Research Article

 

Tick-Borne Diseases-Possible Threat to Humans-Dog Interspecie Bond

 

Said Sajjad Ali Shah1*, Muhammad Ilyas Khan1, Rafiullah1, Mirza Ali Khan1, Hamidullah Khan1, Anwar Ali1, Muhammad Ijaz Ali1, Rafiullah Jan2

1Veterinary Research Institute, Peshawar, Pakistan; 2The University of Agriculture, Peshawar, Pakistan.

 

Editor | Kuldeep Dhama, Indian Veterinary Research Institute, Uttar Pradesh, India.

Received | February 16, 2017; Accepted | March 10, 2017; Published | March 12, 2017

*Correspondence | Said Sajjad Ali Shah, Research Officer (CPP), Veterinary Research Institute, Peshawar, Pakistan; Email: sajjadsheikh0695@gmail.com

Citation | Shah SSA, Khan MI, Rafiullah, Khan MA, Khan H, Ali A, Ali MI, Jan R (2017). Tick-borne diseases-possible threat to humans-dog interspecie bond. Adv. Anim. Vet. Sci. 5(3): 115-119.

DOI | http://dx.doi.org/10.14737/journal.aavs/2017/5.3.115.119

ISSN (Online) | 2307-8316; ISSN (Print) | 2309-3331

Copyright © 2017 Shah et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

 

INTRODUCTION

 

Humans and dogs lived for years together and now it turn out to be one the best human’s friend and become valued pet. Dogs are closest to humans due to their splendid and remarkable social behaviors (Ugbomoiko et al., 2008). Due to higher influence on society and numerous roles, dog has given the sobriquet, “man’s best friend”. Dog evolved from gray wolves and is considered to be the most abundant carnivore (Vila et al., 1999; Thalmann et al., 2013; Zhenxin et al., 2016). Dogs fulfill its duty for humans in the form of hunting, herding sheep and goats, protection, assisting security forces and more recently, dogs are used to identify thefts (Savolainen et al., 2002).

 

In Pakistan, dogs are mainly kept by security forces, as watch dog in houses and for herding of sheep etc by shepherds (Jafri and Rabbani, 1999). Despite of its definite role in society, large number of dogs still live as feral and stray dogs which receive minimal public attention. Though a felony offence but in most parts of the country dogs are kept for fighting purposes. There is growing trend of keeping dog as pet animal in urban population of Pakistan and mostly kept by middle and upper-middle class households. Different breeds of dogs i.e. German shepherd, Pointer, Labrador and Spaniel are kept by corps which aids them in routine security operations as sniffer dogs which perform search duties with high sense of responsibility. Apart from corps, local population kept Bull Terrier (Local name Gull Terr, for security and fighting purpose), German shepherd (Popular name in locals, Alsatian dog) and Hounds (Tazi, for hunting).

 

Dog population is faced with different viral, bacterial, fungal and parasitic diseases. Tick borne diseases i.e. Canine babesiosis and anaplasmosis are most important parasitic diseases of dogs. Etiological agents of Canine babesiosis are Babesia canis, Babesia gibsoni and Babesia vogeli in which Babesia canis is of significant importance (Toboada, 1998; Birkenheuer et al., 1999). Canine babesiosis is transmitted by different tick vectors i.e. Hyalomma, Rhipicephalus sanguineus and Dermacentor variabilis. Anaplasmosis is caused by Anaplasma phagocytophilum, an intracellular parasite, transmitted by tick vector Ixodes (Dumler et al., 2001; Cohn, 2003). Anaplasma phagocytophilum has wide range of host including sheep and goats and also have zoonotic potential.

 

Currently, there is limited data available about dogs in Pakistan, and this is the most neglected specie in the research institutes of the country. Presently only few published reports are available on canine babesiosis but none about anaplasmosis. Due to huge population of stray dogs in urban areas of the country, it is of utmost importance to study various canine diseases. Aim of the present study was to find out the prevalence and hematological changes of haemo-parasites in dogs and to correlate it with its health status.

