Abstract
The review examines the role of blood in homeostasis, diagnosis and treatment of disease as influenced by meteorological stress factors, age, sex and physical activity of the donkeys. Haematological parameters play a crucial role in clinical diagnosis of infectious and parasitic diseases, in assessing the responses of donkeys to treatment and in prevention of diseases. The changes in blood values are important in evaluating the responses of the animals to various physiologic conditions. In conclusion, haematological values of donkeys are largely influenced by age, sex, physical factors of the environment and physical activity, and consideration of the factors will aid accurate diagnosis and therapeutic evaluation of equine diseases.
Similar content being viewed by others
Introduction
The donkey (Equus asinus) has been used as a working animal for at least 5000 years mainly for transportation, conveying farm produce to the market or pulling of carts and also for farm tillage (Starkey and Starkey 2004). Presently, donkeys are used in the production of milk for children who are allergic to bovine milk (Carrocio et al. 2000; Muraro et al. 2002; Caldin et al. 2005; Mansueto et al. 2013) and in animal-assisted therapy and activity in humans (Borioni et al. 2012). The population of donkeys is on the increase in Africa, and the animals are increasingly becoming important in transportation of farm produce. In Nigeria, donkeys are used mainly in transportation of goods and agricultural produce (Blench 2004).
Haematological examination has been performed for a variety of reasons: as a screening procedure to examine general health of the animal, as an adjunct to a patient’s infection and to evaluate the progress of certain disease conditions. Haematological values play a vital role in clinical diagnosis, the assessment of patient before surgical procedure and in monitoring the progress of animals to treatment (Mori et al. 2004; Satue et al. 2009; Yaqub et al. 2013). The diagnosis and treatment of diseases in animals greatly depends on clinical examination and haematologic results, which reflect biological variation. This in turn requires the understanding of haematological profiles of an, apparently, healthy animal, whose physiological parameters provide invaluable information regarding the health status of the animal (Kral and Suchy 2000; Mori et al. 2003, 2004; Cetin et al. 2009). Inspite of the clinical significance, correct haematological interpretation and analysis are sometimes difficult because many factors considerably influence the haematological parameters in goats, pigs, rabbits, camels, cattle, horses and donkeys, including age (McFarlane et al. 2001; Caldin et al. 2005; Gurgoze and Icen 2010; Melo et al. 2013; Padalino et al. 2014; Girardi et al. 2014;), sex (Cetin et al. 2009; Mirzadeh et al. 2010; Uluisik et al. 2013; Girardi et al. 2013, 2014), breed (Tibbo et al. 2004; Lacerda et al. 2006; Orozco et al. 2007; Šimpraga et al. 2013), seasons (Dmoch et al. 2008; Adenkola et al. 2011; Mirzadeh et al. 2010; Abdelatif and Alameen 2012; Babeker et al. 2013; Šimpraga et al. 2013), diet (Ekenyem and Madubruke 2000; Iyayi 2001; Kumar et al. 2005), health status and sub-clinical disease (Rose and Hodgson 1994; Petrov et al. 2011; Kalai et al. 2012) work or exercise (Piccione et al. 2001; Zobba et al. 2011; Kedzierski et al. 2009; Miranda et al. 2011) and pregnancy (Harvey et al. 1994; Orozco et al. 2007; Satué et al. 2010a, b; Farooq et al. 2011; Okonkwo et al. 2011; Aoki and Ishii 2012).
The aim of the present review was to determine the effect of age, sex, physical factors of the environment and physical activity on haematological parameters of donkeys.
Domestication and uses of donkeys
Domestication of the donkey transformed ancient societies and initiated the development of nomadic pastoral communities in Africa and the expansion of land-based routes in the Middle East (Marshall 2007; Rossel et al. 2008). Marshall (2007) stressed on the importance of African pastoralist use of donkeys for transport during long-distance movements, for women’s daily tasks, such as fetching water or firewood, and in the sustainable management of rangelands. The relationship between humans and the ancestors of modern donkeys was established by pastoralists, who had to use the animals to assist them to survive the harsh Saharan terrain in Northern Africa more than 5000 years ago (Kimura et al. 2011). Today, donkeys play critical role in assisting African herders to cope with unpredictable climatic fluctuations. They provide greater mobility with which to face erratic rainfalls and are used for carrying loads including firewood, water, household structures, goods and children (Marshall and Weissbrod 2011). In India, donkeys have been used to carry arms and ammunition to the difficult terrains that mechanized vehicles cannot reach easily (Singh et al. 2005). The ultimate use of donkeys for human therapeutic purpose is in the field of onotherapy, a method frequently used for people who have disabilities and discomforts (Karatosidi et al. 2013).
