Platelet Indices and Hemoglobin, Albumin, Lymphocyte, and Platelet (HALP) Score Alterations in Sheep with Molecularly Confirmed Theileria spp. Infection
,
Abstract
Background: The hemoglobin (Hb), albumin (ALB), lymphocyte (LYM), and platelet (PLT) components of the HALP score, a human-derived immune-nutritional index, are currently being investigated in the veterinary field. We aimed to evaluate and compare the HALP score and platelet indices (PI) in Theileria-infected and non-infected sheep.
Methods: One hundred sheep from different farms in Semnan Province were screened for the presence of Theileria between June and August 2023 using microscopy and molecular-based methods. Hematocrit (Hct), Hb, red blood cell (RBC), LYM, PLT, plateletcrit (PCT), mean platelet volume (MPV), platelet distribution width (PDW), and ALB were measured. The HALP score was calculated by multiplying Hb in ALB by LYM and dividing by PLT.
Results: Microscopic and PCR analyses identified 21 and 27 positive samples for Theileria species, respectively. Results showed T. ovis in 52%, T. lestoquardi in 26%, T. annulata in 11%, and a co-infection of T. ovis and T. lestoquardi in 11% of the samples. The PLT and PCT showed significant differences in sheep infected with T. lestoquardi. A significant difference was also observed in PDW between sheep infected with T. ovis and T. lestoquardi compared to those infected with T. annulata. Statistical differences in the HALP score were noted for T. lestoquardi (P = 0.03), T. annulata (P = 0.01), and co-infections of T. ovis and T. lestoquardi (P = 0.05) versus T. ovis.
Conclusion: PLT indices (PI) and HALP scores can improve diagnostic processes, and future studies should use them alongside other methods for diagnosing Theileria species.
1. Almazan C, Scimeca RC, Reichard MV, Mosqueda J. Babesiosis and theileriosis in North America. Pathogens. 2022;11(2):168.
2. Zhang J, Kelly P, Li J, Xu C, Wang C. Molecular detection of Theileria spp. in livestock on five Caribbean islands. Biomed Res Int. 2015;2015:624728.
3. Rashid M, Akbar H, Rashid I, et al. Economic significance of tropical theileriosis on a Holstein Friesian dairy farm in Pakistan. J Parasitol. 2018;104(3):310-12.
4. Abdigoudarzi M. Detection of naturally infected vector ticks (Acari: Ixodidae) by different species of Babesia and Theileria agents from three different enzootic parts of Iran. J Arthropod Borne Dis. 2013;7(2):164-72.
5. Zaeemi M, Haddadzadeh H, Khazraiinia P, Kazemi B, Bandehpour M. Identification of different Theileria species (T. lestoquardi, T. ovis, and T. annulata) in naturally infected sheep using nested PCR–RFLP. Parasitol Res. 2011;108(4):837-43.
6. Tageldin MH, Fadiya AA-K, Sabra AA-Y, Ismaily SIA-I. Theileriosis in sheep and goats in the Sultanate of Oman. Trop Anim Health Prod. 2005;37(6):491-93.
7. Yaghfoori S, Mohri M, Razmi G. Experimental Theileria lestoquardi infection in sheep: Biochemical and hematological changes. Acta Trop. 2017;173:55-61.
8. Razmi G, Yaghfoori S, Mohri M, Haghparast A, Tajeri S. The haematological, proinflammatory cytokines and IgG changes during an ovine experimental theileriosis. Onderstepoort J Vet Res. 2019;86(1):e1-6.
9. Baghshani H, Razmi GR, Yaghfoori S, Dezaki AA. Investigation of selected biochemical parameters in sheep naturally infected with theileriosis. Comp Clin Path. 2012;21(6):1417-20.
10. Yaghfoori S, Razmi GR, Mohri M, Razavizadeh ART, Movassaghi AR. An experimental ovine theileriosis: The effect of Theileria lestoquardi infection on cardiovascular system in sheep. Acta Trop. 2016;161:55-61.
