Systematic Review of Ticks and Tick-Borne Pathogens of Small Ruminants in Pakistan
Abstract
:1. Introduction
2. Methods
2.1. Review Protocol
2.2. Literature Search
2.3. Quality Assessment and Selection
2.4. Estimation of Prevalence
3. Results and Discussion
3.1. Studies on Ticks
3.1.1. Tick Species
3.1.2. Epidemiology of Ticks
3.1.3. Identification of Ticks
3.1.4. Control of Ticks in Small Ruminants
State(s) | District(s) | Host(s) | Tick(s) | Method(s) of Identification | % Infested Animals (Proportion; 95% Confidence Interval) | Reference |
---|---|---|---|---|---|---|
Khyber Pakhtunkhwa | Charsadda, Karak, Mardan, Lower Kohistan, Peshawar | Sheep | Haemaphysalis longicornis, Hyalomma impeltatum | Morphological | 16.3 (13/80; 8.2–24.3) | [23] |
Goats | Hae. montgomeryi, Hae. longicornis, Hy. impeltatum | 68.3 (82/120; 60.0–76.7) | ||||
Peshawar | Sheep | Dermacentor variabilis, Ixodes ricinus, Rhipicephalus simus, Otobius megnini | Molecular | Not provided | [42] | |
Goats | Rh. appendiculatus, Rh. microplus, Rh. simus | |||||
Bannu | Sheep | Not provided | Not performed | 7.8 (39/500; 5.4–10.2) | [43] | |
Goats | 10.2 (51/500; 7.5–12.9) | |||||
Bajaur, Khyber, Mohmand, Orakzai, North and South Waziristan | Sheep, Goats | Hae. sulcata, Hae. punctata, Hy. anatolicum, Hy. detritum, Hy. excavatum, Hy. scupense, Rh. microplus, Rh. sanguineus | Morphological | Not Provided | [21] | |
Karak | Sheep | Hy. marginatum, Rh. annulatus | Morphological | 26.7 (8/30; 10.8–42.5) | [44] | |
Goats | Hae. bispinosa, Rh. microplus, Rh. sanguineus | 20.0 (9/45; 8.3–31.7) | ||||
Dera Ismail Khan, Lakki Marwat | Sheep | Not provided | Not performed | 27.3 (9/33; 12.1–42.5) | [45] | |
Goats | Not provided | 23.1 (34/147; 16.3-29.9) | ||||
Peshawar | Sheep | Amblyomma, Boophilus, Haemaphysalis, Ixodes and Rhipicephalus species | Morphological | 66.7 (50/75; 56.0–77.3) | [46] | |
Goats | 73.7 (70/95; 64.8–82.5) | |||||
Bannu, Chitral, Dir, Mardan, Peshawar, Swat | Sheep | D. raskemensis, Hy. anatolicum, Hy. detritum, Rh. microplus, Rh. sanguineus | Morphological | Not provided | [47] | |
Goats | Hae. montgomeryi, Hy. anatolicum, Hy. marginatum turanicum, Rh. haemaphysaloides, Rh. microplus, Rh. sanguineus | |||||
Mansehra | Sheep | Rh. sanguineus | Morphological | Not provided | [48] | |
Goats | ||||||
Bajaur, Khyber, Mohmand, North Waziristan, Orakzai | Sheep | Hae. sulcata, Hy. anatolicum, Rh. microplus, Rh. turanicus | Morphological and molecular | Not provided | [22] | |
Goats | Hae. punctata, Hae. sulcata, Hy. anatolicum, Rh. haemaphysaloides, Rh. microplus, Rh. turanicus | |||||
Khyber Pakhtunkhwa and Gilgit-Baltistan | Astor, Diamer, Gilgit, Haripur, Kohistan, Mansehra, Shangala | Sheep | Hyalomma and Rhipicephalus spp. | Morphological | 81.5 (189/232; 76.5–86.5) | [49] |
Goats | 72.1 (263/365; 67.5–76.7) | |||||