In ancient civilization, donkeys were used for different purposes than today. They were not only used as pack (load-carrying) animals but their milk, skin and meat were useful. Donkey milk has recently generated scientific interest because of its attractive nutrient and functional components. It is considered a valid substitute for infants with severe IgE-mediated cow’s milk protein allergy (Monti et al. 2007). Donkey milk is a potent vasodilator, making it potentially useful in the prevention of atherosclerosis (Tafaro et al. 2007) and has been shown to exert suppressive effect against human lung tumour in vitro (Mao et al. 2009). The milk was highly prized because it contains more sugar and protein than bovine milk. It is also a good substitute for babies and the sick (Criscione et al. 2009). Donkeys have recently gained new application with the use of their milk to feed humans with allergic disorders. The Ragusana and Martina Franca breed from Sicily, Italy, is used to produce milk for human consumption (Caldin et al. 2005).
Homeostatic role of blood
Blood is a special type of regulatory, protective and homeostatic connective tissue, comprising formed elements (erythrocytes, leucocytes and platelets) and plasma (Nasyrova et al. 2006; Eze et al. 2010). The main function of the blood is the transportation of oxygen, which is achieved through the presence of conjugated metallo-protein known as haemoglobin (Ashton 2013). Blood values are used for evaluating stress and the well-being of the animal. Its profiles in animals provide means of assessing the internal environment and understanding the causes of impairment in homeostasis as evidenced by marked fluctuations in physiogical indices under different internal and external environmental conditions (Sattar and Mirza 2009). Blood constituents reflect the influence of normal physiological and pathological states of the animals, including thermal stress (Satue et al. 2009). For example, packed cell volume (PCV) and haemoglobin concentration (Hb) are used in the assessment of metabolic profile of animals (Kida 2002). Neutrophil blood counts are the consequence of a very dynamic feedback mechanism, which are controlled by different environmental and genetic factors that remain largely unknown (Von Vietinghoff and Ley 2008). At present, neutrophil/lymphocyte ratio (N:L) is a well-accepted indicator for stress assessment in animals (Rajion et al. 2001; Goundasheva et al. 2005; Stanger et al. 2005; Quiñonero et al. 2009; Holub et al. 2012).
Platelets are important in physiologic and pathologic processes of inflammation, tumour metastasis, haemostasis, wound healing and host defense (Semple et al. 2011). Variation in haematological parameters is a reflection of an animal’s response to its external and internal environments (Esonu et al. 2001).
The use of haematological parameters in diagnosis and treatment
Inappropriate reference values for haematology increase the risks of unnecessary investigations and diagnostic failures. Species, breed, environment, handling and physiological state influence haematologic and biochemical variables (Šimpraga et al. 2013; Etim et al. 2013; Girardi et al. 2014). Haematology and serum biochemistry are important diagnostic aids use to assess metabolic status in starved equids and to rule out pathologic conditions. The knowledge of the haematologic findings in emaciated equine is useful in scoring the intensity of emaciation, in establishing a prognosis and a plan to recover the health status of these animals (Muñoz et al. 2010). Haematological values during different physiological situations are beneficial in ensuring accurate diagnosis of various pathological and metabolic disorders, which may adversely affect livestock performance (Sattar and Mirza 2009). The comparison between individuals using reference data is necessary, based on normal variations due to sex, age and breed in order to increase diagnostic precision in clinical situations (Satue et al. 2009).
Haematological responses to stress factors
The haematological profile is important in the determination of physiological changes occurring in animals (Kumar and Pachaura 2000; Anderson et al. 1999). Haematological parameters such as packed cell volume (PCV), total erythrocyte count (RBC), mean corpuscular haemoglobin (MCV), mean corpuscular haemoglobin concentration (MCHC), mean corpuscular haemoglobin (MCH) and total differential leucocyte counts (WBC) are used to evaluate adaptability of animals to adverse environmental conditions (Koubkova et al. 2002). Research in haematology is of ecological and physiological importance, and the findings are of value in understanding the relationship between blood characteristics and the environment (Ovuru and Ekweozor 2004) and selection of animals with superior genetic traits (Mmereole 2008; Isaac et al. 2013). Strenuous exercise or work results in severe haematological, metabolic, acid-base and ionic changes in animals, which are specie-specific, and are influenced by the magnitude of the cumulative effects of physiological and physical trauma, related to the stressful events (Hassanein 2010). Acidosis and physical stress result in disturbances in haematological parameters such as haemoglobin and haematocrit levels (Moyes et al. 2006).