11. Sonmez O, Sonmez M. Role of platelets in immune system and inflammation. Porto Biomed J. 2017;2(6):311–14.
12. Chen XL, Xue L, Wang W, et al. Prognostic significance of the combination of preoperative hemoglobin, albumin, lymphocyte and platelet in patients with gastric carcinoma: a retrospective cohort study. Oncotarget. 2015;6(38):41370–82.
13. Mahmoud MHS, Al-Dhalimy AMB, Al-Dujaily AH. Study of hematological and biochemical changes in sheep and goats infected with theileriosis at Al-Najaf province, Iraq. Biochem Cell Arch. 2019;19(1):803–06.
14. Habela M, Reina D, Niecto C, Navarrete I. Theileria ovis in Extremadura, Spain. Study of pathogenicity. Rev Iber Parasitol. 1989;49(2):117.
15. Al-Fahdi A, Alqamashoui B, Al-Hamidhi S, et al. Molecular surveillance of Theileria parasites of livestock in Oman. Ticks Tick Borne Dis. 2017;8(5):741–48.
16. Mans BJ, Pienaar R, Latif AA. A review of Theileria diagnostics and epidemiology. Int J Parasitol Parasites Wildl. 2015;4(1):104–18.
17. Fattahi R, Shayan P, Ebrahimzadeh E, Amininia N. Differential Diagnosis of Theileria lestoquardi, Theileria ovis and Theileria annulata in Sheep, Using Molecular Method, PCR. J Vet Res. 2020;75(1):8-16.
18. Shayan P, Jafari S, Fattahi R, Ebrahimzade E, Amininia N, Changizi E. Identification and characterization of Theileria ovis surface protein (ToSp) resembled TaSp in Theileria annulata. Parasitol Res. 2016;115(5):1893–99.
19. Al-Saadi M. Quantification of acute and chronic theileriosis in sheep by quantitative PCR (qPCR). Arch Razi Inst. 2023;78(1):389.
20. Nagore D, García-Sanmartín J, García-Pérez AL, Juste RA, Hurtado A. Identification, genetic diversity and prevalence of Theileria and Babesia species in a sheep population from Northern Spain. Int J Parasitol. 2004;34(9):1059–67.
21. El Imam AE, Hassan SM, Gameel AA, El Hussein AM, Taha KM, Oosthuizen MC. Molecular identification of different Theileria and Babesia species infecting sheep in Sudan. Ann Parasitol. 2016;62(1):47-52.
22. Saeed S, Jahangir M, Fatima M, et al. PCR-based detection of Theileria lestoquardi in apparently healthy sheep and goats from two districts in Khyber Pukhtoon Khwa (Pakistan). Vet Med Int. 2015; 32(2):225-32.
23. Altay K, Dumanli N, Holman PJ, Aktas M. Detection of Theileria ovis in naturally infected sheep by nested PCR. Vet Parasitol. 2005;127(2):99–104.
24. Soosaraei M, Haghi MM, Etemadifar F, et al. Status of theileriosis among herbivores in Iran: A systematic review and meta-analysis. Vet World. 2018;11(3):332–41.
25. Zarei F, Ganjali M, Nabavi R. Identification of Theileria species in sheep and vector ticks using PCR method in Zabol, Eastern Iran. J Arthropod Borne Dis. 2019;13(1):76.
26. Jalali SM, Khaki Z, Kazemi B, Rahbari S, Shayan P, Bandehpour M, Yasini SP. Molecular detection and identification of Theileria species by PCR-RFLP method in sheep from Ahvaz, Southern Iran. Iran J Parasitol. 2014;9(1):99.
27. Habibi G, Mehrabadi MHF, Fathi S, Esmaeilnia K, Shahedi A, Yazdani F, Afshari A. Detection of Babesia spp. and Theileria spp. in sheep across diverse provinces of Iran. Vet Parasitol Reg Stud Rep. 2024;56:101131.
28. Motavallihaghi S, Fakhar M, Sharbatkhori M, Paghe AS. First molecular evidence of Theileria lestoquardi in small ruminants in northern Iran. Ann Parasitol. 2022;68(3): 531-536.