Punjab | Attock, Bahawalpur, Bhakkar, Chakwal, Faisalabad, Gujranwala, Jhang, Khushab, Layyah, Muzaffargarh, Rajanpur, Rawalpindi | Sheep | Hy. anatolicum, Rh. appendiculatus, Rh. decolaratus, Rh. microplus, Rh. sanguineus | Morphological | 29.0 (812/2800; 27.3–30.7) | [25] |
Goats | Hy. anatolicum, Hy. dromedarii, Hy. marginatum, Rh. appendiculatus, Rh. decolaratus, Rh. microplus, Rh. sanguineus | 36.1 (1012/2800; 34.4–37.9) | ||||
Toba Tek Singh | Goats | Hy. anatolicum, Rh. microplus | Morphological | 6.7 (270/4020; 5.9–7.5) | [50] | |
Sargodha | Goats | Hy. anatolicum and Amblyomma, Haemaphysalis, Ixodes, and Rhipicephalus spp. | Morphological | 86.5 (1038/1200; 84.6–88.4) | [51] | |
Multan | Sheep | Hy. anatolicum, Hy. marginatum, Rh. sanguineus | Morphological | 68.0 (17/25; 49.7–86.3) | [52] | |
Goats | 40.0 (8/20; 18.5–61.5) | |||||
Multan | Sheep | Hae. punctata, Hy. anatolicum, Hy. excavatum | Morphological | 50.0 (100/200; 43.1–56.9) | [26] | |
Goats | Hy. excavatum, Rh. microplus | 40.8 (102/250; 34.7–46.9) | ||||
Attock, Bahawalpur, Gujranwala, Kasur, Khanewal, Multan, Okara, Rahim Yar Khan, Vehari | Sheep | Hy. anatolicum, Rh. microplus | Morphological and molecular | 11.1 (2/18; 1.3–34.7) | [19] | |
Goats | Hy. anatolicum, Hy. dromedarii, Rh. microplus, Rh. turanicus | 60.0 (48/80; 49.3–70.7) | ||||
Layyah, Muzaffargarh | Sheep | No ticks found | Morphological | 0.0 (0/1400; 0.0–0.2) | [24] | |
Goats | Hy. anatolicum, Rh. sanguineus | 51.6 (723/1400; 49.0–54.3) | ||||
Layyah, Muzaffargarh | Goats | Hy. anatolicum, Rh. sanguineus | Morphological | 60.1 (481/800; 56.7–63.5) | [53] | |
Lahore | Sheep | Boophilus, Hyalomma and Rhipicephalus spp. | Morphological | Not provided | [27] | |
Multan | Goats | Haemaphysalis and Rhipicephalus spp. | Morphological | 43.4 (201/463; 38.9–47.9) | [54] | |
Faisalabad, Jhang, Toba Tek Singh | Sheep | D. marginatus, Hy. anatolicum, Hy. marginatum isaaci, Rh. annulatus, Rh. microplus, Rh. sanguineus | Morphological | 18.8 (846/4500; 17.7–19.9) | [55] | |
Goats | Hy. aegyptium, Hy. anatolicum, Hy. marginatum isaaci, Rh. annulatus, Rh. microplus, Rh. sanguineus | 12.3 (553/4500; 11.3–13.2) | ||||
Lahore, Sheikhupura | Sheep | Hae. burnati, Hy. anatolicum, Rh. annulatus, Rh. microplus, Rh. sanguineus | Morphological | Not provided | [56] | |
Goats | ||||||
Punjab and Islamabad Capital Territory | Livestock experimental stations located in Attock and Islamabad Capital Territory | Sheep | Haemaphysalis and Rhipicephalus spp. | Morphological | 43.4 (95/219; 36.8–49.9) | [57] |
Goats | Amblyomma, Haemaphysalis, Ixodes and Rhipicephalus spp. | 41.5 (184/443; 36.9–46.1) | ||||
Balochistan | Harnai | Sheep | Hy. anatolicum, Hy. dromedarii, Rh. annulatus, Rh. microplus | Morphological | 30.0 (12/40; 15.8–44.2) | [58] |
Goats | Am. hebraeum, Hy. anatolicum, Hy. dromedarii, Rh. annulatus | 27.5 (11/40; 13.7–41.3) | ||||
