Abstract
Physiological blood parameters help assess the health, feeding, immune, and reproductive status of wild animals. However, complicated sampling procedures make it difficult to establish the reference intervals for hematological parameters. Wild boar (Sus scrofa, Linnaeus 1758) is a popular game species. As a result, its population in Russia has been declining for the last decade. The wild boar is fertile and ecologically flexible; it responds well to biotechnical measures and have high population density. The research renders new data on the biology and physiology of wild boars.The blood samples were obtained from 68 juvenile and adult wild boars in the Kirov Region in 2017–2023. The body weight varied from 30 to 211 kg. Blood from the jugular vein was collected into anticoagulant test tubes. The laboratory tests involved a veterinary version of a MicroCC-20 Plus automatic analyzer (High Technology, USA). The stained smears were examined using a MEIJI TECHNO light microscope (Japan) under an immersion system with a ×100 lens. The red blood cell parameters were measured using the Vision Bio software (Epi, Austria).
The research revealed the hematological profile of wild boars; the data were statistically processed, including, for the first time, the effect of sex and age on various hematological parameters. The significant differences (p < 0.05) between juvenile and adult females included the relative red cell distribution width by volume (standard deviation) and red blood cell thickness. The significant differences (p < 0.05) between juvenile and adult males were in hemoglobin, hematocrit, lymphocytes, and segmented neutrophils, as well as in such red blood cell parameters as total count, relative width by volume, area, perimeter, diameter, and sphericity index. The significant differences (p < 0.05) between juvenile females and males referred to hemoglobin and such parameters of red blood cells as total count, area, perimeter, and diameter. In adult males and females, it was the red blood cell thickness and platelet count. The research also yielded the lymphocytic profile of wild boar blood. The age affected such parameters as hematocrit (p = 0.02), segmented neutrophils (p = 0.00), and lymphocytes (p = 0.00). The body weight affected the hematocrit (p = 0.02) and mean red blood cell volume (p = 0.04).
The differences in Sus scrofa hematological profile depended on the physiological status, diet, minerals, age, sex, and stress. The reference intervals may help interpret the hematological profiles of other wild boar populations and optimize the game resource management.
Keywords
Sus scrofa, wild animals, hematology, blood cells, blood parameters, platelets, cell morphologyFUNDING
The research was carried out at the Professor Zhitkov Russian Research Institute of Game Management and Fur Farming, Kirov, Russia with the support of the Fundamental Scientific Research Program of the State Academies of Sciences FSZZ-2019-0001 (AAAA-A19-119020190132-5).REFERENCES
- Shender LA, Botzler RG, George TL. Analysis of serum and whole blood values in relation to helminth and ectoparasite infections of feral pigs in Texas. Journal of Wildlife Diseases. 2002;38:385–394. https://doi.org/10.7589/0090-3558-38.2.385
- López-Olvera JR, Höfle U, Vicente J, Fernández-de-Mera IG, Gortázar C. Effects of parasitic helminths and ivermectin treatment on clinical parameters in the European wild boar (Sus scrofa). Parasitology Research. 2006;98:582–587. https://doi.org/10.1007/s00436-005-0099-2
- Arenas-Montes A, García-Bocanegra I, Paniagua J, Franco JJ, Miró F, et al. Blood sampling by puncture in the cavernous sinus from hunted wild boar. European Journal of Wildlife Research. 2013;59:299–303. https://doi.org/10.1007/s10344-013-0701-3
- Casas-Díaz E, Closa-Sebastià F, Marco I, Lavín S, Bach-Raich E, et al. Hematologic and biochemical reference intervals for wild boar (Sus scrofa) captured by cage trap. Veterinary Clinical Pathology. 2015;44(2):215–222. https://doi.org/10.1111/vcp.12250
- Maceda-Veiga A, Figuerola J, Martínez-Silvestre A, Viscor G, Ferrari N, et al. Inside the redbox: Applications of haematology in wildlife monitoring and ecosystem health assessment. Science of The Total Environment. 2015;514:322–332. https://doi.org/10.1016/j.scitotenv.2015.02.004
- Didkowska A, Klich D, Anusz K, Wojciechowska M, Kloch M, et al. Determination of hematological and biochemical values blood parameters for European bison (Bison bonasus). Plos One. 2024;19(5):e0303457. https://doi.org/10.1371/journal.pone.0303457
- Perevozchikova MA, Domsky IA, Sergeyev AA. Hematological parameters of free-ranging moose Alces alces (Linnaeus 1758) (Ruminantia, Cervidae). Foods and Raw Materials. 2024;12(1):80–90. https://doi.org/10.21603/2308-4057-2024-1-592
- Geffré A, Friedrichs K, Harr K, Concordet D, Trumel C, et al. Reference values: A review. Veterinary Clinical Pathology. 2009;38(3):288–298. https://doi.org/10.1111/j.1939-165X.2009.00179.x
- General information. In: OIE Terrestrial Manual editor. Collection and shipment of diagnostic specimens. Chapter 1.1.1. Paris: OIE; 2008. 14 p.