 

MATERIALS AND METHODS

 

Study Area

 

This study was conducted in district Peshawar and Charsadda. Peshawar district lies at 34.04°N latitude and 71.5°E longitude with an altitude of 359m and has area of 1257 km2 While district Charsadda is located at 34.8°N latitude and 71.43°E longitude with an altitude of 276m (908 feet) and lies 29 km from the provincial capital, Peshawar.

 

Sample Collection

 

This study was conducted from January, 2015 to December, 2016. Blood samples (n=121) were collected and received from different areas of Peshawar and Charsadda in the Center of Parasitology and Poultry (CPP) and Center of Microbiology and Biotechnology (CMB), Veterinary research institute, Peshawar. Whole blood samples collected in anti-coagulant added vacutainer tubes were transported to Veterinary Research Institute, Peshawar for onward processing.

 

Microscopic Examination

 

Blood smears were prepared, fixed with methanol for 5 min and stained with 10% giemsa. Microscopic examination of the stained smears was performed at 100× objective for the presence or absence of parasites (Ahmad et al., 2007).

 

Hematology

 

For estimation of hematological alterations, anti-coagulant added blood was submitted to Pathology Lab, Veterinary Research Institute, Peshawar and were processed for complete blood count through Automatic Hematology analyzer (Urit Vet 2900) (Yasini et al., 2012).

 

Statistical Analysis

 

Data thus collected was analyzed by Chi square test for prevalence of tick borne diseases with respect to season, location, breed, age and sex while student t-test was used for analysis of hematological data. Means of hematological parameters were compared by LSD at a probability level ≤ 0.05 using Statistical Package for Social Services (SPSS) version 16.0.

 

RESULTS AND DISCUSSION

 

Prevalence Of Haemo-Parasites

 

Results of the study showed that out of 121 blood samples 64 (52.8%) samples were positive for Haemo-parasites. Anaplasmosis was recorded as 34%, while Canine babesiosis as 19% (Figure 1).

 

Risk Factors For Haemo-Parasites

 

Different risk factors associated with occurrence of canine babesiosis and anaplasmosis were studied in detail. Results of the study showed that haemo-parasites were more in summer season (62%) as compare to winter (35.7%). Statistically significant difference (P<0.05) was recorded in the incidence of haemo-parasites with respect to season. This study was conducted in two districts of Khyber Pakhtunkhwa i.e. Peshawar and Charsadda. Slight difference in incidence was recorded in both districts but was statistically non-significant (P>0.05). Breed wise prevalence was recorded as 62.2, 30, 22.2, 14.2, 80.9 and 38% for German shepherd, Spaniel, Labrador, Pointer, Gull Terr and Tazi, respectively. Statistically significant difference (P<0.05) was recorded with respect to breed. Dog owners were also studied as risk factor in the present study and it was observed that occurrence of haemo-parasites were more in

 

Table 1: Prevalence of Haemo-protozoan in dogs with respect to season, location, breed, owner, sex and age

 

Variables	Category	N	Haemo-parasites prevalence (%)	Chi square value	P value
Season	Winter	42	35.7	8.18	0.01*
	Summer	79	62%
Location	Peshawar	101	52.4	0.58	0.74
	Charsadda	20	55
Breed	German shepherd	53	62.2	21.24	0.01*
	Spaniel	10	30
	Labrador	9	22.2
	Pointer	7	14.2
	Gull Terr	21	80.9
	Tazi	21	38
Owner	Farmer	78	64.1	11.38	0.00*
	Govt	43	32.5
Sex	Female	4	50	0.182	0.91
	Male	117	52.9
Age	Adult	60	81.6	39.5	0.00*
	Young	61	24.5

 

* shows significant difference at level P<0.01; N: Total number of cases

 

 

dogs kept by farmers individually as compare to dogs kept by security forces and difference was statistically significant (P<0.05). Occurrence was recorded more in males as compare to females but statistically non significant (P>0.05%). In these study two age groups i.e. adults (age group more than 3 years) and young (age group less than 3 years) were studied. Haemo-parasites occurrence was found statistically higher (P<0.05) in adults i.e. 81.6% as compare to young dogs i.e. 24.5% (Table 1).