Mustang and Quetta | Goats | Hy. anatolicum, Hy. excavatum, Rh. appendiculatus, Rh. microplus | Morphological | Not provided | [59] | |
Specimens collected from 26 districts (names not provided) | Sheep and Goats | Hae. flava, Hy. anatolicum | Morphological | Not provided | [60] | |
Harnai, Kalat, Killa Abdullah, Khuzdar, Lasbela, Loralai, Pishin, Quetta, Sherani, Sibi, Ziarat, Zhob | Sheep | Hy. anatolicum, Hy. dromedarii, Hy. excavatum, Hy. marginatum, Hy. scupense, Rh. microplus, Rh. turanicus | Morphological and molecular | Not provided | [61] | |
Goats | Hy. anatolicum, Hy. dromedarii, Hy. excavatum, Hy. marginatum | |||||
Sindh | Khairpur, Larkana, Sehwan, Thatta, Umerkot | Sheep | Hae intermedia, Hae kutchensis, Hae. bispinosa, Hy. anatolicum, Hy. bravepunctata, Hy. detritum, Hy. dromedarii, Hy. hussaini, Hy. impeltatum, Hy. marginatum isaaci, Hy. marginatum turanicum, Rh. annulatus, Rh. haemaphysaloides, Rh. microplus, Rh. sanguineus, Rh. turanicus | Morphological | Not provided | [62] |
Goats | ||||||
Khairpur | Goats | Hy. anatolicum, Hy. dromedarii, Hy. impeltatum, Hy. marginatum isaaci, Rh. haemaphysaloides, Rh. turanicus | Morphological | Not provided | [63] | |
Azad Jammu and Kashmir | Muzaffarabad | Sheep | Not provided | Not performed | 22.2 (2/9; 2.8–60.0) | [64] |
Goats | 46.3 (19/41; 31.1–61.6) | |||||
Poonch | Sheep | Haemaphysalis, Hyalomma and Otobius spp. | Morphological | 54.7 (82/150; 46.7–62.6) | [65] | |
Goats | 48.3 (145/300; 42.7–54.0) | |||||
Poonch | Sheep | Hy. anatolicum | Morphological | 54.7 (164/300; 49.0–60.3) | [66] | |
Goats | 48.0 (288/600; 44.0–52.0) | |||||
Azad Jammu and Kashmir, Balochistan, Gilgit Baltistan, Khyber Pakhtunkhwa, Punjab and Sindh | District information not provided | Sheep | Ar. persicus, Hae. bispinosa, Hae. cornupunctata, Hae kashmirensis, Hae. montomeryi, Hy. anatolicum, Hy. dromedarii, Hy. hussaini, Hy. isaaci, Hy. scupense, Or. tholozani, Rh. haemaphysaloides, Rh. microplus | Morphological | Not provided | [20] |
Goats | Same as above except Argas (Ar.) persicus absent | |||||
Azad Kashmir, Balochistan, Gilgit Baltistan, Khyber Pakhtunkhwa, Punjab and Sindh | Specimens were collected from 12 administrative divisions of West Pakistan and Azad Kashmir | Sheep | D. raskemensis, Hae. bispinosa, Hae. cornupunctata, Hae. kashmirensis, Hae. montgomeryi, Hae. sulcata, Hy. anatolicum, Hy. asiaticum, Hy. detritum, Hy. dromedarii, Hy. excavatum, Hy. kumari, Hy. marginatum isaaci, Hy. marginatum turanicum, Rh. annulatus, Rh. haemaphysaloides, Rh. microplus, Rh. sanguineus, Rh. turanicus | Morphological | Not provided | [41] |
Goats | Same species as above except Hy. excavatum and Rh. annulatus absent |
Ticks | Number of Species Reported | Selected References | |
---|---|---|---|
Hyalomma (Hy.) | Hy. anatolicum, Hy. asiaticum, Hy. bravepunctata, Hy. detritum, Hy. dromedarii, Hy. excavatum, Hy. hussaini, Hy. impeltatum, Hy. kumari, Hy. marginatum, Hy. marginatum isaaci, Hy. marginatum turanicum, Hy. scupense | 13 | [20,21,22,23,25,41,47,55] |