- Morelli J, Rossi S, Fuchs B, Richard E, Barros DSB, et al. Evaluation of three medetomidine-based anesthetic protocols in free-ranging wild boars (Sus scrofa). Frontiers in Veterinary Science 2021;(8):655345. https://doi.org/10.3389/fvets.2021.655345
- Casas-Díaz E, Marco I, López-Olvera JR, Mentaberre G, Lavín S. Comparison of xylazine–ketamine and medetomidine–ketamine anaesthesia in the Iberian ibex (Capra pyrenaica). European Journal of Wildlife Research. 2011;57:887–893. https://doi.org/10.1007/s10344-011-0500-7
- Perevozchikova MA, Domskiy IA, Sergeev AA, Berezina YuA, Bespyatykh OYu, et al. A study of post-mortem hematological parameters of arctic foxes, Vulpes Lagopus (Linnaeus, 1758). Transactions of the Karelian Research Centre RAS. 2023;(7):83–96. (In Russ.) https://elibrary.ru/MRLDYD
- Tryland M. ‘Normal’ serum chemistry values in wild animals. Veterinary Record. 2006;158(6):211–212. https://doi.org/10.1136/vr.158.6.211-b
- Kukharenko NS, Kukharenko AA, Kovalchuk IV. Anemia as the reason for wild boar livestock reduction in the Amur region. Bulliten KrasSAU. 2011;(10):177–180. (In Russ.) https://elibrary.ru/OIGGUP
- Harapin I, Bedrica L, Hahn V, Šoštarić B, Gračner D. Haematological and biochemical values in blood of wild boar (Sus scrofa ferus). Veterinarski Arhiv. 2003;73(6):333–343.
- Tušek T, Mihelić D, Firšt L, Janicki Z, Opančar D. A comparative survey of the red blood count in the boar and native European pig. Veterinarska Stanica. 1994;25(2):81–84.
- Vidal D, Naranjo V, Mateo R, Gortazar C, de la Fuente J. Analysis of serum biochemical parameters in relation to Mycobacterium bovis infection of European wild boars (Sus scrofa) in Spain. European Journal of Wildlife Research. 2006;52:301–304. https://doi.org/10.1007/s10344-006-0062-2
- Vitic J, Tosic L, Stevanovic J. Comparative studies of the serum lipoproteins and lipids in domestic swine and wild boar. Acta Veterinaria. 1994;44:49–56.