 

Table 2: Hematological parameters of infected and non-infected dogs

 

Parameter	Negative	Infected	P-value
TEC (x106/µl)	6.01a±0.08	3.90b±0.12	0.00*
Hb (g/dl)	16.02a±0.37	9.65b±0.32	0.00*
HCT (%)	39.4a±0.55	25.32b±0.81	0.00*
MCH (pg)	26.58a±0.49	25.04b±0.46	0.02**
MCV (fl)	65.69a±0.45	65.16a±0.49	0.43
MCHC (g/dl)	40.47a±0.61	38.38b±0.51	0.00*
TLC (x103/µl)	15.41a±1.3	10.32b±0.85	0.01*
Granulocytes (%)	51.12a±3.29	44.38a±3.07	0.13
Lymphocytes (%)	33.53a±2.85	29.85a±2.07	0.29
Monocytes (%)	22.03a±0.90	18.86a±1.22	0.04**
Platelets (x103/µl)	217.65 a±13.07	122.77 b±10.43	0.00*

 

a, b means with different superscript with in row are significant at *P-value< 0.01 and **P-value <0.05; TEC: Total erythrocytes count; Hb: Hemoglobin; HCT: Hematocrit; MCV: Mean corpuscular volume; MCH: Mean corpuscular hemoglobin; MCHC: Mean corpuscular hemoglobin concentration; TLC: Total leukocytic count

 

Hematological Profile

 

Hematological results showed that there was significant decrease (P<0.01) in the total erythrocyte count in infected animals. Similarly, hemoglobin and hematocrit values of infected animals were lowered from that of normal animals and these were found highly significant statistically (P<0.01). Results of Erythrocytic indices showed that there was significant decrease in the value of Mean corpuscular hemoglobin (MCH) (P<0.05) and MCHC (P<0.01) while no significant changes were observed in the value of Mean corpuscular volume (MCV) (P>0.05). Significant changes were observed in the value of Total leukocytes count (TLC) (P<0.01) and monocytes (P<0.05), whereas no significant changes were observed in granulocytes and lymphocytes (P>0.05). Platelets value of infected dogs were lowered from non-infected and was found significant statistically (P<0.01) (Table 2).

 

Due to close association and dependency on each other, dogs and humans lived for years together and dogs had performed various roles for human beings. Dogs were used in the past only for guarding, fighting, hunting and herding of sheep and goats, but over the years its role has changed and it can be kept as pet, as sniffing dog by security forces for narcotics, ammunition and also for identification of thefts and culprits. Due to its numerous roles and services for human, it is fully justified to call it “man’s best friend” (Vila et al., 1999; Savolainen et al., 2002; Thalmann et al., 2013). Despite of its definite role in society, huge population of dogs still present as feral and stray dogs in Pakistan and has nominal public attention. Due to this negligence, no proper statistics is presently available about dog’s population in the country and researchers are still reluctant to work in this neglected area.

 

Overall incidence of haemo-parasites in the current study was recorded as 19 and 34% for canine babesiosis and anaplasmosis, respectively. Prevalence of canine babesiosis was almost similar to results of (Ahmad et al., 2007) who recorded 14% prevalence of canine babesiosis in Lahore, Pakistan. These results are further supported by findings of (Mas, 1990) (20%) and (Cabannes et al., 2002) (14%). (Laha et al., 2014) reported higher prevalence (56%) of canine babesiosis which might be due to the reason that (Laha et al., 2014) studied molecular prevalence of canine babesiosis, while microscopy was used in the present study which is less sensitive comparatively. Prevalence of anaplasmosis in the present study was found similar with the findings of (Pennisi et al., 2012) who reported 38% prevalence of anaplasma. Findings of (Bhattacharjee and Sarmah, 2013) are not in agreement with current study and the possible reasons may be that (Bhattacharjee and Sarmah, 2013) reported only Anaplasma platys and did not reported Anaplasma phagocythophilum.