Erythropoietic responses observed during exercise are the results of myriads of interacting mechanisms that involve oxidative stress and haematopoietic system (Lorena et al. 2006). Changes in the osmotic fragility of equine erythrocytes during exercise are important indicator of stress and intravascular haemolysis (Hanzawa and Watanabe 2000). Cuniberti et al. (2012) observed that exercise results in significant increase in erythrocyte count, haemoglobin concentration, PCV and neutrophil, lymphocyte and monocyte counts. A direct relationship exists between leucocyte profiles, stress and glucorticoid levels (Vleck et al. 2000). Glucorticoids secreted in stress act to increase the number and percentage of neutrophils while decreasing the number and percentage of lymphocytes (Johnstone et al. 2012). Thus, neutrophil:lymphocyte ratio is of diagnostic value in stress (Altan et al. 2003; Walsh et al. 2005; Zazula et al. 2008).
Effect of age on haematological parameters
Effects of age on haematological parameters have been documented in various breeds of horses (Hernández et al. 2008; Satue et al. 2009). Grondin and Dewitt (2010) and Sgorbini et al. (2013) reported that newborn foals have high PCV, RBC and Hb because erythrocytes are of foetal origin. Thus, the involvement of the liver and spleen in erythropoiesis and probably due to the transfusion of placental blood to the foal at birth may result in increased erythrocytic values. The high values of PCV, haemoglobin concentration and erythrocyte count observed in foals may also occur as a result of functional changes in haematopoiesis and high water content in foals or due to haemoconcentration because foals depend mainly on milk. Sgorbini et al. (2013), Muñoz et al. (2012) and Grondin and Dewitt (2010) observed that PCV, Hb and erythrocyte count decreased significantly after the first 48 h of life, probably as a result of haemodilution, physiological destruction of erythrocytes by the spleen and decreased erythropoietin production secondary to increased blood oxygenation by lungs after birth. Muñoz et al. (2012) also reported higher PCV, RBC and Hb in Spanish foals than those in adult Spanish horses. There is an increase in erythrocyte counts, PCV and Hb in donkeys as they get older (Etana et al. 2011). A reduction of erythrocyte count with a compensatory increase in MCV and MCH in older Carthusian pregnant mares and Spanish purebred mares have been reported (Hernández et al. 2008). Satue et al. (2009), observed increased MCH, MCV and MCHC in adult horses. In a study conducted on working donkeys, the RBC, Hb, MCV, MCHV, PCV and MCH are higher in adult donkeys than in young ones (Etana et al. 2011). According to Folch et al. (1997), young donkeys had significantly lower values of MCV and MCH as well as higher counts of leucocytes, segmented neutrophils, immature neutrophils and eosinophils than older animals. PCV and Hb increase with age in working horses (Pritchard et al. 2009). MCV in foals less than 1 year is significantly lower than that of the adult horses. Lippizan foals aged between 4 months and below have higher erythrocyte count and PCV than stallions and mares of the same breed (Cebulj-Kadunc et al. 2002). Brommer et al. (2001) reported an increase in neutrophil and lymphocyte counts during the first months of life. Uluisik et al. (2013) observed significant difference in RBC, PCV and MCV in horses of different ages. Adult working donkeys have higher PCV, RBC, Hb, MCV, MCHC and MCH than young donkeys (Lemma and Moges 2009). Old pregnant Andalusian mares have lower total leucocyte and lymphocyte counts, compared to younger ones (Satue et al. 2009). In addition, higher leucocyte count in younger animals when compared to adult was observed in Kathiawari horses in India (Gupta et al. 2002). The decrease in leucocyte count in healthy, aged horses may be related to age-associated decrease in immunocompetency (Mcfarlane et al. 2001).