Rhipicephalus (Rh.) | Rh. annulatus, Rh. appendiculatus, Rh. decolaratus, Rh. haemaphysaloides, Rh. microplus, Rh. sanguineus, Rh. simus, Rh. turanicus | 8 | [20,21,22,25,41,47,55] |
Haemaphysalis (Hae.) | Hae. burnati, Hae. bispinosa, Hae. cornupunctata, Hae. flava, Hae. intermedia, Hae. kashmirensis, Hae. kutchensis, Hae. longicornis, Hae. montgomeryi, Hae. punctata, Hae. sulcata | 11 | [20,21,22,23,41,47] |
Other ixodids and argasids | Amblyomma hebraeum, Dermacentor marginatus, D. variabilis, D. raskimensis, Ixodes ricinus, Ar. persicus, Otobius megnini, Ornithodoros tholozani | 8 | [20,41,47,55] |
Tick-Borne Pathogens | |||
Anaplasma (A.) | A. centrale, A. marginale, A. ovis | 3 | [22,86,87] |
Babesia (B.) | B. ovis | 1 | [28,88] |
Theileria (T.) | T. annulata, T. luwenshuni, T. ovis, T. lestoquardi, T. sp. MK, T. sp. OT1 | 6 | [27,89] |
Rickettsia (R.) | Candidatus R. amblyommii, R. aeschlimannii, R. conorii, R. massiliae, R. slovaca, | 5 | [20,22] |
Other pathogens | Coxiella burnetii, Crimean-Congo haemorrhagic fever virus | 2 | [32,34,35] |
Study Type | Drug(s) Tested (Concentration/Dose/Method of Application) | Number of Animals per Group | Duration of Trial (Days) | Efficacy (%) | Reference | ||
---|---|---|---|---|---|---|---|
Sheep | Goats | Sheep | Goats | ||||
Acaricidal efficacy against ticks | Diazinon (0.6% spray) | 20 | 20 | 56 | 89.5 | 92 | [48] |
Coumaphos (0.1% spray) | 20 | 20 | 93.6 | 95 | |||
Cypermethrin (2% spray) | 20 | 20 | 100 | 100 | |||
Ivermectin (0.2 mg/kg, injection) | NS | 90 | 20 | NA | No | [53] | |
Cypermethrin (5% spray) | 90 | Yes | |||||
Drug efficacy against anaplasmosis | Oxytetracycline (1 mL/kg, injection) | NS | 10 | 30 * | NA | 30 | [98] |
Imidocarb dipropionate (0.1/kg, injection) | 10 | 80 | |||||
Diminazene aceturate (0.3 mL/kg, injection) | 10 | 60 | |||||
Oxytetracycline (20 mg/kg, injection) | 4 | 4 | 10 | 100 | 100 | [87] | |
Imidocarb dipropionate (3 mg/kg, injection) | 4 | 4 | 100 | 87.5 | |||
Diminazene aceturate (3.5–7 mg/kg, injection) | 4 | 4 | 50 | 75 | |||
Drug efficacy against babesiosis | Imidocarb dipropionate + oxytetracycline (2 mg/kg + 10 mg/kg, injection) | 10 | 10 | 10 | 100 | 100 | [99] |
Imidocarb dipropionate (2 mg/kg, injection) | 10 | 10 | 80 | 80 | |||
Diminazene aceturate + oxytetracycline (3.5 mg/kg + 10 mg/kg, injection) | 10 | 10 | 80 | 90 | |||
Diminazene aceturate (3.5 mg/kg, injection) | 10 | 10 | 70 | 70 | |||
Imidocarb dipropionate (2 mg/kg, injection) | 10 | NS | 10 | 100 | NA | [100] | |
Diminazene aceturate (3.5 mg/kg, injection) | 10 | 80 |
3.2. Tick-Borne Pathogens in Pakistani Small Ruminants and Their Ticks
3.2.1. Anaplasmosis
3.2.2. Babesiosis
3.2.3. Theileriosis
3.2.4. Other Tick-Borne Diseases (TBDs) of Small Ruminants
