PREVALENCE OF IXODIDAE TICKS AND THEIR ASSOCIATION WITH DIFFERENT RISK FACTORS IN KHYBER PAKHTUNKHWA, PAKISTAN
M. Shoaib1, I. Rashid1*, H. Akbar1, A. A. Sheikh2, S. H. Farooqi3, M. A. Khan4, S. Mahmood5 and F. A. Khan6
1Department of Parasitology, University of Veterinary and Animal sciences, Lahore
2Department of Microbiology, University of Veterinary and Animal sciences, Lahore
3College of Veterinary and Animal sciences, Narowal
4Livestock and Dairy Development (Extension), KP
5Department of Geography, G.C, University, Lahore
6College of Veterinary sciences, The University of Agriculture, Peshawar, KP
*Corresponding author’s email: imran.rashid@uvas.edu.pk
ABSTRACT
Ixodid ticks are in varying distribution patterns throughout Pakistan. They cause substantial losses to livestock industry in terms of hide loss and vector-borne disease transmission. This study was conducted in three districts of Khyber Pakhtunkhwa (KPK) from March 2018 to February 2019 with the aim of determining the prevalence and seasonal variation in tick species belonging to Ixodidae family in cattle population. A total of 1145 adult ticks were collected by a convenient method of sampling from 434 infested cattle of various breeds, age groups and sexes. Identification of ticks up to genus and species level was done with the help of specific morphological keys. The results showed higher prevalence of Rhipicephalus (Boophilus) microplus (77%) followed by R. (B) annulatus (70%), R. (B) decoloratus (54%), H. anatolicum (52%) and the least prevalence was recorded in R. (B) turanicus (12%). The prevalence of all ixodid tick species with exception of R. (B) annulatus and R. (B) decoloratus was significantly associated (p<0.05) with districts, breed, age and sex of cattle. Tick prevalence was higher in Achai and Friesian breeds, young stock and male animals. Prevalence of tick infestation was at its peak during summer and rainy seasons and remained low during winter season. In conclusions, that cattle tick R. (B) microplus was the dominant tick species infesting cattle population of KPK province and tick burden presented the highest record in summer season.
Key words: Prevalence, Ixodid tick species, Cattle, Season, KPK.
https://doi.org/10.36899/JAPS.2022.2.0438
Published first online August 13, 2021
INTRODUCTION
Ticks are a major group of ectoparasites belong to Arachnida class. There are three main families of ticks. Family Ixodidae (hard ticks) accounting for 727 species, family Argasidae (soft ticks) having 211 species and family Nuttalliellidae with only one species (Barros-Battesti et al., 2006). In tropical and subtropical countries, livestock are affected mostly by tick infestation either by blood sucking directly or through transmission of toxins and pathogens indirectly, so they are harmful to economic (Jongejan and Uilenberg, 1994). They transmit pathogens like viruses, bacteria, protozoans and rickettsiae and have been ranked as the first vector of animal diseases while second as human diseases after mosquitoes (Zhou et al., 2009). Important hemoparasitic diseases like theileriosis, babesiosis and anaplasmosis are transmitted by ticks (Norval et al., 1984) and they result in lowered productivity (Sajid et al., 2007). Rhipicephalus (Boophilus) microplus and R. (B) decoloratus were the reported species of ticks in cattle of Cameroon (Silatsa et al., 2019). Dermacentor reticulatus and Ixodes ricinus were the prominent tick species in Lithuania (Sidorenko et al., 2021).