The role of sex on haematology of donkeys
The sex of an animal affects blood parameters in many animal species, and values in females are lower than in males. The PCV in male Red Sokoto goats are higher than in females. Slight differences or variation in blood parameters have been reported in equids. Male horses have slight RBC, Hb and PCV than female. Mares have been reported to have higher MCH values (Hernández et al. 2008; Satue et al. 2009). Significant differences related to sex of thoroughbred foals were reported with regard to PCV at 1 year and WBC at day one (Uluisik et al. 2013). Sex variation in immune function is well established in vertebrates. Total leucocyte count is higher in mares than stallions of the Spanish purebred (Hernández et al. 2008). However in other studies, no significant differences between male and female horses were obtained (Lacerda et al. 2006). The increase in haematological parameters in males compared to females may be due to the effect of androgens, which stimulate erythropoiesis (Kelani and Durotoye 2002). In a study conducted to determine baseline values for haematology in working donkeys (Etana et al. 2011), there were significant variations in total leucocyte, MCV and neutrophil counts between sexes. Male Przewalski horses were characterized by significantly higher erythrocyte count and immature neutrophilic granulocytes than female Przewalski horses (Tomenenendalova et al. 2014). In the experiment conducted by Tomenenendalova et al. (2014), stallions were also observed to have a relatively higher haemoglobin concentration and leucocyte and monocyte counts than mares but without significant significance. The PCV and haemoglobin concentration are lower in mares than in working horses with low body condition scores (Pritchard et al. 2009). The PCV in female foals was reported to be higher than in colts of 1–2 months of age. The work of Mori et al. (2004) and Gul et al. (2007) on donkeys reported no sex differences in haematological parameters. There were variations in RBC, MCV and neutrophil counts between different male and female donkeys (Etana et al. 2011). Leucocyte count was higher in female Spanish purebred horses than males (Hernández et al. 2008). Studies conducted by Hernández et al. (2008) and Satue et al. (2009) showed that male horses have slightly higher PCV, RBC and Hb than female horses. The slight increase in erythrocytic parameters in males may be attributed to the effect of androgens, which stimulate erythropoiesis (Gaspar-López et al. 2010). Mikniene et al. (2014) established that female Zematukai horses have higher Hb, PCV, RBC and MCHC than male horses. Zinkl et al. (1990) observed that female donkeys had higher values of MCHC and leucocyte and neutrophil counts than adult males.
Influence of physical factors of the environment on haematological parameters
Season and meteorological parameters are external factors that control the dynamics of blood constituents in the equine (Satué et al. 2011). In the equine, seasonal changes may decrease some haematological parameters, including RBC, Hb and PCV. Season is an external factor that controls the dynamics of blood constituents in equines (Satué 2004; Satué et al. 2011). In Carthusian mares, PCV, RBC and MCV are higher in the summer than any other seasons (Satué et al. 2011). It has been suggested that extreme cold reduces the number of erythrocytes due to the reduction in the half-life of the erythrocytes (Ruiz et al. 2004). Seasonal changes in ambient temperature, relative humidity and air velocity influence the physiological responses of animals. Changes in haematological values such as PCV, RBC, MCV and MCHC are used in determining the adaptation of animals to the environment (Koubkova et al. 2002). In Polish warmblood mares, significant increases in neutrophil count, MCH and MCHC were obtained in the summer than in the winter and spring (Dmoch et al. 2008). Blood parameters in Arabian horses such as PCV, Hb and RBC are significantly lower in the summer, compared with the winter season (Gill et al. 1979). Gill and Kompanowska-Jezierska (1986) reported that Arabian mare and thoroughbred horses have higher PCV, RBC and Hb during the winter than the other seasons. In the tropics, animals are predominantly kept outdoor, and they are exposed to direct solar radiation during the day and other thermal stressors, including high ambient temperature, high humidity and rainfall, exerting significant effect on their performance (Silanikove 2000; Scharf 2008; Hetem et al. 2011). Animals under heat stress must alter their behaviour and physiology to increase heat loss, reduce heat production and restore homeostasis. This is done at the expense of productivity (Huynh et al. 2005; Lin et al. 2009). Ungulates in the arid regions are able to survive extreme environmental conditions due to behavioural and physiological adaptations of the animal to combat these adverse conditions (Cain et al. 2006; Sneddon et al. 2006). The environment in which equines are raised influences the ability of the animals to maintain thermal equilibrium, which is, in turn, related to their thermal characteristics and regulatory physiological mechanisms (Castanheira et al. 2010). In the Northern Guinea Savanna zone of Nigeria, the early rainy season was observed to be stressful to packing donkeys (Ayo et al. 2008). Heat stress causes cascade of changes in the physiological mechanisms of animals. Increase in physiological parameters of donkeys above the normal range indicates that the animals are stressed (Minka and Ayo 2007). Extreme hot and cold ambient temperatures affect animals, which is evident in fluctuations of physiological responses to combat the thermal environmental stress (Pandey et al. 2012).