3.2.5. Diagnosis and Control of TBPs in Pakistan
State | District(s) | Host(s)/Vector | Method(s) of Detection | Target Animal Population | Pathogen(s) Detected | % Test-Positive (Proportion; 95% CI) | Reference |
---|---|---|---|---|---|---|---|
Punjab | Lahore | Sheep | Morphological | Suspected of anaplasmosis | Anaplasma ovis | 55.3 (83/150; 47.4–63.3) | [87] |
Goats | 30.7 (46/150; 23.3–38.0) | ||||||
Mianwali | Sheep | Molecular | Healthy | Anaplasma species | 32.0 (24/75; 21.4–42.6) | [106] | |
Goats | 25.3 (19/75; 15.5–35.2) | ||||||
Sheep and goats | Morphological | 29.3 (44/150; 22.0–36.6) | |||||
Attock, Bahawalpur, Gujranwala, Kasur, Khanewal, Multan, Okara, Rahim Yar Khan, Vehari | Ticks from sheep and goats | Molecular | Healthy | A. ovis, A. centrale, A. marginale, A. platys-like organism, Anaplasma sp. BL099-6 | 38.9 (21/54; 26.2–53.1) | [86] | |
Khyber Pakhtunkhwa | Charsadda, Mardan, Nowshera, Peshawar | Sheep | Morphological | Suspected of anaplasmosis | Anaplasma sp. | 29.6 (32/108; 21.0–38.2) | [107] |
Goats | 1.7 (1/60; 0.0–8.9) | ||||||
Karak | Sheep | Morphological | Suspected of anaplasmosis | A. marginale | 22.0 (55/250; 16.9–27.1) | [29] | |
Goats | 17.2 (43/250; 12.5–21.9) | ||||||
Sheep | Serological * | 36.8 (92/250; 30.8–42.8) | |||||
Goats | 32.8 (82/250; 27.0–38.6) | ||||||
Sheep | Molecular | 47.2 (118/250; 41.0–53.4) | |||||
Goats | 34.8 (87/250; 28.9–40.7) | ||||||
Peshawar | Sheep | Serological | Healthy | A. marginale | 24.5 (92/376; 20.1–28.8) | [108] | |
Charsadda | Sheep | Serological | Healthy | Anaplasma sp. | 19.3 (58/300; 14.9–23.8) | [109] | |
Goats | 25.0 (75/300; 20.1–29.9) | ||||||
District information not provided | Goats | Morphological | Healthy | A. ovis | 9.6 (7/73; 2.8–16.3) | [110] | |
Mardan | Sheep | Morphological | Healthy | Anaplasma sp. | 13.9 (25/180; 8.8–18.9) | [111] | |
Goats | 8.3 (15/180; 4.3–12.4) | ||||||
Sheep | Serological | 23.9 (43/180; 17.7–30.1) | |||||
Goats | 20.6 (37/180; 14.7–26.5) | ||||||
Bajaur, Khyber, Mohmand, North Waziristan, Orakzai | Ticks from sheep | Molecular | Healthy | A. centrale, A. marginale, A. ovis | 39.1 (9/23; 19.2–59.1) | [22] | |
Ticks from goats | 35.5 (11/31; 18.6–52.3) | ||||||
Peshawar | Sheep | Morphological and molecular | Suspected of anaplasmosis | Anaplasma sp. | 28.0 (28/100; 19.2–36.8) | [112] | |
Sindh | Mirpur Khas | Goats | Morphological | Healthy | A. marginale | 13.3 (40/300; 9.5–17.2) | [98] |
State(s) | District(s) | Host(s)/Ticks | Method(s) of Detection | Target Animal Population | Pathogen(s) Detected | % Test-Positive (Proportion; 95% CI) | Reference |
---|---|---|---|---|---|---|---|
Punjab | Lahore | Sheep | Morphological | Suspected of piroplasmosis | Theileria sp. | 22.0 (44/200; 16.3–27.7) | [27] |
Molecular | Theileria ovis | 27.5 (55/200; 21.3–33.7) | |||||
T. lestoquardi | 7.5 (15/200; 3.8–11.2) | ||||||