 

Findings of (Hamel et al., 2015) were not in agreement with the results of the present study who reported 24% prevalence of anaplasma species. Higher prevalence in the present study might be due to the fact that Peshawar and Charsadda districts offer favorable environment for tick infestation and tick borne diseases in other domestic animals.

 

Prevalence of anaplasmosis and canine babesiosis were studied in detail with respect to different risk factors i.e. season, location, breed, owner, sex and age. Prevalence of haemo-parasites was higher in summer season as compare to winter and this was found statistically significant. In summer season, ticks infestation is high comparatively due to which the occurrence of tick borne diseases are higher. This finding is supported by many workers that season play key role in occurrence of parasitic diseases (Lorusso et al., 2010; Ahmad et al., 2011; Jalali et al., 2013). The present study was conducted in two districts of Khyber Pakhtunkhwa and to the authors knowledge no publish material is available currently about the prevalence of anaplasmosis and canine babesiosis in Khyber Pakhtunkhwa, Pakistan. Prevalence of haemo-parasites was more in district Charsadda as compare to Peshawar but the differences were not statistically significant. Increased humidity and rural environment in district Charsadda might be the possible reason for slightly higher occurrence of haemo-parasites. These findings are fully supported by the study conducted by (Jalali et al., 2013) that prevalence is higher in rural environment as compare to urban.

 

Samples collected were from two different sources i.e. public and private sectors including armed forces. Occurrence was higher in dogs kept at personal level as compare to dogs from government institutions and it was found statistically significant. Government agencies kept dogs for special purposes and they treat their dogs regularly whereas, lack of awareness in farmers may be the cause for higher prevalence. Secondly, government agencies kept dogs in kennels which are cleaned regularly whereas, farmers kept dogs in close vicinity of cattle, sheep, goats and are highly exposed to ticks infestation by ticks migration. Individual farmers mostly kept Gull Terr dog for the purpose of protection and fighting, German shepherd and Tazi dog for hunting, while government agencies have different breeds for different purposes i.e. German Shepherd, Spaniel, Labrador and Pointer. Breed wise occurrence was higher in Gull Terr and German shepherd and was found statistically significant. Similar findings were recorded by (Shrivastava et al., 2014)that prevalence was higher in German shepherd. Sex was also considered as an important indicator for the prevalence of haemo-parasites in dogs by many workers (Bashir et al., 2009), but in the present study no significant differences were observed because most of samples received or collected were from male dogs. Occurrence of haemo-parasites is age dependent and in young animals its prevalence is lower as compare to adults. In adult dogs, significantly higher incidence was recorded comparatively. These findings are in congruent with the study conducted by (Bashir et al., 2009; Jalali et al., 2013).

 

There was significant decrease in the value of TEC, Hb and PCV which are important indicators of anemia. Many workers in the past also considered anemia as an important outcome of haemo-parasitic diseases in dogs. Anemia may be due to direct parasite damage to red blood cells or due to auto antibodies directed against erythrocytes cell membrane. Similar results of hematology were also reported by (Day, 1999; Pederson, 1999; Taboada and Lobetti, 2006; Salem and Farag, 2014). On the basis of erythrocytic indices, anemia can be classified as normocytic hypochromic because MCHC was lower and MCV was in normal range. Along with parasitic diseases normocytic hypochromic anemia can also be attributed to iron and folate deficiency (haematinics).

 

Acknowledgements

 

We are very thankful to Pathology section, Center of Microbiology and Biotechnology (CMB), Veterinary Research Institute, Peshawar for providing hematological data.

 

Conflict of Interest

 

There is no conflict of interest.