The relationship between physical activity and haematological parameters of donkeys
Physical activity or work in animal is a commonly recognized stress factor which can influence haematological parameters. Physiological changes in haematological parameters occur in response to exercise and training in thoroughbreds and standardbreds (Fazio et al. 2011). The rate of metabolism of neutrophils is higher in regularly trained horses than in animals that engage in mild physical activity (Krumrych 2009). Piccione et al. (2008) observed that platelet aggregation in exercising horses is different from that in resting horses. Physical activity or exercise exerts effect on the daily rhythm of platelets in horses. Lemma and Moges (2009) in Ethiopia established that clinical and haematological values were not affected by the degree of work performance in working donkeys. However, serum biochemical values, except total protein, were significantly affected by workload. According to Olaifa et al. (2012), packing significantly decreases the PCV and RBC of donkeys, while the neutrophil/lymphocyte ratio rose significantly after the donkeys were subjected to packing. Oxygen consumption and average heart rate in donkeys and running at a maximum speed significantly increased heart rate in animals, compared to values obtained in non-exercising horses (Mueller et al. 1994). Changes occurring in haematologic parameters induced by physical work have been well documented (Hinchcliff et al. 2002; Lorena et al. 2006).
Erythrocyte osmotic fragility is used to determine the level of stress in animals (Hesta et al. 2008). Alterations in the erythrocyte osmotic fragility occurs during strenuous work in horses (Hanzawa and Watanabe 2000). Metabolic responses to exercise differ between Andalusian horses and other breeds, although changes in activities of plasma muscle enzymes have not been reported, and most useful information is obtained from animals subjected to different training programmes (Muñoz et al. 2002). Rovira et al. (2007) observed that exercise competitions induce mild to moderate alterations in haematologic and biochemical parameters; consistent with splenic contraction, increased lipolysis and utilization of anaerobic pathways involved in energy re-synthesis in the muscle.
Concluding remarks
Endogenous and exogenous factors such as age, sex and physical factors of the environment significantly affect or influence the haematological parameters of donkeys. Extreme meteorological factors, including high ambient temperature, relative humidity, solar radiation and wind velocity are stressors that alter the haematological parameters of donkeys. Frequent use of pack donkeys without adequate rest can lead to physical exhaustion due to work stress, thereby impairing haematological parameters of donkeys. Reference haematological parameters obtained from equids may enhance the current understanding of the haematologic values, which in turn may assist in equipping veterinarians with the ability to establish an accurate interpretation of laboratory data, critical in diagnosis, prognosis and treatment of diseases in donkeys.
References
Abdelatif AM, Alameen AO (2012) Influence of season and pregnancy on thermoregulation and haematological profile in crossbred dairy cows in tropical environment. Glob Vet 9:334–340
Adenkola AY, Ayo JO, Asala OO (2011) Variations in haematological parameters and erythrocyte osmotic fragility of pigs during hot-dry and harmattan season in northern guinea savanna zone of Nigeria. Niger J Physiol Sci 26:113–118
Altan O, Pabuccuoglu A, Koyanliogu S, Bayraktav H (2003) Effect of heat stress on oxidative stress, lipid peroxidative and some stress parameters in broilers. Br Poult Sci 44:545–550
Anderson BH, Watson DL, Colditz IG (1999) The effect of dexamethasone on some immunological parameters in cattle. Vet Res Commun 23:399–413
Aoki T, Ishii M (2012) Haematological and biochemical profiles in peripartum mares and neonatal foals (heavy draft horse). J Equine Vet Sci 32:120–176
Ashton N (2013) Physiology of red and white blood cells. Anaesth Intensive Care Med 14:261–266