- Barasona JA, López-Olvera JR, Beltrán-Beck B, Gortázar C, Vicente J. Trap-effectiveness and response to tiletaminezolazepam and medetomidine anaesthesia in Eurasian wild boar captured with cage and corral traps. BMC Veterinary Research. 2013;(9):107. https://doi.org/10.1186/1746-6148-9-107
- Danilkin AA. Trends of wild ungulate population dynamics in Russia. Biology Bulletin. 2019;46(10):1368–1373. https://doi.org/10.1134/S106235901910008X
- Ekonomov AV, Kolesnikov VV, Dolinin VV, Sergeev AA. Wild boar (Sus scrofa L., 1758) resources in the range of the amur tiger (Panthera tigris L., 1758) in the far east of the Russian Federation Far Eastern Agricultural Journal. 2022;16(2)2:98–107. (In Russ.) https://doi.org/10.22450/19996837_2022_2_98
- Domskiy IA, Sergeyev AA, Ekonomov AV, Kolesnikov VV, Makarov VV, Tselykhova EK. Current status of the wild boar population in Russia in relation to the spread of African swine fever. Contributions to hunting and game research. 2020;(45):33–46. (In German.) https://elibrary.ru/CJSUCK
- Makarov VV, Domsky IA, Sergeev AA. To the problem of the «boar-African swine pest» Vestnik of the Russian agricultural science. 2020;(6):58–62. (In Russ.) https://doi.org/10.30850/vrsn/2020/6/58-62
- Vicente J, Segalés J, Höfle U, Balasch M, Plana-Durán J, et al. Epidemiological study on porcine circovirus type 2 (PCV2) infection in the European wild boar (Sus scrofa). Veterinary Research. 2004;35(2):243–253. https://doi.org/10.1051/VETRES:2004008
- Fernandez-de-Mera IG, Gortazar C, Vicente J, Höfle U, Fierro Y. Wild boar helminths: Risks in animal translocations. Veterinary Parasitology. 2003;115(4):335–341. https://doi.org/10.1016/s0304-4017(03)00211-5
- Höfle U, Vicente J, Nagore D, Hurtado A, Peña A, et al. The risks of translocating wildlife: Pathogenic infection with Theileria sp. and Elaeophora elaphi in an imported red deer. Veterinary Parasitology. 2004;126:387–395. https://doi.org/10.1016/j.vetpar.2004.07.026
- Baeza C, Gädicke P, Ruiz A. Determination of new hematologic reference intervals for sows with optimal reproductive performance, according to reproductive stage, parity and body condition: A cohort study. Preprint (Version 1) available at Research Square. 2021:1–16. https://doi.org/10.21203/rs.3.rs-317100/v1
- Žvorc Z, Mrljak V, Sušić V, Pompe Gotal J. Haematological and biochemical parameters during pregnancy and lactation in sows. Veterinarski arhiv. 2006;76(3):245–253.
- Perri AM, O’Sullivan TL, Harding JCS, Wood RD, Friendship RM. Hematology and biochemistry reference intervals for Ontario commercial nursing pigs close to the time of weaning. Canadian Journal of Veterinary Research. 2017;58(4):371–376.
- Boadella M, Gortazar C. Effect of haemolysis and repeated freeze-thawing cycles on wild boar serum antibody testing by ELISA. BMC Research Notes. 2011;4:498. https://doi.org/10.1186/1756-0500-4-498
- Koshurnikova MA, Domskiy IA. Sample collection, storage and laboratory analysis of biological material derived from hunter harvested wild animals. Transactions of the Karelian Research Centre of the Russian Academy of Sciences. 2022;(7):75–84. (In Russ.) https://elibrary.ru/DFYMXW
- Ivanter EV, Korosov AV. Elementary biometrics. In: Obarchuk OV, editor. Petrozavodsk: Petrozavodsk State University, 2005. 104 p.