Ticks from sheep | Not applicable | T. ovis | 65.9 (27/41; 51.3-80.4) | ||||
T. lestoquardi | 66.7 (30/45; 52.9-80.4) | ||||||
Bahawalnagar, Dera Ghazi Khan, Layyah, Multan, Muzaffargarh | Sheep | Molecular | Healthy | T. lestoquardi | 8.2 (4/49; 0.5-15.8) | [125] | |
Goats | 0.0 (0/66; 0.0-5.4) | ||||||
Lahore | Sheep | Morphological | Suspected of piroplasmosis | Babesia sp. | 23.5 (57/243; 18.1–28.8) | [99] | |
Goats | 13.5 (51/377; 10.1–17.0) | ||||||
Bahawalnagar, Dera Ghazi Khan, Khanewal, Layyah, Multan, Muzaffargarh, Vehari | Sheep | Molecular | Healthy | Babesia ovis | 50.0 (20/40; 34.5–65.5) | [118] | |
Goats | 23.9 (16/67; 13.7–34.1) | ||||||
Lahore | Sheep | Morphological | Suspected of piroplasmosis | Theileria sp. | 13.9 (38/273; 9.8–18.0) | [123] | |
Goats | 8.2 (21/256; 4.8–11.6) | ||||||
Sahiwal | Sheep | Morphological | Healthy | Babesia sp. | 9.7 (30/310; 6.4–13.0) | [100] | |
Multan | Sheep and goats | Morphological | Healthy | Theileria sp. | 3.7 (11/300; 1.5–5.8) | [126] | |
Sheep | Molecular | T. ovis | 15.3 (23/150; 9.6–21.1) | ||||
T. lestoquardi | 10.7 (16/150; 5.7–15.6) | ||||||
Goats | T. ovis | 5.3 (8/150; 2.5–10.6) | |||||
T. lestoquardi | 4.0 (6/150; 1.6–8.9) | ||||||
Multan | Sheep and goats | Morphological | Healthy | Theileria sp. | 12.4 (31/250; 8.3–16.5) | [127] | |
Sheep | Molecular | 16.0 (25/156; 10.3–21.8) | |||||
Goats | 69.1 (65/94; 59.8–78.5) | ||||||
Attock, Bahawalpur, Gujranwala, Kasur, Khanewal, Multan, Okara, Rahim Yar Khan, Vehari | Ticks from sheep and goats | Molecular | Healthy | Babesia and Theileria spp. | Not provided | [86] | |
Multan | Sheep and goats | Morphological | Healthy | Theileria sp. | 12.5 (25/200; 7.9–17.1) | [128] | |
Molecular | 39.5 (79/200; 32.7–46.3) | ||||||
Livestock Experimental Stations, Okara | Sheep | Morphological | Healthy | B. ovis | 29.0 (58/200; 22.7–35.3) | [28] | |
T. ovis | 37.0 (74/200; 30.3–43.7) | ||||||
Molecular | B. ovis | 55.0 (110/200; 48.1–61.9) | |||||
T. ovis | 7.5 (15/200; 3.8–11.2) | ||||||
Multan | Goats | Morphological | Healthy | Theileria | 5.4 (25/463; 3.3–7.5) | [54] | |
Molecular | T. ovis, T. lestoquardi | 16.0 (74/463; 12.6–19.3) | |||||
Okara | Sheep | Morphological | Healthy | Theileria sp. | 16.5 (66/400; 12.9–20.1) | [129] | |
Punjab and Islamabad Capital Territory | Livestock Experimental Stations located at Attock and Islamabad Capital Territory | Sheep | Morphological | Healthy | Theileria sp. | 7.4 (7/95; 2.1–12.6) | [57] |
Goats | 3.8 (7/184; 1.0–6.6) | ||||||
Punjab and Khyber Pakhtunkhwa | Kohat, Multan | Sheep | Molecular | Healthy | Theileria sp. | 31.7 (26/82; 21.6–41.8) | [88] |
Goats | 5.3 (6/114; 1.2–9.4) | ||||||
Multan | Sheep and goats | 5.5 (7/128; 1.5–9.4) | |||||
Kohat | 34.7 (25/72; 23.7–45.7) | ||||||
Dera Ghazi Khan, Kohat, Layyah, Multan, Rahim Yar Khan | Sheep | Molecular | Healthy | T. ovis | 11.1 (11/99; 4.9–17.3) | [130] | |