Hyalomma tick is the most prevalent tick genus followed by Boophilus, Haemaphysalis and Rhipicephalus, respectively in Kasur, Pakistan (Durrani and Kamal, 2008). Rhipicephalus (Boophilus) microplus and Hyalomma anatolicum anatolicum are the tick species identified from various livestock species in Haripur, Mansehra, Kohistan and Shangla of KPK province and Gilgit Baltistan province of Pakistan (Sajid et al., 2017). Hyalomma anatolicum and R. (B) microplus are the tick species from Gujranwala, Sheikhupura, Gujrat and Sialkot of Pakistan (Adegoke et al., 2020). Hyalomma hussaini, R. (B) microplus, R. (B) annulatus, H. scupense and H. anatolicum were the five identified tick species of hard ticks of family Ixodidae from five different zones of Pakistan (Ghafar et al., 2020). Rhipicephalus (Boophilus) annulatus is the most predominant species in three temporal zones of KPK, R. (B) microplus stands second followed by H. aciculifer. Besides these, R. appendiculatus, R. decoloratus, H. detritium, H. anatolicum, H. trancatum, R. evertsi, R. arnoldi, R. kochi, A. pomposum, D. rhinocerinus, D. circumguttatus, H. excavatum, H. houyi, H. impeltatum, R. distinctus, H. aegyptium, Heamaphyslais parmata, H. rufipes, R. parvas and R. longus are other tick species identified (Farooqi et al., 2017). Rhipicephalus microplus, R. haemaphysaloides, R. sanguineus, R. turanicus, R. annulatus, Haemphysalis bispinosa, Hae. kashmirensis, Hae. montgomeryi, Hae. cornupunctata, Hae. sulcata, Hae. montomeryi, Hyalomma anatolicum, Hy. kumari, Hy. isacci, Hy. dromedarii, Hy. turanicum, Hy. scupense, Ornithodorus tholozani, Argas percicus are the identified nineteen tick species infesting livestock in Pakistan. Rhipicephalus haemaphysaloides, R. turanicus and Haemaphysalis montomeryi are the tick species identified from KPK province (Karim et al., 2017). Therefore, this study was designed to find out the prevalence of tick species along with their seasonal distribution in districts Mardan, Swat and Kohat of Khyber Pakhtunkhwa province.
MATERIALS AND METHODS
Study Area: There are three zones (northern, southern and central) in KPK province based on climatic data such as temperature and rainfall (Farooqi et al., 2017). Three districts namely Swat, Kohat and Mardan were selected as the study areas from above zones respectively. These districts were selected based on temporal changes among the zones and the huge population of livestock in these districts. In the study areas, there are four seasons viz. winter (November-January), spring (February-April), summer (May-July) and autumn (August-October).
Study Population: The tick samples were collected from different cattle breeds in the selected districts of KPK province. Two periodical visits were made once a week to find out the seasonal prevalence of ticks in the three districts. These tick samples were collected from animals of local farmers and small holder farms. Ticks were collected from 434 infested cattle by a convenient method of sampling (Muhib et al., 2001). A total of 1145 ticks were collected from infested cattle (Mardan = 396, Kohat = 369 and Swat = 380). Cattle of both sexes, age and breed were examined, and therefore recorded as a sample unit. The examined breeds of cattle were Friesian, Cross-bred, Achai and Sahiwal.
Collection of ticks and storage: The study was carried out from March 2018 to February 2019. Tick samples were collected from infested animals. A questionnaire was used having information regarding date of collection, place of collection, details about animals (age, sex and breed) and body site of collection (Thrusfield, 2018). Ticks were collected from various body parts of animal i.e., axillary region, neck and back region, perineum and dewlap of animals with the aid of forceps and taking care of their mouthparts (Soulsby, 1982). 70% ethanol solution in labeled disposable tubes was used as preservative of ticks.
Identification of ticks: The preserved tick specimens were examined under stereomicroscope in the entomology laboratory, Department of Parasitology UVAS, Lahore. Identification up to genus and species level was done with the help of specific morphological keys (Karim et al., 2017; Keirans and Litwak, 1989).
Statistical Analysis: Data regarding tick prevalence and associated risk factors were analyzed using Pearson’s Chi-square (χ2) test. Specific software named statistical package for social science (SPSS) version 20 was used for Pearson’s Chi-square (χ2). The risk factors association with tick burden was considered significant at p value <0.05 (Farooqi et al., 2017).
RESULTS
The study was conducted to determine the distribution of tick infestation in cattle population of KPK province. Rhipicephalus and Hyalomma were the two dominant genera in the present study. The identified species were R. (B) microplus, R. (B) annulatus, R. (B) decoloratus, R. (B) turanicus and H. anatolicum (Fig.2).