Ayo JO, Dzenda T, Zakari FO (2008) Individual and diurnal variations in rectal temperature, respiratory, and heart rate of pack donkeys during the early rainy season. J Equine Vet Sci 28:281–288
Babeker EA, Elmansoury YHA, Suleem AE (2013) The influence of season on blood constituents of dromedary camel (Camelus dromedaries). Online J Anim Feed Res 3:1–8
Blench R (2004) The history and spread of donkeys in Africa. In: Starkey P, Fielding D (eds) Donkeys, People and Development. A Resource Book of the Animal Traction Network for Eastern and Southern Africa (ATNESA). ACP-EU Technical Centre for Agricultural and Rural Cooperation (CTA), Wageningen, p 244
Borioni M, Marinaro P, Celestini S, Del Sole F, Magro R, Zoppi D (2012) Effect of equestrian therapy and onotherapy in physical and psycho-social performances of adults with intellectual disability—a preliminary study of evaluation tools based on the ICF classification. Disabil Rehabil 34:279–297
Brommer H, Sloet Van Oldruitenborgh-Oosterban MM, Kessels B (2001) Haematological and blood biochemical characteristics of Dutch warmblood foals managed under three different rearing conditions from birth to 5 months of age. Vet Q 23:92–95
Cain JW, Krausman PR, Rosenstock SS, Turner JC (2006) Mechanisms of thermoregulation and water balance in desert ungulates. Wildl Soc Bull 34:570–581
Caldin M, Furlanello T, Solano-Gallego L, De Lorenzi D, Carli E, Tasca S, Lubas G (2005) Reference ranges for haematology, biochemical profile and electrophoresis in a single herd of Ragusana donkeys from Sicily (Italy). Comp Clin Path 14:5–12
Carrocio A, Cavataio F, Montallo G (2000) Intolerance to hydrolysed cow’s milk proteins in infants: clinical characteristic and dietary treatment. Clin Exp Allergy 30:1597–1603
Castanheira M, Paiva SR, Louvandini H, Landim A, Fiorvanti MCS, Paludo GR, McManus C (2010) Multivariate analysis for characteristics of heat tolerance in horses in Brazil. Trop Anim Health Prod 42:185–191
Cebulj-Kadunc N, Bozic M, Kosec M, Cestnik V (2002) The influence of age and gender on haematological parameters in Lipizzan horses. J Vet Med 49:217–221
Cetin N, Bekyurek T, Cetin E (2009) Effect of sex, pregnancy and season on some haematological and biochemical blood values in Angora rabbits. Scand J Lab Anim Sci 36:155–162
Criscione A, Cunsolo V, Bordonaro S, Guastella AM, Saletti R, Zuccaro A, Marletta D (2009) Donkeys’ milk protein fraction investigated by electrophoretic methods and mass spectrometric analysis. Int Dairy J 19:190–197
Cuniberti B, Badino P, Odore R, Girardi C, Re G (2012) Effects induced by exercise on lymphocyte B-adrenergic receptors and plasma catecholamine levels in performance horses. Res Vet Sci 92:116–120
Dmoch M, Polonis A, Saba L (2008) Influence of seasons on the haematological and biochemical parameters of blood in horses. Med Weter 64:930–933
Ekenyem BU, Madubruke FN (2000) Haematological and serum biochemistry of grower pigs fed varying levels of Ipomoea asarifolia leaf meal. Pak J Nutr 6:603–606
Esonu BO, Emenalom OO, Udedebie U, Herbert DF, Ekpori IC, Iheukwuemere FC (2001) Performance and blood chemistry of weaner pigs fed raw mucuna bean (velvet bean) meal. Trop Anim Prod Invest 4:141–150
Etana KM, Jenbere TS, Bojia E, Negusie H (2011) Determination of reference haematological and serum biochemical values for working donkeys of Ethiopia. Vet Res 4:90–94
Etim NN, Williams ME, Akpabio U, Offiong EE (2013) Haematological parameters and factors affecting their values. Sci Educ Cent N Am 2:37–47
Eze JI, Onunkwo JI, Shoyinka SVO, Chah FK, Ngene AA, Okolinta N, Onyenwe IW (2010) Haematological profiles of pigs raised under intensive management system in South-Eastern Nigeria. Niger Vet J 31:115–123
Farooq H, Samad HA, Sajjad S (2011) Normal reference haematological values of one-humped camels (Camelus dromedarius) kept in Cholistan desert. J Anim Plant Sci 21:157–160
Fazio F, Assenza A, Tosto F, Casella S, Piccione G, Caola G (2011) Training and haematochemical profile in thoroughbreds and standardbreds: a longitudinal study. Livest Sci 141:221–226
Folch P, Jordana J, Cuenca R (1997) Reference ranges and the influence of age and sex on haematological values of the endangered Catalonian donkey. Vet J 154:163–168