- Friedrichs KR, Harr KE, Freeman KP, Szladovits B, Walton RM, et al. ASVCP reference interval guidelines: Determination of de novo reference intervals in veterinary species and other related topics. Veterinary Clinical Pathology. 2012;41(4):441–453. https://doi.org/10.1111/vcp.12006
- Kukharenko NS, Kukharenko AA, Kovalchuk IV. Comparative analysis of hematological parameters of wild boars and pigs in Amur region. Actual Questions of Veterinary Biology. 2011;(3):7–10. (In Russ.) https://elibrary.ru/OBEXKH
- Semenova ID, Rudishin OYu, Burtseva SV, Klemin VP. Hematologic indices of various age-sex groups of pigs of newly bred landrace breed type. Bulletin of Altai State Agricultural University. 2013;10:90–92. (In Russ.) https://elibrary.ru/RDKETL
- Gimadeeva LS, Gusev IV, Ryzhkov VA, Rykov RA. Comparative assessment of hematological profile of pigs of different technological groups. Bulletin of Orenburg State Agrarian University. 2015;(5):148–151. (In Russ.) https://elibrary.ru/UZBYIL
- Dimitrakakis N, Waterhouse A, Lightbown S, Leslie DC, Jiang A, et al. Biochemical and hematologic reference intervals for anesthetized, female, juvenile Yorkshire swine. Journal of the American Association for Laboratory Animal Science. 2022;61(1):21–30. https://doi.org/10.30802/AALAS-JAALAS-21-000014
- Giraud-Billoud M, Rivera-Ingraham GA, Moreira DC, Burmester T, Castro-Vazquez A, et al. Twenty years of the ‘Preparation for Oxidative Stress’ (POS) theory: Ecophysiological advantages and molecular strategies. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology. 2019:234. https://doi.org/10.1016/j.cbpa.2019.04.004
- Estienne MJ, ClarkDeener SG, Williams KA. Growth performance and hematology characteristics in pigs treated with iron at weaning as influenced by nursery diets supplemented with copper. Journal of Swine Health and Production. 2020;28(4):190–203. https://doi.org/10.54846/jshap/1165
- Stockham SL, Scott MA. Fundamentals of veterinary clinical pathology. Hoboken, NJ: John Wiley & Sons, 2013. 928 p.
- Zhang S, Yu B, Liu Q, Zhang Y, Zhu M, et al. Assessment of hematologic and biochemical parameters for healthy commercial pigs in china. Animals. 2022;12(18):2464. https://doi.org/10.3390/ani12182464
- Moyseenko NA. Components of red blood in young moose. Alces. 2002;(2):93–97.
- Taylor JA, Feldman BF, Zinki JG, Jain NC. Leukocyte responses in ruminants. Schalm’s veterinary hematology. Baltimore, Maryland: Lippincott Williams & Wilkins; 2000. p. 391–393.
- Revsbech IG, Fago A. Regulation of blood oxygen transport in hibernating mammals. Journal of Comparative Physiology B. 2017;187:847–856. https://doi.org/10.1007/s00360-017-1085-6
- Lee S, Lee SC, Jeon Y. Analysis of blood composition by porcine breeding cycle. Veterinary Medicine and Science. 2024;10(2):e31376. https://doi.org/10.1002/vms3.1376
- Erjavec V, Vovk T, Nemec Svete A. The effect of two acute bouts of exercise on oxidative stress, hematological, and biochemical parameters, and rectal temperature in trained canicross dogs. Frontiers in Veterinary Science. 2022;2:767482. https://doi.org/10.3389/fvets.2022.767482
- López-Olvera JR, Höfle U, Vicente J, Fernández-de-Mera IG, Gortázar C. Effects of parasitic helminths and ivermectin treatment on clinical parameters in the European wild boar (Sus scrofa). Parasitology Research. 2006;98:582–587. https://doi.org/10.1007/s00436-005-0099-2
- Wolkers J, Wensing T, Groot Bruinderink GWTA, Schonewille JT. The effect of undernutrition on haematological and serum biochemical variables in wild boar (Sus scrofa). Comparative Biochemistry and Physiology. 1994;108(2–3):431–437. https://doi.org/10.1016/0300-9629(94)90115-5
- Wolkers J, Wensing T, Groot Bruinderink GW, Schonewille AT. Comparative nutrition papers: Nutritional status of wild boar (Sus scrofa): II. Body fat reserves in relation to haematology and blood chemistry. Comparative Biochemistry and Physiology Part A: Physiology. 1993;105(3):539–542. https://doi.org/10.1016/0300-9629(93)90431-3
- Petrova OV, Shashin SA, Tarasov DG. Significance of platelet indices determination in patients after coronary artery bypass grafting. Russian Journal of Cardiology and Cardiovascular Surgery. 2014;7(3):58–62. (In Russ.) https://elibrary.ru/SUCVCB
- Balakrishnan A, Shetty A, Vijaya C. Estimation of platelet counts: Auto analyzer versus counts from peripheral blood smear based on traditional and platelet: Red blood cell ratio method. Tropical Journal of Pathology and Microbiology. 2018;4(5):389–395. https://doi.org/10.17511/jopm.2018.i05.04
- Mabood A, Chaturvedi V, Gupta S, Alam MQ, Dwivedi N, et al. Thrombocyte estimation based on blood smear and its comparison using automated haematology analysers. Journal of Evolution of Medical and Dental Sciences. 2019;8(19):1588–1591. https://doi.org/10.14260/jemds/2019/351
- Dolgov VV, Svirin PV. Laboratory diagnostics of hemostasis disorders. Moscow–Tver: Triada, 2005. 227 p. (In Russ.)