Goats | 0.9 (1/111; 0.0–4.9) | ||||||
Sheep and goats | Morphological | 1.0 (2/210; 0.1–3.4) | |||||
Dera Ghazi Khan, Layyah, Multan, Rahim Yar Khan | Molecular | 1.7 (2/118; 0.3–6.6) | |||||
Kohat | 10.9 (10/92; 4.5–17.2) | ||||||
Khyber Pakhtunkhwa | Charsadda, Mardan, Nowshera, Peshawar | Sheep | Morphological | Suspected of piroplasmosis | Theileria sp. | 15.7 (17/108; 8.9–22.6) | [107] |
Babesia sp. | 14.8 (16/108; 8.1–21.5) | ||||||
Goats | Theileria sp. | 0.0 (0/60; 0.0–7.5) | |||||
Babesia sp. | 41.7 (25/60; 29.2–54.1) | ||||||
Lower Dir | Sheep | Molecular | Healthy | T. annulata, T. luwenshuni, T. ovis, Theileria sp. MK, Theileria sp. OT1 | 72.5 (58/80; 62.7–82.3) | [89] | |
Goats | 40.8 (49/120; 32.0–49.6) | ||||||
Kohat, Peshawar | Sheep | Molecular | Healthy | T. lestoquardi | 4.5 (2/44; 0.6–15.5) | [131] | |
Goats | 2.5 (3/121; 0.5–7.0) | ||||||
Khyber, Peshawar | Sheep | Morphological | Healthy | Babesia sp. | 7.0 (21/300; 4.1–9.9) | [132] | |
Goats | Theileria sp. | 6.0 (18/300; 3.3–8.7) | |||||
Bannu, Dera Ismail Khan, Tank | Goats | Molecular | Healthy | Theileria ovis | 9.0 (54/600; 6.7–11.3) | [31] | |
T. lestoquardi | 5.3 (32/600; 3.5–7.1) | ||||||
Bannu, Dera Ismail Khan, Tank | Sheep | Morphological | Healthy | Theileria sp. | 20 (120/600; 16.8–23.2) | [133] | |
Mansehra | Ticks from sheep | Morphological | Not applicable | B. ovis | 1.5 (3/200; 0.3–4.3) | [48] | |
Ticks from goats | 1.0 (2/201; 0.1–3.5) | ||||||
Bannu, Dera Ismail Khan, Tank | Sheep | Molecular | Healthy | T. ovis | 13.0 (78/600; 10.3–15.7) | [30] | |
T. lestoquardi | 9.0 (54/600; 6.7–11.3) | ||||||
Bajaur, Khyber, Mohmand, North Waziristan, Orakzai | Ticks from sheep | Molecular | Healthy | Theileria sp. | 30.4 (7/23; 11.6–49.2) | [22] | |
Ticks from goats | 35.5 (11/31; 18.6–52.3) | ||||||
Ticks from sheep | B. ovis | 0.0 (0/23; 0.0–17.8) | |||||
Ticks from goats | 0.0 (0/31; 0.0–13.7) | ||||||
Balochistan | Loralai, Quetta | Sheep | Morphological and molecular | Healthy | T. ovis | 5.5 (120/2200; 4.5–6.4) | [134] |
T. lestoquardi | 15.4 (338/2200; 13.9–16.9) | ||||||
Goats | T. ovis | 6.7 (45/670; 4.8–8.6) | |||||
T. lestoquardi | 3.0 (20/670; 1.7–4.3) |
State | District(s) | Host(s) | Method(s) of Detection | Target Animal Population | Pathogen(s) Detected | % Test-Positive (Proportion; 95% CI) | Reference |
---|---|---|---|---|---|---|---|
Punjab | Bahawalpur, Bhakkar, Khanewal, Khushab, Layyah, Okara, Rajanpur | Sheep | Serological (ELISA) | Healthy | Coxiella burnetti (antibodies) | 15.6 (78/500; 12.4–18.8) | [34] |
Goats | 15.0 (75/500; 11.9–18.1) | ||||||
Ticks from sheep | Molecular (qPCR) | Coxiella burnetti (DNA) | 31.0 (9/29; 14.2–47.9) | ||||
Ticks from goats | 7.7 (2/26; −2.6–17.9) | ||||||
Layyah, Muzaffargarh | Sheep | Serological (ELISA) | Healthy | C. burnetti (antibodies) | 33.2 (90/271; 27.6–38.8) | [33] | |