Gaspar-López E, Landete-Castillejos T, Estévez JA, Ceacero F, Gallego L, García AJ (2010) Biometrics, testosterone, cortisol and antler growth cycle in Iberian red deer (Cervus elaphus hispanicus). Reprod Domest Anim 45:243–249
Gill J, Kompanowska-Jezierska E (1986) Seasonal changes in the red blood cell indices in Arabian broodmares and their foals. Comp Biochem Physiol 83:643–651
Gill J, Szwarocka-Priebe T, Krupska U, Peplowska Z (1979) Seasonal changes in haematological indices, protein and glycoprotein levels and in activity of some enzymes in Arabian horses. Bull Acad Pol Sci Biol 26:719–723
Girardi AM, Marques LC, De Toledo CZP, Barbosa JC, Maldonado Jr, W, Jorge RLN, Da Silva Nogueira CA (2013) Biochemical profile of the Pêga donkey (Equus asinus) breed: influence of age and sex. Comp Clin Path 1–7
Girardi AM, Marques LC, De Toledo CZP, De Campos FE (2014) Hematological variables of the Pęga donkey (Equus asinus) breed: influence of age and sex. Comp Clin Path. doi:10.1007/s00580-014-1905-y
Goundasheva D, Hubenov H, Kostov K, Karadjov T (2005) Changes in levels of some innate immune response parameters, blood vitamins E and A in stallions, following castration. Trakia J Sci 3:1–4
Grondin TM, Dewitt SF (2010) Normal haematology of the horse and donkey. In: Weiss DJ, Wardrop KJ (eds) Schalm's Veterinary Haematology. Wiley Blackwell Inc., Ames, IA, pp 821–828
Gul ST, Ahmad M, Khan A, Hussain I (2007) Haemato-biochemical observations in apparently healthy equine species. Pak Vet J 27:155–158
Gupta AK, Kumar S, Pal Y (2002) Biochemical, haematologcal and thyroid hormone profile in healthy Indian Kathiawari horses. Asian Australas J Anim Sci 15:1215–1221
Gurgoze SY, Icen H (2010) The influence of age on clinical biochemical parameters in pure-bred Arabian mares. J Equine Vet Sci 30:569–574
Hanzawa K, Watanabe S (2000) Changes in osmotic fragility of erythrocytes during exercise in athletic horses. J Equine Sci 11:51–61
Harvey JW, Asquith RC, Patel MG, Kiripelto J, Chen CL, Ott EA (1994) Haematological findings in pregnant, postparturient and nursing mares. Comp Haematol Int 4:25–29
Hassanein LH (2010) The physiological and physical response to capture stress in sharks. Plymouth Stud Sci 4:413–422
Hernández AM, Satué K, Lorente C, Garcés C, O’connor JE (2008) The influence of age and gender on haematological parameters in Spanish Horses. Proc Vet Eur Equine Meeting - XIV SIVE Congress, Venice (Italy)
Hesta M, Ottermans C, Krammer-Lucas S, Zentek J, Helweg P, Buyse J (2008) The effect of vitamin C supplementation in healthy dogs on antioxidative capacity and immune parameters. J Anim Physiol Anim Nutr 93:26–34
Hetem RS, Strauss WM, Heusinkveld BG, De Bie S, Prins HHT, Van Wieren SE (2011) Energy advantages of orientation to solar radiation in three African ruminants. J Therm Biol 36:452–460
Hinchcliff KW, Geor RJ, Pagan E (2002) Equine exercise physiology. Equine Vet J 34:23–26
Holub M, Beran O, Kaspříková N, Chalupa P (2012) Neutrophil to lymphocyte count ratio as a biomarker of bacterial infections. Cent Eur J Med 7:258–261
Huynh TTT, Aarnink AJA, Verstegen MWA, Gerrits WJJ, Heetkamp MJW, Kemps B, Canh TT (2005) Effects of increasing temperatures on physiological changes in pigs at different relative humidities. J Anim Sc 83:1385–1396
Isaac LJ, Abah G, Akpan B, Ekaette IU (2013) Haematological properties of different breeds and sexes of rabbits. Proc 18th Annual Conference Anim Sci Assoc Nig Pp. 24–27
Iyayi EA (2001) Cassava leaves as supplements for feeding weaner swine. Trop Anim Prod Invest 4:141–150
Johnstone CP, Reina RD, Lil A (2012) Interpreting indices of physiological stress in free living vertebrates. J Comp Physiol 182:861–879
Kalai K, Nehete RS, Ganguly S, Ganguli M, Dhanalaksmi S, Mukhopadhayay SK (2012) Investigation of parasitic and bacterial diseases in pigs with analysis of haematological and serum biochemical profile. J Parasit Dis 36:129–134
Karatosidi D, Marsico G, Tarvicone S (2013) Modern use of donkeys. Iran J Appl Anim Sci 3:13–17
Kedzierski W, Bergero D, Assenza A (2009) Trends of hematological and biochemical values in the blood of young race horses during standardized field exercise tests. Acta Vet 59:457–466