29. Ashley LA, Hackner SG, Prittie J. Clinical management of canine babesiosis. J Vet Emerg Crit Care. 2012;22(1):77–89.
30. Garcia ATC. Piroplasma infection in dogs in northern Spain. Vet Parasitol. 2006;138(1-2):97–102.
31. Harrus S, Waner T. Diagnosis of canine monocytotropic ehrlichiosis (Ehrlichia canis): An overview. Vet J. 2011;187(3):292–6.
32. Solano-Gallego L, Baneth G. Babesiosis in dogs and cats – expanding parasitological and clinical spectra. Vet Parasitol. 2011;181(1):48–60.
33. Rosa CT, Pazzi P, Nagel S, McClure V, Christie J, Troskie M, Dvir E. Theileriosis in six dogs in South Africa and its potential clinical significance: clinical communication. J S Afr Vet Assoc. 2014;85(1): 1114.
34. Snarska A, Pomianowski A, Krystkiewicz W, Sobiech P, Lew S, Bednarek D. Influence of invasion of intracellular parasites on platelet response in dogs based on clinical cases. J Vet Res. 2012; 56:519–23.
35. Noori Alavije H, Ahmadi-Hamedani M, Moslemi H. Evaluation of platelet indices and mean platelet volume to platelet count ratio in experimentally varicocele-induced adolescent and adult rats. Andrologia. 2022;54(3):e14345.
36. Majumdar A, Kumar A, Biswas S. Automated complete blood count profile as a probable indicator of dengue fever severity in children. J Sci Soc. 2022;49(3):186–9.
37. Sontakke RA, Aglave NR, Dua H. Correlation of platelet parameters with the severity of thrombocytopenia in dengue fever in children aged less than 18 years at a tertiary care center: a cross-sectional study. Cureus. 2024;16(3):e56829.
38. Mohr R, Martinowitz U, Golan M, Ayala L, Goor DA, Ramot B. Platelet size and mass as an indicator for platelet transfusion after cardiopulmonary bypass. Circulation. 1986;74(1):153.
39. Van der Lelie J, Von dem Borne AEG. Platelet volume analysis for differential diagnosis of thrombocytosis. J Clin Pathol. 1986;39(2):129-133.
40. Ustundag Budak Y, Polat M, Huysal K. The use of platelet indices, plateletcrit, mean platelet volume and platelet distribution width in emergency non-traumatic abdominal surgery: a systematic review. Biochem Med (Zagreb). 2016;26(2):178–93.
41. Abdullah SH, Dyary HO, Saeed NM. Molecular detection of Theileria spp. in native sheep and estimation of hemato-biochemical parameters from Sulaimani province/Iraq. Front Vet Sci. 2022;9:1059599.
42. Ullah N, Durrani AZ, Ullah S, et al. Study on potential factors and physiological biomarkers associated with the occurrence of ovine theileriosis. Small Rumin Res. 2018;168:32–8.
43. Shah S, Khan M, Rahman H. Epidemiological and hematological investigations of tick-borne diseases in small ruminants in Peshawar and Khyber Agency, Pakistan. J Adv Parasitol. 2017;4(1):15–22.
44. Nazifi S, Razavi S, Kianiamin P, Rakhshandehroo E. Evaluation of erythrocyte antioxidant mechanisms: antioxidant enzymes, lipid peroxidation, and serum trace elements associated with progressive anemia in ovine malignant theileriosis. Parasitol Res. 2011;109(1):275–81.
45. Al-Hamidhi S, Elshafie EI, Yaghfoori S, et al. Comparative study of single Theileria lestoquardi and mixed infections with Theileria ovis. Parasit Vectors. 2021;14(1):370.
46. Shahzad S, Tipu M, Aslam A, et al. Comparative hemato-biochemical study on theileriosis in naturally infected Punjab Urial (Ovis vignei punjabiensis) and domestic sheep (Ovis aries) in Pakistan. J Anim Plant Sci. 2015;25(2):472–76.
