstract The study was conducted during the period between January 2005 and June 2006 to determine the frequency of gastrointestinal (GI) nematode infections of dogs in and around Debre Zeit, using qualitative and quantitative coprological (N = 100) and postmortem examinations (N = 20). By coproscopy 51% dogs were positive for different types of nematodal eggs, out of which 23.5% were with mixed infections. On necropsy 95% animals were found positive for adult parasites, of which 31.6% were showing more than one species of adult nematodes. The coproscopical examination revealed 32% infection with Ancylostoma caninum followed by Toxocara canis (21%), Spirocerca lupi (7%) and Trichuris vulpis (3%), while postmortem examination showed 70, 45, 23.5 and 5% infection, respectively. The study further indicated significant difference (P < 0.05) in overall frequency of GI nematode infections among different age groups but no difference (P > 0.05) between sexes. # 2007 Elsevier B.V. All rights reserved. Keywords: Coproscopy; Debre Zeit; Mixed infection; Nematodes; Frequency

1. Introduction Many families in Ethiopia keep one or more dogs either as hunting or guard dogs, or pets. However, there is no comprehensive work available that describes the population size, breeds, management systems, health conditions and public awareness, as to the needs and care of such important animals. A large number of dogs are commonly seen at abattoirs, butcher shops, market places and streets. Gastrointestinal (GI) parasites are worldwide problems and important cause of production and productivity loss in livestock, manifested by reduced weight gain, lowered meat and milk production and mortality (Githigia et al., 2005). Furthermore, competition for the nutrients and tissue damage during feeding and

* Corresponding author. Tel.: +251 911 176085. E-mail address: [email protected] (A.K. Basu). 0304-4017/$ – see front matter # 2007 Elsevier B.V. All rights reserved. doi:10.1016/j.vetpar.2007.06.007

migration, could cause severe clinical signs such as anorexia, anaemia, diarrhea and oedema associated with poor performance and mortality particularly in young, aged and immuno-suppressed animals (Urquhart et al., 1996; Fox, 1997; Eysker and Ploeger, 2003). In dogs GI helminths exert serious problems resulting in lowered resistance to infectious disease, retarded growth, reduced work efficiency and general ill-health. Furthermore, dogs are final hosts for numerous helminths which are of zoonotic importance (Aiello and Mays, 1998; Hendrix, 1998). This is particularly true for developing countries where control measures are often not being practised (MacDonald et al., 2002). In Ethiopia, very few studies have been conducted on GI helminths of dogs (Getahun, 1987; Muktar, 1988; Temesgen, 1990; Shihun, 1994). Hence, the present study was carried out with the following objectives: (i) to assess the frequency of infection, (ii) to identify the predominant GI nematodes in the study area, and (iii) to recommend suitable preventive and control strategies.

H.T. Yacob et al. / Veterinary Parasitology 148 (2007) 144–148

2. Materials and methods 2.1. Study area Debre Zeit is located in Oromia National Regional State, about 47 km Southeast of Addis Ababa, at an altitude of 1900 m above sea level. The area experiences a rainfall pattern, a short rainy season from March to May and long rainy season from June to September. It has a mean annual rainfall of 350 mm and a mean annual temperature of 17 8C. 2.2. Study period The study was carried out during the period between January 2005 and June 2006.

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technique (Hendrix, 2003) and quantitative examination using McMaster egg counting technique (Urquhart et al., 1996). Identification of eggs was made by measuring each nematode egg and by observing their characters (Soulsby, 1982; Hendrix, 2003). 2.4.2. Postmortem examination Twenty dogs, 13 male and 7 female (8 young and 12 adults) were euthanized and the alimentary tract was dissected out. The oesophagus, stomach, small intestine, ceacum and colon were separated. Each of the portions was opened longitudinally and examined for the presence of nematodes. Identification and counting of parasites were made as described by Georgi and Theodorides (1980) and Soulsby (1982). 2.5. Statistical analysis

2.3. Study animals Out of 120 dogs examined, 20 animals captured by the Municipal Authorities under stray dog control programme were euthanized and subjected to detailed examination for GI nematodes. The faecal samples were collected from other 100 dogs, brought to the Clinic, Faculty of Veterinary Medicine (FVM), Debre Zeit and from dogs kept in some families of the town. These dogs were never exposed to any deworming before. The history, sex and approximate age, using dentition formulae described by Aiello and Mays (1998), were recorded. Those dogs less than 1 year were classified as young (N = 38) and those over 1 year as adult (N = 62). The numbers of male and female dogs were 69 and 31, respectively. 2.4. Study design 2.4.1. Coproscopic examination The faecal samples were taken directly from the rectum of the dogs using gloved finger and brought to the Parasitology laboratory, FVM, Debre Zeit. The samples were subjected to qualitative (Flotation)