Fig. 1. Map of Pakistan showing three targeted districts of Khyber Pakhtunkhwa province (KP) i.e., Mardan, Kohat and Swat. Tick samples were collected from these three districts
Fig. 2. Different ixodid ticks species of KPK. Basic morphological structures of tick like scutum, shape of porose area and hypostomal teeth configuration which are helpful in ixodid ticks species identification.
It was found that the difference in prevalence of ixodid tick species was significant (p<0.05) among the study districts except R. (B) annulatus and R. (B) decoloratus. Rhipicephalus(Boophilus) microplus was the most prevalent tick species followed by R. (B) annulatus, R. (B) decoloratus, H. anatolicum and the least prevalent was R. turanicus species, respectively in the studied districts as shown in Table 1. The results showed a significant association (p<0.05) of tick infestation with all the cattle breeds except R. (B) annulatus and R. (B) decoloratus. Rhipicephalus (Boophilus) microplus, R. (B) annulatus and H. anatolicum were the predominant tick species in local breed (Achai) and R. (B) decoloratus and R. (B) turanicus in exotic breed (Friesian), respectively (Table 2). It was observed from the results that there was significant association (p<0.05) of tick species infestation with age and sex of the cattle among study districts except R. (B) annulatus and R. (B) decoloratus where there was non-significant association (p>0.05) as shown in Tables 3 and 4. The prevalence of tick species infestation was higher in young than adult cattle (Table 3). Similarly, male cattle were infested more with tick species than females in the studied districts (Table 4). It was observed from the study that there was higher ratio of male tick species than females except R. (B) turanicus where female ticks were higher in number than males as shown in Table 5. The study showed that there was significant association of tick infestation (p<0.05) with the seasons among the investigated districts. The prevalence of tick infestation presented higher in summer, followed by autumn, spring and lower in winter as shown in Table 6. Similarly, prevalence of tick species infestation recorded the highest in July followed by June and August, respectively and the lowest one in December followed by January and February, respectively as shown in Fig. 3.
Fig. 3. Seasonal prevalence of ixodid ticks in three districts of KPK. The ticks were in abundance in summer, followed by autumn, spring and winter season, respectively in the studied districts. Month wise prevalence shows that tick prevalence was highest in July followed by August and June respectively and was lowest in December followed by November and October respectively.
Table 1. Prevalence of ixodid tick species in three districts of KPK, Pakistan
Tick species
|
Mardan n(%)
|
Kohat n(%)
|
Swat n(%)
|
Total n(%)
|
p-value
|
R.(B) microplus
|
156(97.50)
|
122(93.10)
|
55(38.51)
|
333(76.70)
|
0.000
|
R. (B) annulatus
|
110(68.81)
|
96(73.31)
|
97(67.80)
|
303(69.80)
|
0.577
|
R. (B) decoloratus
|
80(50.00)
|
70(53.41)
|
83(58.01)
|
233(53.70)
|
0.374
|
H. anatolicum
|
40(25.00)
|
81(61.81)
|
105(73.41)
|
226(52.10)
|
0.000
|
R. (B) turanicus
|
10(06.30)
|
0.00
|
40(28.01)
|
50(11.50)
|
0.000
|
Note: H. =Hyalomma, B. =Boophilus, R. =Rhipicephalus