47. Col R, Uslu U. Changes in selected serum components in cattle naturally infected with Theileria annulata. Bull Vet Inst Pulawy. 2007;51(1):15–18.
48. Homer MJ, Aguilar-Delfin I, Telford SR 3rd, Krause PJ, Persing DH. Babesiosis. Clin Microbiol Rev. 2000;13(3):451–69.
49. Antar R, Farag C, Xu V, Drouaud A, Gordon O, Whalen MJ. Evaluating the baseline hemoglobin, albumin, lymphocyte, and platelet (HALP) score in the United States adult population and comorbidities: an analysis of the NHANES. Front Nutr. 2023;10:1206958.
2. Zhang J, Kelly P, Li J, Xu C, Wang C. Molecular detection of Theileria spp. in livestock on five Caribbean islands. Biomed Res Int. 2015;2015:624728.
3. Rashid M, Akbar H, Rashid I, et al. Economic significance of tropical theileriosis on a Holstein Friesian dairy farm in Pakistan. J Parasitol. 2018;104(3):310-12.
4. Abdigoudarzi M. Detection of naturally infected vector ticks (Acari: Ixodidae) by different species of Babesia and Theileria agents from three different enzootic parts of Iran. J Arthropod Borne Dis. 2013;7(2):164-72.
5. Zaeemi M, Haddadzadeh H, Khazraiinia P, Kazemi B, Bandehpour M. Identification of different Theileria species (T. lestoquardi, T. ovis, and T. annulata) in naturally infected sheep using nested PCR–RFLP. Parasitol Res. 2011;108(4):837-43.
6. Tageldin MH, Fadiya AA-K, Sabra AA-Y, Ismaily SIA-I. Theileriosis in sheep and goats in the Sultanate of Oman. Trop Anim Health Prod. 2005;37(6):491-93.
7. Yaghfoori S, Mohri M, Razmi G. Experimental Theileria lestoquardi infection in sheep: Biochemical and hematological changes. Acta Trop. 2017;173:55-61.
8. Razmi G, Yaghfoori S, Mohri M, Haghparast A, Tajeri S. The haematological, proinflammatory cytokines and IgG changes during an ovine experimental theileriosis. Onderstepoort J Vet Res. 2019;86(1):e1-6.
9. Baghshani H, Razmi GR, Yaghfoori S, Dezaki AA. Investigation of selected biochemical parameters in sheep naturally infected with theileriosis. Comp Clin Path. 2012;21(6):1417-20.
10. Yaghfoori S, Razmi GR, Mohri M, Razavizadeh ART, Movassaghi AR. An experimental ovine theileriosis: The effect of Theileria lestoquardi infection on cardiovascular system in sheep. Acta Trop. 2016;161:55-61.
11. Sonmez O, Sonmez M. Role of platelets in immune system and inflammation. Porto Biomed J. 2017;2(6):311–14.
12. Chen XL, Xue L, Wang W, et al. Prognostic significance of the combination of preoperative hemoglobin, albumin, lymphocyte and platelet in patients with gastric carcinoma: a retrospective cohort study. Oncotarget. 2015;6(38):41370–82.
13. Mahmoud MHS, Al-Dhalimy AMB, Al-Dujaily AH. Study of hematological and biochemical changes in sheep and goats infected with theileriosis at Al-Najaf province, Iraq. Biochem Cell Arch. 2019;19(1):803–06.
14. Habela M, Reina D, Niecto C, Navarrete I. Theileria ovis in Extremadura, Spain. Study of pathogenicity. Rev Iber Parasitol. 1989;49(2):117.
15. Al-Fahdi A, Alqamashoui B, Al-Hamidhi S, et al. Molecular surveillance of Theileria parasites of livestock in Oman. Ticks Tick Borne Dis. 2017;8(5):741–48.
16. Mans BJ, Pienaar R, Latif AA. A review of Theileria diagnostics and epidemiology. Int J Parasitol Parasites Wildl. 2015;4(1):104–18.