The data thus obtained was analyzed using SPSS version 11.5 for Windows. Percentage of frequency was calculated by dividing the number of animals harbouring any nematode by the total animals examined. The chi-square (x2) test was used to assess difference in frequency of the nematodes between the sex and age groups. In all cases, 95% confidence intervals and P < 0.05, were set for significance. 3. Results 3.1. Coproscopic observations Coproscopic examination revealed 51 dogs (51%) harbouring eggs of GI nematodes. The study revealed the frequency of overall infection in 57.9% of young and 47.8% of adult dogs. Furthermore, the overall infection was recorded in 46.4% of males and 61.3% of females (Table 1). There was no significant difference (P > 0.05) in the frequency of nematode infection between sexes and age groups. Among the infected animals 12 (23.5%) showed polyparasitism. The results revealed 10.3% of a total of

Table 1 Overall frequency of GI nematodes in dogs and frequency in different sex and age groups obtained by coproscopical and postmortem examinations Coproscopy

Postmortem 2

Group

No. of examined

Frequency (%) of infection

x (P value)

No. of examined

Frequency (%) of infection

x2 (P value)

Male Female Young Adult

69 31 38 62

46.4 61.3 57.9 47.8

1.90 (P > 0.05) 7.429 (P > 0.05)

13 7 8 12

92.3 100 100 91.7

0.567 (P > 0.05) 0.702 (P > 0.05)

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Table 2 Overall frequency of mixed infection with GI nematodes in dogs and frequency in different sex and age groups obtained by coproscopical and postmortem examinations Coproscopy No. of positive

Postmortem No. and percent in parenthesis of mixed infection

Adult Young

29 22

3 (10.3) 9 (40.9)

Total

51

12 (23.5)

Male Female

32 19

8 (25) 4 (21)

Total

51

12 (23.5)

x2 (P value)

No. of positive

No. and percent in parenthesis of mixed infection

x2 (P value)

6.48 (P < 0.05)

11 8

4 (36.4) 2 (25)

0.28 (P < 0.05)

19

6 (31.6)

12 7

4 (33.3) 2 (28.6)

19

6 (31.6)

0.103 (P > 0.05)

29 infected adults and 40.9% of 22 infected young with mixed infection. Again 25% of the 32 infected males and 21% of 19 infected females were found with mixed infection. The frequency of mixed nematode infections showed significant difference (P < 0.05) between age groups, whereas no difference (P > 0.05) was observed between sexes (Table 2). Eggs of four different types of GI nematodes were found. Out of total animals examined 32% was infected with Ancylostoma caninum followed by 21% with Toxocara canis, 7% with Spirocerca lupi and 3% with Trichuris vulpis, with mean egg per gram (epg) of faeces 260, 250, 160 and 183.3, respectively. The frequency of infection in young and adult dogs with A. caninum was 44.7 and 24.2% and with T. canis 34.2% and 12.9%, respectively. On the other hand S. lupi and T. vulpis were found only in adults at a frequency of 9.7 and 4.8%, respectively. The frequency of infection in male and female was 30.4 and 35.5% with A. caninum, 17.4 and 29% with T. canis, 5.8 and 6.5% with S .lupi and 2.9 and 3.2% with T. vulpis, respectively (Table 3). The average measurement of egg-size of A. caninum, T. canis, S. lupi and T. vulpis was 64 mm  42 mm, 90 mm  75 mm, 34 mm  12 mm and 89  32 mm, respectively.

0.05 (P < 0.05)

3.2. Postmortem observations Out of 20 dogs examined, 19 (95%) harboured one or more GI nematodes. The study revealed that 92.3% of 13 examined males and all examined females (7) were infected with GI nematodes. Regarding the age groups it was found that all examined young (8) and 91.7% of 12 adult dogs examined were infected (Table 1). There was no significant difference (P > 0.05) in the total frequency between sex and age groups. Among the positive animals, 31.6% were infected with two or more GI nematodes. Mixed infection was observed in 36.4% of infected adult and 25% of infected young dogs. Furthermore, 33.3% of the infected males and 28.6% of the infected females were found with mixed infection. There was no difference (P > 0.05) in frequency of mixed infection between age groups and sexes (Table 2). Among the infected animals 70% were found with A. caninum followed by 45% with T. canis, 23.5% with S. lupi and 5% with T. vulpis along with 16.2, 7.4, 23 and 3 mean worm-burdens, respectively. The frequency of infection with A. caninum was 75 and 66.7% and with T. canis was 50 and 41.6% of young and adults, respectively. S. lupi and T. vulpis were recorded only