- Momot AP. Pathology of hemostasis. Principles and algorithms of clinical and laboratory diagnostics. St. Petersburg: FormaT; 2006. 208 p. (In Russ.)
- Mininkova AI. A review of analytical capabilities of hematological analyzers in platelet assessment. Clinical Laboratory Diagnostics. 2012;(3):27–34. (In Russ.) https://elibrary.ru/PFHMRN
- Puchinskaya MV, Pochtovtsev AYu. Clinical significance of platelet indices in cardiology. Military Medicine. 2011;(2):77–81. (In Russ.) https://www.elibrary.ru/RQDYIL
- Brækkan SK, Mathiesen EB, Njølstad I, Wilsgaard T, Størmer J, et al. Mean platelet volume is a risk factor for venous thromboembolism: The Tromsø study. Journal of Thrombosis and Haemostasis. 2010;8(1):157–162. https://doi.org/10.1111/j.1538-7836.2009.03498.x
- Buttarello M, Plebani M. Automated blood cell counts: State of the art. American Journal of Clinical Pathology. 2008;130(1):104–116. https://doi.org/10.1309/ek3c7ctdknvpxvtn
- Thorn CE. Hematology of the pig. In: Weiss DJ, Wardrop KJ, Schalm OW, editors. Schalm’s Veterinary Hematology. Wiley Blackwell, 2010. pp. 843–851.
- Bazzano M, Giannetto C, Fazio F, Rizzo M, Giudice E, et al. Physiological adjustments of haematological profile during the last trimester of pregnancy and the early post-partum period in mares. Animal Reproduction Science. 2014;149(3–4):199–203. https://doi.org/10.1016/j.anireprosci.2014.07.005
- Bakrim S, Motiaa Y, Ouarour A, Masrar A. Hematological parameters of the blood count in a healthy population of pregnant women in the Northwest of Morocco (Tetouan-M’diq-Fnideq provinces). Pan African Medical Journal. 2018;29:205. https://doi.org/10.11604/pamj.2018.29.205.13043
- Bhattarai S, Framstad T, Nielsen JP. Stillbirths in relation to sow hematological parameters at farrowing: A cohort study. Journal of Swine Health and Production. 2018;26(4):215–222. https://doi.org/10.54846/jshap/1052
- Ježek J, Starič J, Nemec M, Plut J, Golinar Oven I, et al. The influence of age, farm, and physiological status on pig hematological profiles. Journal of Swine Health and Production. 2018;26(2):72–78. https://doi.org/10.54846/jshap/1049
- Martínez-Miró S, Tecles F, Ramón M, Escribano D, Hernández F, et al. Causes, consequences and biomarkers of stress in swine: An update. BMC Veterinary Research. 2016;12:171. https://doi.org/10.1186/s12917-016-0791-8
- Zhang S, Yu B, Liu Q, Zhang Y, Zhu M, et al. Assessment of hematologic and biochemical parameters for healthy commercial pigs in China. Animals. 2022;12(18):2464. https://doi.org/10.3390/ani12182464
- Perri AM, O’Sullivan TL, Harding JCS, Wood RD, Friendship RM. Hematology and biochemistry reference intervals for Ontario commercial nursing pigs close to the time of weaning. The Canadian Veterinary Journal. 2017;58(4):371–376.