17. Fattahi R, Shayan P, Ebrahimzadeh E, Amininia N. Differential Diagnosis of Theileria lestoquardi, Theileria ovis and Theileria annulata in Sheep, Using Molecular Method, PCR. J Vet Res. 2020;75(1):8-16.
18. Shayan P, Jafari S, Fattahi R, Ebrahimzade E, Amininia N, Changizi E. Identification and characterization of Theileria ovis surface protein (ToSp) resembled TaSp in Theileria annulata. Parasitol Res. 2016;115(5):1893–99.
19. Al-Saadi M. Quantification of acute and chronic theileriosis in sheep by quantitative PCR (qPCR). Arch Razi Inst. 2023;78(1):389.
20. Nagore D, García-Sanmartín J, García-Pérez AL, Juste RA, Hurtado A. Identification, genetic diversity and prevalence of Theileria and Babesia species in a sheep population from Northern Spain. Int J Parasitol. 2004;34(9):1059–67.
21. El Imam AE, Hassan SM, Gameel AA, El Hussein AM, Taha KM, Oosthuizen MC. Molecular identification of different Theileria and Babesia species infecting sheep in Sudan. Ann Parasitol. 2016;62(1):47-52.
22. Saeed S, Jahangir M, Fatima M, et al. PCR-based detection of Theileria lestoquardi in apparently healthy sheep and goats from two districts in Khyber Pukhtoon Khwa (Pakistan). Vet Med Int. 2015; 32(2):225-32.
23. Altay K, Dumanli N, Holman PJ, Aktas M. Detection of Theileria ovis in naturally infected sheep by nested PCR. Vet Parasitol. 2005;127(2):99–104.
24. Soosaraei M, Haghi MM, Etemadifar F, et al. Status of theileriosis among herbivores in Iran: A systematic review and meta-analysis. Vet World. 2018;11(3):332–41.
25. Zarei F, Ganjali M, Nabavi R. Identification of Theileria species in sheep and vector ticks using PCR method in Zabol, Eastern Iran. J Arthropod Borne Dis. 2019;13(1):76.
26. Jalali SM, Khaki Z, Kazemi B, Rahbari S, Shayan P, Bandehpour M, Yasini SP. Molecular detection and identification of Theileria species by PCR-RFLP method in sheep from Ahvaz, Southern Iran. Iran J Parasitol. 2014;9(1):99.
27. Habibi G, Mehrabadi MHF, Fathi S, Esmaeilnia K, Shahedi A, Yazdani F, Afshari A. Detection of Babesia spp. and Theileria spp. in sheep across diverse provinces of Iran. Vet Parasitol Reg Stud Rep. 2024;56:101131.
28. Motavallihaghi S, Fakhar M, Sharbatkhori M, Paghe AS. First molecular evidence of Theileria lestoquardi in small ruminants in northern Iran. Ann Parasitol. 2022;68(3): 531-536.
29. Ashley LA, Hackner SG, Prittie J. Clinical management of canine babesiosis. J Vet Emerg Crit Care. 2012;22(1):77–89.
30. Garcia ATC. Piroplasma infection in dogs in northern Spain. Vet Parasitol. 2006;138(1-2):97–102.
31. Harrus S, Waner T. Diagnosis of canine monocytotropic ehrlichiosis (Ehrlichia canis): An overview. Vet J. 2011;187(3):292–6.
32. Solano-Gallego L, Baneth G. Babesiosis in dogs and cats – expanding parasitological and clinical spectra. Vet Parasitol. 2011;181(1):48–60.
33. Rosa CT, Pazzi P, Nagel S, McClure V, Christie J, Troskie M, Dvir E. Theileriosis in six dogs in South Africa and its potential clinical significance: clinical communication. J S Afr Vet Assoc. 2014;85(1): 1114.
34. Snarska A, Pomianowski A, Krystkiewicz W, Sobiech P, Lew S, Bednarek D. Influence of invasion of intracellular parasites on platelet response in dogs based on clinical cases. J Vet Res. 2012; 56:519–23.