Goats | 28.4 (77/271; 23.0–33.8) | ||||||
Attock, Chakwal, DG Khan, Faisalabad, Gujranwala, Lahore, Sahiwal, Sargodha, Sheikhupur | Sheep | Serological (ELISA) | Healthy | C. burnetti (antibodies) | 17.9% (33/184; 12.4–23.5) | [136] | |
Goat | 16.4% (46/280; 12.1–20.8) | ||||||
Khyber Pakhtunkhwa | Bajaur, Khyber, Mohmand, North Waziristan Orakzai | Ticks from sheep | Molecular (qPCR) | Not applicable | Rickettsia (DNA) | 73.9 (71/23; 56.0–91.9) | [22] |
Ehrlichia (DNA) | 8.7 (2/23; 1.1–22.0) | ||||||
Francisella-like (DNA) | 30.4 (7/23; 11.6–49.2) | ||||||
Coxiella-like (DNA) | 8.7 (2/23; 1.1–22.0) | ||||||
Ticks from goats | Rickettsia (DNA) | 83.9 (26/31; 70.9–96.8) | |||||
Ehrlichia (DNA) | 3.2 (1/31; 0.0–16.7) | ||||||
Francisella-like (DNA) | 16.1 (5/31; 3.2–29.1) | ||||||
Coxiella-like (DNA) | 6.5 (2/31; 1.1–22.8) | ||||||
Balochistan | Harnai, Kalat, Killa Abdullah, Khuzdar, Lasbela, Loralai, Pishin, Quetta, Sherani, Sibi, Ziarat, Zhob | Ticks from sheep and goats | Molecular (qPCR) | Not applicable | Crimean-Congo haemorrhagic fever Virus (DNA) | 3.8 (20/525; 2.2–5.4) | [61] |
Harnai, Kalat, Killa Abdullah, Khuzdar, Lasbela, Loralai, Pishin, Quetta, Sherani, Sibi, Ziarat, Zhob | Sheep | Serological (ELISA and IFA) and molecular | Healthy | CCHF virus (antibodies) | 18.6 (149/800; 15.9–21.3) | [35] | |
Goats | 4.6 (37/800; 3.2–6.1) | ||||||
Sindh | Karachi | Sheep | Serological (CFT) | Not applicable | C. burnetti (antibodies) | 18.3 (11/60; 8.5–28.1) | [135] |
Goats | 4.6 (3/65; 1.0–12.9) | ||||||
Punjab, Sindh, Khyber Pakhtunkhwa, and Balochistan | District information not provided | Sheep | Serological (ELISA) | Healthy | CCHF virus (antigen) | 32.5 (138/424; 28.1–37.0) | [32] |
Goats | 18.9 (83/440; 15.2–22.5) | ||||||
Azad Jammu and Kashmir, Balochistan, Gilgit Baltistan, Khyber Pakhtunkhwa, Punjab and Sindh | District information not provided | Ticks from sheep and goats | Next-Generation Sequencing | Not applicable | Several bacterial species (DNA) | Not provided | [20] |
4. Conclusions and Future Perspectives
Author Contributions
Funding
Conflicts of Interest
References
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Ghafar, A.; Abbas, T.; Rehman, A.; Sandhu, Z.-u.-D.; Cabezas-Cruz, A.; Jabbar, A. Systematic Review of Ticks and Tick-Borne Pathogens of Small Ruminants in Pakistan. Pathogens 2020, 9, 937. https://doi.org/10.3390/pathogens9110937
Ghafar A, Abbas T, Rehman A, Sandhu Z-u-D, Cabezas-Cruz A, Jabbar A. Systematic Review of Ticks and Tick-Borne Pathogens of Small Ruminants in Pakistan. Pathogens. 2020; 9(11):937. https://doi.org/10.3390/pathogens9110937
Chicago/Turabian StyleGhafar, Abdul, Tariq Abbas, Abdul Rehman, Zia-ud-Din Sandhu, Alejandro Cabezas-Cruz, and Abdul Jabbar. 2020. "Systematic Review of Ticks and Tick-Borne Pathogens of Small Ruminants in Pakistan" Pathogens 9, no. 11: 937. https://doi.org/10.3390/pathogens9110937