Table 2. Ixodid tick species prevalence in cattle breeds
Tick species
|
Breed
|
Mardan n(%)
|
Kohat n(%)
|
Swat n(%)
|
Total n(%)
|
p-value
|
R. (B) microplus
|
Friesian
|
35(100.00)
|
14(82.40)
|
14(43.81)
|
63(75.00)
|
0.000
|
Crossbreed
|
66(95.71)
|
60(93.81)
|
22(31.90)
|
148(73.30)
|
0.000
|
Achai
|
45(100.00)
|
38(97.41)
|
14(42.42)
|
97(82.90)
|
0.000
|
Sahiwal
|
10(90.90)
|
10(90.91)
|
05(55.62)
|
25(80.60)
|
0.078
|
R. (B) annulatus
|
Friesian
|
24(68.60)
|
10(58.81)
|
23(71.92)
|
57(67.90)
|
0.644
|
Crossbreed
|
48(69.60)
|
45(70.31)
|
46(66.72)
|
139(68.80)
|
0.890
|
Achai
|
33(73.30)
|
31(79.51)
|
23(69.72)
|
87(74.40)
|
0.625
|
Sahiwal
|
05(45.50)
|
10(90.91)
|
05(55.61)
|
20(64.50)
|
0.067
|
R. (B) decoloratus
|
Friesian
|
20(57.10)
|
08(47.11)
|
22(68.81)
|
50(59.50)
|
0.315
|
Crossbreed
|
36(52.20)
|
29(45.30)
|
35(50.71)
|
100(49.50)
|
0.709
|
Achai
|
20(44.40)
|
25(64.11)
|
21(63.61)
|
66(56.40)
|
0.119
|
Sahiwal
|
04(36.41)
|
08(72.70)
|
05(55.61)
|
17(54.80)
|
0.230
|
H. anatolicum
|
Friesian
|
12(34.30)
|
08(47.11)
|
25(78.11)
|
45(53.60)
|
0.001
|
Crossbreed
|
12(17.41)
|
37(57.80)
|
49(71.00)
|
98(48.50)
|
0.000
|
Achai
|
14(31.11)
|
28(71.80)
|
26(78.81)
|
68(58.10)
|
0.000
|
Sahiwal
|
02(18.20)
|
08(72.71)
|
05(55.60)
|
15(48.40)
|
0.033
|
R. (B) turanicus
|
Friesian
|
10(28.60)
|
0.00
|
10(31.21)
|
20(23.80)
|
0.035
|
Crossbreed
|
0.00
|
0.00
|
16(23.20)
|
16(07.90)
|
0.000
|
Achai
|
0.00
|
0.00
|
09(27.30)
|
09(0 7.70)
|
0.000
|
Sahiwal
|
0.00
|
0.00
|
05(55.60)
|
05(16.10)
|
0.001
|
Table 3. Ixodid tick species prevalence according to the age of cattle
Tick species
|
Age
|
Mardan n(%)
|
Kohat n(%)
|
Swat n(%)
|
Total n(%)
|
p-value
|
R. (B) microplus
|
Young
|
34(100.00)
|
31(91.20)
|
15(46.91)
|
80(80.00)
|
0.000
|
Adult
|
122(96.80)
|
91(93.81)
|
40(36.00)
|
253(75.70)
|
0.000
|
R. (B) annulatus
|
Young
|
22(64.70)
|
26(76.51)
|
24(75.01)
|
72(72.00)
|
0.502
|
Adult
|
88(69.80)
|
70(72.22)
|
73(65.81)
|
231(69.20)
|
0.595
|
R. (B) decoloratus
|
Young
|
17(50.00)
|
17(50.01)
|
21(65.61)
|
55(55.00)
|
0.342
|
Adult
|
63(50.00)
|
53(54.61)
|
62(55.90)
|
178(53.30)
|
0.634
|
H. anatolicum
|
Young
|
09(26.51)
|
22(64.70)
|
24(75.02)
|
55(55.00)
|
0.000
|
Adult
|
31(24.61)
|
59(60.80)
|
81(73.01)
|
171(51.20)
|
0.000
|
R. (B) turanicus
|
Young
|
05(14.71)
|
0.00
|
12(37.50)
|
17(17.00)
|
0.000
|
Adult
|
05(04.01)
|
0.00
|
28(25.21)
|
33(09.90)
|
0.000
|
Table 4. Sex wise prevalence of ixodid tick species in cattle
Tick species
|
Sex
|
Mardan n(%)
|
Kohat n(%)
|
Swat n(%)
|
Total n(%)
|
p-value
|
R. (B) microplus
|
Male
|
48(100.00)
|
41(95.31)
|
17(43.62)
|
106(81.50)
|
0.000
|
Female
|
108(96.40)
|
81(92.00)
|
38(36.51)
|
227(74.70)
|
0.000
|
R. (B) annulatus
|
Male
|
35(72.91)
|
35(81.40)
|
30(76.92)
|
100(76.90)
|
0.632
|
Female
|
75(67.00)
|
61(69.31)
|
67(64.42)
|
203(66.80)
|
0.772
|
R. (B) decoloratus
|
Male
|
27(56.20)
|
24(55.81)
|
27(69.22)
|
78(60.00)
|
0.372
|
Female
|
53(47.30)
|
46(52.31)
|
56(53.81)
|
155(51.00)
|
0.606
|
H. anatolicum
|
Male
|
13(27.11)
|
30(69.81)
|
31(79.50)
|
74(56.90)
|
0.000
|
Female
|
27(24.11)
|
51(58.00)
|
74(71.22)
|
152(50.00)
|
0.000
|
R. (B) turanicus
|
Male
|
03(06.20)
|
0.00
|
13(33.31)
|
16(12.30)
|
0.000
|
Female
|
07(06.20)
|
0.00