Table 3 Frequency of infection, epg and worm burden with different species of nematodes in different sex and age groups of dogs based on coproscopic and postmortem examination Coproscopy

Ancylostoma caninum Toxocara canis Spirocerca lupi Trichuris vulpis

Postmortem

Animal infected (%)

Mean epg

Male (69)

Female (31)

Young (38)

Adult (62)

Animal infected (%)

Worm burden

Male (13)

Female (7)

Young (8)

Adult (12)

32 21 7 1

260 250 160 183

30.4 17.4 5.8 2.9

35.5 29 6.5 3.2

44.7 34.2 0 0

24.2 12.9 9.7 4.8

70 45 23.5 5

16.2 7.4 23 3

69.2 46.2 23.1 7.7

71.4 42.9 14.3 0

75 50 0 0

66.7 41.6 33.3 8.3

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in adult dogs. Similarly, 69.2, 46.2 and 23.1% of the infected male and 17.4, 42.9 and 14.3% of infected female animals were parasitized with A.caninum, T. canis and S. lupi, respectively, while T. vulpis was recorded only in males (Table 3). 4. Discussion The coproscopical and postmortem examinations revealed the frequency of nematode infection to be 51 and 95%, respectively. There was significant difference in the results obtained between the two techniques followed. This could be due to the fact that coprological examinations may not detect the immature parasites, which are unable to lay eggs. However, the overall frequency rate thus obtained on coprological examination is in agreement with previous works in Argentina (Fontanarrosa et al., 2006), Bratislava (Totkova et al., 2006). A high frequency rate was obtained in Turkey (Senlik et al., 2006), Iowa State (Lightner et al., 1978), Netherlands (le Nobel et al., 2004), Belgium (Vanparijs et al., 1991) and in Greece (Haralabidis et al., 1988) but a lower frequency rate was recorded in Santa Catarina (Blazius et al., 2005) and in Nigeria (Ugochukwu and Ejimadu, 1985a). The discrepancy in the overall frequency rates reported in various countries could be attributed to the difference in health care and animal management practices followed in different countries. However, the overall frequency of infection (95%) obtained at postmortem examination is in agreement with previous reports from Debre Zeit (Shihun, 1994). Coproscopical examination revealed a frequency of 32% infection with A. caninum, and a mean epg value of 260. It indicates that this parasite was the most dominant of all the nematodes found. The finding is corroborated with previous reports from Ethiopia (Muktar, 1988; Temesgen, 1990; Shihun, 1994) and few other reports (Okaeme, 1985; Oliveira-Sequeira et al., 2002). But it is significantly higher than the frequencies mentioned in most of the reports from Europe (Gothe and Reichler, 1990; Overgaauw, 1997; Fontanarrosa et al., 2006; Totkova et al., 2006) and lower than that reported from other African countries (Hassan, 1982; Ugochukwu and Ejimadu, 1985b; Blazius et al., 2005). On the other hand, 21% infection with T. canis along with mean epg value of 250 is in agreement with the earlier reports (Ugochukwu and Ejimadu, 1985a; Haralabidis et al., 1988; Vanparijs et al., 1991; Totkova et al., 2006). The high incidence of A. caninum and T. canis, which could cause creeping eruption and visceral larval migrans, respectively, in human beings, constitutes an important public health problem.