35. Noori Alavije H, Ahmadi-Hamedani M, Moslemi H. Evaluation of platelet indices and mean platelet volume to platelet count ratio in experimentally varicocele-induced adolescent and adult rats. Andrologia. 2022;54(3):e14345.
36. Majumdar A, Kumar A, Biswas S. Automated complete blood count profile as a probable indicator of dengue fever severity in children. J Sci Soc. 2022;49(3):186–9.
37. Sontakke RA, Aglave NR, Dua H. Correlation of platelet parameters with the severity of thrombocytopenia in dengue fever in children aged less than 18 years at a tertiary care center: a cross-sectional study. Cureus. 2024;16(3):e56829.
38. Mohr R, Martinowitz U, Golan M, Ayala L, Goor DA, Ramot B. Platelet size and mass as an indicator for platelet transfusion after cardiopulmonary bypass. Circulation. 1986;74(1):153.
39. Van der Lelie J, Von dem Borne AEG. Platelet volume analysis for differential diagnosis of thrombocytosis. J Clin Pathol. 1986;39(2):129-133.
40. Ustundag Budak Y, Polat M, Huysal K. The use of platelet indices, plateletcrit, mean platelet volume and platelet distribution width in emergency non-traumatic abdominal surgery: a systematic review. Biochem Med (Zagreb). 2016;26(2):178–93.
41. Abdullah SH, Dyary HO, Saeed NM. Molecular detection of Theileria spp. in native sheep and estimation of hemato-biochemical parameters from Sulaimani province/Iraq. Front Vet Sci. 2022;9:1059599.
42. Ullah N, Durrani AZ, Ullah S, et al. Study on potential factors and physiological biomarkers associated with the occurrence of ovine theileriosis. Small Rumin Res. 2018;168:32–8.
43. Shah S, Khan M, Rahman H. Epidemiological and hematological investigations of tick-borne diseases in small ruminants in Peshawar and Khyber Agency, Pakistan. J Adv Parasitol. 2017;4(1):15–22.
44. Nazifi S, Razavi S, Kianiamin P, Rakhshandehroo E. Evaluation of erythrocyte antioxidant mechanisms: antioxidant enzymes, lipid peroxidation, and serum trace elements associated with progressive anemia in ovine malignant theileriosis. Parasitol Res. 2011;109(1):275–81.
45. Al-Hamidhi S, Elshafie EI, Yaghfoori S, et al. Comparative study of single Theileria lestoquardi and mixed infections with Theileria ovis. Parasit Vectors. 2021;14(1):370.
46. Shahzad S, Tipu M, Aslam A, et al. Comparative hemato-biochemical study on theileriosis in naturally infected Punjab Urial (Ovis vignei punjabiensis) and domestic sheep (Ovis aries) in Pakistan. J Anim Plant Sci. 2015;25(2):472–76.
47. Col R, Uslu U. Changes in selected serum components in cattle naturally infected with Theileria annulata. Bull Vet Inst Pulawy. 2007;51(1):15–18.
48. Homer MJ, Aguilar-Delfin I, Telford SR 3rd, Krause PJ, Persing DH. Babesiosis. Clin Microbiol Rev. 2000;13(3):451–69.
49. Antar R, Farag C, Xu V, Drouaud A, Gordon O, Whalen MJ. Evaluating the baseline hemoglobin, albumin, lymphocyte, and platelet (HALP) score in the United States adult population and comorbidities: an analysis of the NHANES. Front Nutr. 2023;10:1206958.
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| Issue | Vol 21 No 1 (2026) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijpa.v21i1.21636 | |
| Keywords | ||
| Hemoglobin Albumin Lymphocyte Nested-PCR Sheep Theileria | ||
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How to Cite
1.
Dokhaei V, Ahmadi-Hamedani M, Salimi Bejestani MR. Platelet Indices and Hemoglobin, Albumin, Lymphocyte, and Platelet (HALP) Score Alterations in Sheep with Molecularly Confirmed Theileria spp. Infection. Iran J Parasitol. 2026;21(1):76-84.