 

AUTHERS’ CONTRIBUTION

 

SSAS and MAK conceived and designed the study. RJ helped in sample collection and processing. Rafiullah and AA provided the hematology data. SSAS, MAK, MJA, HK drafted the manuscript. All authors revised the manuscript and approved the final version.

 

REFERENCES

 

Ahmad SS, Khan MS, Khan MA (2007). Prevalence of Canine Babesiosis in Lahore, Pakistan. J. Anim. Pl. Sci. 17(1-2): 11-13.

Ahmad SS, Khan MS, Khan MA (2011). Epidemiology and seasonal abundance of Canine Babesiosis in Lahore, Pakistan. The Journal of Animal and Plant Sciences, 21(2): 351-353.

Bashir IN, Chaudhry ZI, Ahmed S, Saeed MA (2009). Epidemiological and vector identification studies on canine Babesiosis. Pak. Vet. J. 29: 51–54.

Bhattacharjee K and Sarmah PC (2013). Prevalence of haemoparasites in pet, working and stray dogs of Assam and North-East India: A hospital based study. Vet. World. 6 (11): 874-878

Birkenheuer AJ, Levy MG, Savary KC (1999). Babesia gibsoni infections in dogs from North Carolina. J. Am. Ani. Hos. Asso. 35: 125-128. https://doi.org/10.5326/15473317-35-2-125

Cabannes A, Pels H, Lucchese F, Appriou M (2002). Séroprévalence de la babésiose canine dans le sud-ouest de la France. Rev. Méd. Vét. 153: 27–28.

Cohn LA (2003). Ehrlichiosis and related infections. Veterinary Clinics: Small Animal Practice. 33: 863-884. https://doi.org/10.1016/s0195-5616(03)00031-7

Day MJ (1999). Antigen specificity in canine autoimmune hemolytic anemia. Vet. Immunol. Immunopathol. 69: 215-224. https://doi.org/10.1016/S0165-2427(99)00055-0

Dumler JS, Barbet AF, Bekker CP, Dasch GA, Palmer GH, Ray SC, Rikihisa Y, Rurangirwa FR (2001). Reorganization of genera in the family’s Rickettsiaceae and Anaplasmataceae in the order Rickettsiales: unification of some species of Ehrlichia with Anaplasma, Cowdria with Ehrlichia and Ehrlichia with Neorickettsia, descriptions of six new species combinations and designation of Ehrlichia equi and ’HGE agent’ as subjective synonyms of Ehrlichia phagocytophila. J. Sys. Evol. Microbiol. 51: 2145–2165. https://doi.org/10.1099/00207713-51-6-2145

Hamel D, Shukullari E, Rapti D, Silaghi C, Pfister K, Rehbein S (2015). Parasites and vector-borne diseases in client-owned dogs in Albania. Blood pathogens and seroprevalences of parasitic and other infectious agents. Parasitol. Res.

Jafri SA, Rabbani M (1999). Prevalence of canine diseases in Lahore area. Pak. Vet. j. 19 (1): 40-41.

Jalali R, Mosallanejad MH, Avizeh B, Alborzi R, Hamidi-Nejat AR, Taghipour H (2013). Babesia infection in urban and rural dogs in Ahvaz district, Southwest of Iran. Archives of Razi Institute. 68(1): 37-42.

Laha R, Bhattacharjee K, Sarmah PC, Das M, Goswami A, Sarma D, Sen A (2014). Babesia infection in naturally exposed pet dogs from a north-eastern state (Assam) of India: detection by microscopy and polymerase chain reaction. J Parasit Dis . 38(4): 389–393.

Lorusso V, Dantas-Torres F, Lia RP, Tarallo VD, Mencke N, Capelli G, Otranto D (2010). “Seasonal dynamics of the brown dog tick, Rhipicephalus sanguineus, on a confined dog population in Italy. Med. Vet. Entomol. 24(3): 309-15. https://doi.org/10.1111/j.1365-2915.2010.00885.x

Mas JP (1990). Séroépidémiologie de la babésiose canine en région d’endémie. Thèse Doct. Vét. Lyon, n849.