- Alves MH, Kluyber D, Alves AC, Yogui DR, Pereira FMAM, et al. Hematology and biochemistry reference intervals in chemically immobilized free-ranging giant anteaters (Myrmecophaga tridactyla). European Journal of Wildlife Research. 2023;69:37. https://doi.org/10.1007/s10344-023-01663-5
- Zeiler GE, Meyer LCR. Chemical capture of impala (Aepyceros melampus): A review of factors contributing to morbidity and mortality. Veterinary Anaesthesia and Analgesia. 2017;44(5):991–1006. https://doi.org/10.1016/j.vaa.2017.04.005
- Barić R, Rafaj R, Tončić J, Vicković I, Šoštarić B. Haematological and biochemical values of farmed red deer (Cervus elaphus). Veterinarski arhiv. 2011;81(4):513–523.
- Miller AL, Evans AL, Os Ø, Arnemo JM. Biochemical and hematologic reference values for free-ranging, chemically immobilized wild Norwegian reindeer (Rangifer Tarandus Tarandus) during early winter. Journal of Wildlife Diseases. 2013;49(2):221–228. https://doi.org/10.7589/2012-04-115
- Harvey JW, Pate MG, Kivipelto J, Asquith RL. Clinical biochemistry of pregnant and nursing mares. Veterinary Clinical Pathology. 2005;34(3):248–254. https://doi.org/10.1111/j.1939-165x.2005.tb00049.x
- Czech A, Grela ER. Biochemical and haematological blood parameters of sows during pregnancy and lactation fed the diet with different source and activity of phytase. Animal Feed Science and Technology. 2004;116(3–4):211–223. https://doi.org/10.1016/j.anifeedsci.2004.07.013
- Wolkers J, Wensing Th, Groot Bruinderink GWTA, Schonewille JTh. Lungworm and stomach worm infection in relation to body fat reserves and blood composition in wild boar (Sus scrofa). Veterinary Quarterly. 1994;16(4):193–195. https://doi.org/10.1080/01652176.1994.9694446
- Jur̆icová Z, Hubálek Z. Serologic survey of the wild boar (Sus scrofa) for Borrelia Burgdorferi sensu lato. Vector-Borne and Zoonotic Diseases. 2009;9(5):479–482. https://doi.org/10.1089/vbz.2008.0125
- Faria AS, Paiva-Cardoso MDN, Nunes M, Carreira T, Vale-Gonçalves HM, et al. First detection of Borrelia burgdorferi sensu lato DNA in serum of the wild boar (Sus scrofa) in northern Portugal by Nested-PCR. EcoHealth. 2015;12:183–187. https://doi.org/10.1007/s10393-014-0973-4
- Mays Maestas SE, Campbell LP, Milleson MP, Reeves LE, Kaufman PE, et al. Ticks and tick-borne pathogens from wild pigs in northern and central Florida. 2023;14(7):612. https://doi.org/10.3390/insects14070612
- Perevozchikova MA, Domsky IA, Berezina YuA, Sergeev AA. Blood biochemical parameters in reservoir hosts under ixodid tick-borne borreliosis. Agricultural Biology. 2023;58(4):757–772. (In Russ.) https://doi.org/10.15389/agrobiology.2023.4.757rus
- Karpiński M, Czyżowski P, Beeger S, Flis M. Hematological and serum biochemical values of free-ranging roe deer (Capreolus capreolus) in Poland. Animals. 2023;13(2):242. https://doi.org/10.3390/ani13020242
- Gaspar-López E, Landete-Castillejos T, Estevez JA, Ceacero F, Gallego L, et al. Seasonal variations in red deer (Cervus elaphus) hematology related to antler growth and biometrics measurements. Journal of Experimental Zoology. 2011;315A(4):242–249. https://doi.org/10.1002/jez.670
- Kazakova MS, Lugovskaya SA, Dolgov VV. The reference values of indicators of total blood analysis of adult working population. Clinical Laboratory Diagnostics. 2012;(6):43–49. (In Russ.) https://www.elibrary.ru/PFHTLR
- Bleul U, Bleul U, Sobiraj A, Bostedt H. Effects of duration of storage and storage temperature on cell counts of bovine blood samples as determined by an automated haematology analyser. Comparative Clinical Pathology. 2002;11:211–216. https://doi.org/10.1007/s005800200021