|
27(26.00)
|
34(11.20)
|
0.000
|
Table 5. Sex ratio of ixodid tick species
S. No
|
Tick Species
|
Male
|
Female
|
M:F
|
Total
|
1
|
R. (B) microplus
|
200
|
133
|
1.50:1
|
333
|
2
|
R. (B) annulatus
|
198
|
105
|
1.89:1
|
303
|
3
|
R. (B) decoloratus
|
143
|
90
|
1.6:1
|
233
|
4
|
H. anatolicum
|
140
|
86
|
1.63:1
|
226
|
5
|
R. (B) turanicus
|
20
|
30
|
1:1.5
|
50
|
6
|
Total
|
701
|
444
|
1.74:1
|
1145
|
Table 6. Seasonal prevalence of ixodid tick species
Tick Species
|
Winter n(%)
|
Spring n(%)
|
Summer n(%)
|
Autumn n(%)
|
p-value
|
R. (B) microplus
|
24(07.20)
|
69(20.71)
|
130(39.00)
|
110(33.00)
|
0.000
|
R. (B) annulatus
|
13(04.30)
|
20(06.61)
|
150(49.51)
|
120(39.60)
|
0.002
|
R. (B) decoloratus
|
08(03.40)
|
15(06.41)
|
120(51.50)
|
90(38.60)
|
0.004
|
H. anatolicum
|
16(07.11)
|
40(17.70)
|
90(39.80)
|
80(35.40)
|
0.023
|
R. (B) turanicus
|
0.00
|
0.00
|
30(60.00)
|
20(40.00)
|
0.007
|
DISCUSSION
The results showed that Rhipicephalus (Boophilus) microplus was the most prevalent tick species followed by R. (B) annulatus, R. (B) decoloratus, H. anatolicum and the least prevalent was R. (B) turanicus species respectively over the studied districts. Similar study was done by Mustafa et al. (2014) who reported that there was higher prevalence in R. (B) microplus (22.59%) followed by R. (B) annulatus (17.15%) and H. anatolicum (9.03%). Farooqi et al. (2017), studied the prevalence of ixodid ticks in three temporal zones of Khyber Pakhtunkhwa (KPK) and found that R. (B) annulatus (41.67%) was the predominant tick followed by R. (B) microplus (18.42%), R. appendiculatus (8.25%) and R. decoloratus (6.83%). They observed that sex and age of the animal were significantly (p<0.05) associated with tick infestation which correlates with this study. A number of other researchers studied the prevalence of ixodid tick species in different regions of the world like Sajid et al. (2009), Telmadarraiy et al. (2010), Kabir et al. (2011), Atif et al. (2012), Asmaa et al. (2014), Mandloi et al. (2016), Tesgera et al. (2017), Shanan et al. (2017), Ghashghaei et al. (2017), Kaur et al. (2017), Silatsa et al. (2019), Ghafar et al. (2020) and Sidorenko et al. (2021) which coincide with this study.
The results showed that tick infestation was significantly associated (p<0.05) with age of the cattle among the studied districts of KPK. Young animals were affected more with tick species infestation than adults. These findings are in agreement with the studies conducted by Kabir et al. (2011), Dehuri et al. (2017) and Godara et al. (2018). However, the results of this study disagree with those of Manan et al. (2007) and Vatsya et al. (2007) according to whom tick infestation were more in adult than young cattle. Young cattle have less developed immune system as a result of less exposure to tick vectors and the farmers give more attention to adults and lactating animals than young animals are among the possible reasons for higher tick infestation in young cattle. On the other hand, justifications for above studies with higher prevalence of tick species infestation in adult than young animals can be ascribed to immune system less performant in adults due to poor body status and less hygienic conditions (Farooqi et al., 2017; Rony et al., 2010).