Pederson NC (1999). A review of immunologic diseases of the dog. Vet. Immunol. Immunopathol. 69: 251-342. https://doi.org/10.1016/S0165-2427(99)00059-8

Pennisi MG, Caprì A, Solano-Gallego L, Lombardo G, Torina A, Masucci M (2012). Prevalence of antibodies against Rickettsia conorii, Babesia canis, Ehrlichia canis, and Anaplasma phagocytophilum antigens in dogs from the Stretto di Messina area (Italy). Ticks Tick Borne Dis. 3(5-6). https://doi.org/10.1016/j.ttbdis.2012.10.026

Salem NY, Farag HS (2014). Clinical, hematologic, and molecular findings in naturally occurring Babesia canis vogeli in Egyptian dogs. Veterinary Medicine International. doi: 10.1155/2014/270345.270345

Shrivastava S, Shukla PC, Rao ML (2014). An epidemiological study on canine hemoprotozoa in Jabalpur (Madhya Pradesh). Int. J. Agric. Sci. Vet. Med. 2: 4.

Svolainen P, Zhang YP, Luo J, Lundeberg J, Leitner T (2002). Genetic evidence for an East Asian origin of domestic dogs. Sci. 298: 1610-1613. https://doi.org/10.1126/science.1073906

Taboada J, Lobetti R (2006). Babesiosis, in Infectious Diseases of the Dog and Cat, C. G. Greene, Ed., Elsevier, 3rd edition.

Thalmann O, Shapiro B, Cui P, Schuenemann VJ, Sawyer SK, Greenfield DL, Germonpre MB, Sablin MV, Lopez-Giraldez F, Domingo-Roura X, Napierala H, Uerpmann HP, Loponte DM, Acosta AA, Giemsch L, Schmitz RW, Worthington B, Buikstra JE, Druzhkova A, Graphodatsky AS, Ovodov ND, Wahlberg N, Freedman AH, Schweizer RM, Koepfli K P, Leonard JA, Meyer M, Krause J, Paabo S (2013). Complete Mitochondrial Genomes of Ancient Canids Suggest a European Origin of Domestic Dogs. Sci. 342 (6160): 871. https://doi.org/10.1126/science.1243650

Toboada J (1998). Babesiosis in Greene CE (ed) infectious diseases of the dog and cats. WB Saunders, Philadelphia PA. 473-481.

Ugbomoiko US, Ariza L, Heukelbach J (2008). Pigs are the most important animal reservoir for Tunga Penetrans (Jigger flea) in rural Nigeria. Trop. Doct. 30: 226-227. https://doi.org/10.1258/td.2007.070352

Vila C, Amorim IR, Leonard JA, Posada D, Castroviejo J, Petrucci-Fonseca F, Crandall KA, Ellegre H, Wayne RK (1999). “Mitochondrial DNA phylogeography and population history of the grey wolf Canis lupus”. Molecular Ecology. 8 (12): 2089-103. https://doi:10.1046/j.1365-294x.1999.00825.x. PMID 10632860.

Yasini S, Khaki Z, Rahbari S, Kazemi B, Amoli JS, Gharabaghi A, Jalali S (2012). Hematologic and Clinical Aspects of Experimental Ovine Anaplasmosis Caused by Anaplasma ovis in Iran. Iranian J. Vet. Res. 14 (1): 50-56.

Zhenxin F, Pedro S, Ilan G, Shuoguo W, Serres AA, Rena MS, Oscar R, John P, Marco G, Del-Vecchyo DO, Lianming D, Wenping Z, Zhihe Z, Jinchuan X, Carles V, Tomas M, Raquel G, Bisong Y, Robert KW (2016). “Worldwide patterns of genomic variation and admixture in gray wolves”. Genome Res. 26 (2): 163–73. https://doi.org/10.1101/gr.197517.115