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A frequency of 7% infection with S. lupi along with a mean epg value of 160 is inconsistent with reports from Brazil (Oliveira-Sequeira et al., 2002) and Greece (Haralabidis et al., 1988). On the other hand, 3% infection with T. vulpis along with a mean epg value of 183 is in agreement with the works of Haralabidis et al. (1988), Oliveira-Sequeira et al. (2002), le Nobel et al. (2004) and Senlik et al. (2006) but lower than the findings of few others (Vanparijs et al., 1991; Blazius et al., 2005; Fontanarrosa et al., 2006). The difference in the frequency of the nematode infections between countries is possibly due to the differences in climatic factors required for the biology of the parasites, veterinary facilities and public awareness to take care of the dogs. During the survey it was noted that a large number of dogs scavenge at abattoirs and at butcher shops and those kept indoors are also frequently fed uncooked offal that are not in good hygienic condition. It is also common to find animal cadaver thrown into street where dogs communally feed on, which could be a suitable media for transmission of the parasites. The frequency of T. canis and S. lupi infection found in postmortem study is in agreement with previous reports from Ethiopia (Getahun, 1987; Muktar, 1988; Shihun, 1994; Temesgen, 1990). The significantly higher frequency of nematode infections, specifically with A. caninum and T. canis in young dogs as compared to adults is in consistent with previous studies (Haralabidis et al., 1988; Overgaauw, 1997; le Nobel et al., 2004; Fontanarrosa et al., 2006; Oliveira-Sequeira et al., 2002; Ugochukwu and Ejimadu, 1985b). The higher frequency of these nematodes in younger dogs could be due to the mode of transmission of the parasites and puppies could be infected transplacentally and transmammary which increase the occurrence of the parasites at an early age, whereas, adult dogs may develop immunity which decrease the establishment as well as the fecundity of the parasites (Soulsby, 1982; Urquhart et al., 1996). On the other hand, eggs of S. lupi and T. vulpis were only detected in adult dogs. Similar results were reported for S. lupi from Ethiopia (Shihun, 1994 and Muktar, 1988). It could be associated with the mode of life cycle of S. lupi, which requires long time for migration and development to maturity (Catcott, 1968; Soulsby, 1982). The study also showed no significant difference (P > 0.05) in frequency of GI nematodes of dogs between sex and the results are consistent with previous works (Haralabidis et al., 1988; Fontanarrosa et al., 2006). More than one species of GI nematodes in a

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single host were observed with frequency of 23.55 and 31.6% on coproscopy and postmortem examinations, respectively. It might be due to the fact that the dogs act as scavenger and do not get regular medical care. The presences of different nematode species in a single host as well as high frequency of these parasites in the study area require serious attention due to pathogenic impact of the parasites and their zoonotic importance. Therefore, strategic deworming of dogs using broad-spectrum anthelmintics and public education on the care and management of dogs to create awareness on the transmission and control of zoonotic diseases, have paramount importance. Moreover, further epidemiological studies should be conducted seasonally in different regions of the country. References Aiello, S.E., Mays, A., 1998. The Merck Veterinary Manual, 8th ed. Merck and Co. Inc., NJ, USA, pp. 2305. Blazius, R.D., Emerick, S., Prophiro, J.S., Romao, P.R., Silva, O.S., 2005. Occurrence of protozoa and helminths in fecal samples of stray dogs from Itapema City Santa Catarina. Rev. Soc. Bras. Med. Trop. 38, 73–74. Catcott, E.J., 1968. Canine Medicine, 1st ed. American Veterinary Publication Inc., pp. 859. Eysker, M., Ploeger, H.W., 2003. Value of present diagnostic methods for gastrointestinal tract nematodes infection in ruminant.In: Symposia of the British Society for Parasitology, vol. 37. Cambridge University Press, UK, pp. 109–119. Fontanarrosa, M.F., Vezzani, D., Basabe, J., Eiras, D.F., 2006. An epidemiological study of gastrointestinal parasites of dogs from Southern Greater Buenos Aires (Argentina): age, gender, breed, mixed infections, and seasonal and spatial patterns. Vet. Parasitol. 136, 283–295. Fox, M.T., 1997. Pathophysiology of infection with gastrointestinal nematodes in domestic ruminants: recent developments. Vet. Parasitol. 72, 285–308. Georgi, J.R., Theodorides, V.J., 1980. Parasitology for Veterinarians, 3rd ed. W.B. Sounders Co., Philadelphia, pp. 460. Getahun, D., 1987. Incidence of bovine echinococosis at Melgue Wondo abattoir and the role of dogs. DVM Thesis, Addis Ababa University, Fac. Vet. Med., Ethiopia. Githigia, S.M., Thamsberg, S.M., Maing, N., Munyua, W.K., 2005. The epidemiology of gastrointestinal nematodes in goats in the low potential areas of Thinka, district Kenya. Bull. Anim. Health. Prod. Afr. 53, 5–12. Gothe, R., Reichler, I., 1990. Spectrum of species and infection frequency of endoparasites in bitches and their puppies in south Germany. Tierarztl. Prax. 18, 61–64. Haralabidis, S.T., Papazachariadou, M.G., Koutinas, A.F., Rallis, T.S., 1988. A survey on the prevalence of gastrointestinal

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