Sex of the animal is another important determinant of tick infestation. In this study there was higher prevalence of tick species infestation in male than female cattle. These findings are consistent with those of Sajid et al. (2009) and Musa et al. (2014) according to whom male cattle were infested more with tick species than female cattle. Female cattle are kept by farmers for milk production, so receive more attention than male which are kept for meat and drought purposes and receiving less attention is a justification of higher tick infestation in male than female cattle (Sajid et al., 2009). However, our results do not coincide with those reported by Rony et al. (2010), Kabir et al. (2011), Asmaa et al. (2014) and Tafesse and Amante (2019) who reported that male cattle are affected less with tick infestation than female.
In the current study, the results revealed that there was mixed tick species infestation in cattle breeds. Rhipicephalus (Boophilus) microplus, R. (B) annulatus and H. anatolicum infestations were higher in local breed (Achai) than exotic breeds. This study matches with the work done by Kabir et al. (2011) who reported higher tick infestations in local cattle (43.82%) than crossbred (24.13%). As the exotic breeds are used for higher milk and meat production, the farmers give more attention and care to these breeds than local breeds. So, this can be the reason for higher tick infestation in local than exotic breeds. On the other hand, Rhipicephalus (Boophilus) decoloratus and R. (B) turanicus tick species infestations were recorded higher in exotic breed (Friesian) than local breeds. This correlates with the findings of Sajid et al. (2009), Atif et al. (2012) and Farooqi et al. (2017). Justification for this higher tick infestation in exotic breeds is that indigenous breeds have developed better resistance than European breeds due to their constant exposure (Jongejan and Uilenberg, 2004; Sajid et al., 2009).
It was observed from the study that male ticks were higher in ratio than female ticks except R. (B) turanicus. This is in full agreement with Telmadarraiy et al. (2010) and Tadesse and Sultan (2014). The adult female ticks drop off to land after taking the blood meal and lay eggs while males remain attached for several months on host to start feeding, mating with other female ticks, mature and finally drop off to ground so males remain attached to host for longer time than female ticks. This fact could be the possible reason for male tick dominance than females as discussed in Gebre et al. (2001).
According to the seasonal prevalence of ticks it was clear from the results that the ticks were in abundance in summer, followed by autumn, spring and winter season respectively in the investigated districts. Tick number was higher in the month of July and was lower in December. The findings of this study correlate with Kumar et al. (2004), Islam et al. (2006), Vatsya et al. (2007), Sajid et al. (2009), Kabir et al. (2011), Mustafa et al. (2014), Asmaa et al. (2014), Negi and Arunachalam (2019) and Al-Mayah and Abdul-Karim (2020) who found similar results and justifications about the seasonal prevalence of tick infestations in animals during their studies. This higher prevalence of tick infestation in summer and autumn seasons could be assigned to higher temperature and humidity in environment due to heavy rains (rainy season) which favor the growth of ticks. Similarly, reason for lower number of ticks in winter season is the decreased temperature, dry weather and short- day which retard tick growth, while in spring season tick start increasing their number as the temperature increases (Sajid et al., 2009; Mustafa et al., 2014).
Conclusion: The study concludes that R. (B) microplus was the most prevalent tick species followed by R. (B) annulatus, R. (B) decoloratus, H. anatolicum and the least prevalent was R. turanicus species respectively among the studied districts of KPK province. Districts, breed, age and sex of cattle were found significantly (p<0.05) associated with tick infestation except R. (B) annulatus and R. (B) decoloratus. Tick prevalence was the highest in Achai and Friesian breeds, young stock and male animals. There was higher male tick ratio than female. Prevalence of tick species were at their peak during summer and rainy seasons and remained low during winter season.
Acknowledgement: The authors are thankful to Veterinary officers Dr. Saeed Khan, Dr. Shakeel and their staff for helping in collection of tick samples.
Authors Contributions: MAK and SHF helped in collection of tick samples. FAK, SM and MA helped in Lab work and drafting of the research article. IR, HA and AAS designed and supervised the study.
Statement of conflict of interest: The authors declared that they have no conflict of interest.
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