Kelani OL, Durotoye LA (2002) Haematological responses of the African giant rat (Cricetomys gambianus) to castration and androgen replacement. Vet Arh 72:39–49
Kida K (2002) The metabolic profile test: its practicability in assessing feeding management and periparturient diseases in high yielding commercial dairy herds. J Vet Med Sci 64:557–563
Kimura B, Marshall FB, Chen S, Rosenbom S, Moehlman PD, Tuross N, Sabin RC, Peters J, Banch B, Yahnunes H, Kebede F, Teclai R, Beja-Pereira A, Mulligan CJ (2011) Ancient DNA from Nubian and Somali wild ass provides insights into donkey ancestry and domestication. Proc R Soc Br Biol Sci 278:50–57
Koubkova M, Knizkova I, Kunc P, Hartlova H, Flusser J, Dolezal O (2002) Influence of high environmental temperature and evaporative cooling on some physiological, haematological and biochemical parameters in high-yielding dairy cows. Czech J Anim Sci 47:309–318
Kral L, Suchy P (2000) Haematological studies in adolescent breeding cocks. Acta Vet Brno 69:189–194
Krumrych W (2009) Effect of physical exercise on oxygen metabolism of neutrophils in horses. Bull Vet Inst Pulawy 53:97–103
Kumar B, Pachaura SP (2000) Haematological profile of crossbred dairy cattle to monitor herd status at medium elevation in central Himalayas. Res Vet Sci 69:141–145
Kumar S, Sahu NP, Pal AK, Choudhury D, Yengkokpam S, Mukherjee SC (2005) Effect of dietary carbohydrate on haematology, respiratory burst activity and histological changes in Labeo rohita juveniles. Fish Shellfish Immunol 19:331–344
Lacerda L, Campos R, Sperb M, Scares E, Barbosa P, Godinho E, Ferreira R, Santos V, Gonzalez F (2006) Haematologic and biochemical parameters in three high performance horse breeds from Southern Brazil. Arch Vet Sci 11:40–43
Lemma A, Moges M (2009) Clinical, haematological and serum biochemical reference values of working donkeys (Equus asinus) owned by transport operators in Addis Ababa, Ethiopia. Heart 36:38–3
Lin H, Jiao HC, Buyse J, Decuypere E (2009) Strategies for preventing heat stress in poultry. Worlds Poult Sci J 62:71–86
Lorena D, Da Ponte A, Cozzi M, Carbone A, Pomati M, Nava I, Cappellini MD, Fiorelli G (2006) Changes in erythropoiesis iron metabolism and oxidative stress after half-marathon. Intern Emerg Med 1:30–34
Mansueto P, Iacono G, Taormina G, Seidita A, D’Alcamo A, Adragna FR, Carta M, Rini G, Carrocio A (2013) Asses milk in allergy to cow’s milk protein: a review. Acta Med Mediterr 29:153
Mao X, Gu J, Sun Y, Xu S, Zhang X, Yang H, Ren F (2009) Antiproliferative and anti-tumour effect of active components in donkey milk on A549 human lung cancer cells. Int Diary J 19:703–708
Marshall F (2007) African pastoral perspectives on domestication of the donkey: a first synthesis. In: Denham TP, Iriarte J, Vrydaghs L (eds) Rethinking agriculture: archaeological and ethnoarchaeological perspectives. Walnut Creek, California, pp 537–594
Marshall F, Weissbrod L (2011) Domestication processes and morphological change. Curr Anthropol 52:397–413
McFarlane D, Sellon DC, Gibbs SA (2001) Age-related quantitative alterations in lymphocyte subsets and immunoglobulin isotypes in healthy horses. Am J Vet Res 62:1413–1417
Melo SKM, Lira LBD, Almeida TLA, Rego EW, Manso HEC, Manso Filho HC (2013) Hematological parameters and blood biochemistry in pleasure horses in tropical region. Ciên Anim Bras 14:208–215
Mikniene Z, Maslauskas K, Kerziene S, Kucinskiene J, Kucinskas A (2014) The effect of age and gender on blood haematological and serum biochemical parameters in Zemaetukai horses. Vet Med Zootec 65:37–43
Minka NS, Ayo JO (2007) Effect of shade provision on some physiological parameters, behaviour and performance of pack donkeys (Equus asinus) during the hot-dry season. J Equine Sci 18:39–46
Miranda RLD, Mundim AV, Saquy ACS, Costa ÁS, Guimarães EC, Gonçalves FC, Silva FOC (2011) Hematologic profile of horses subjected to Team Penning. Pesqui Vet Bras 31:81–86
Mirzadeh K, Tabatabaei S, Bojarpour M, Mamoei M (2010) Comparative study of hematological parameters according strain, age, sex, physiological status and season in Iranian cattle. J Anim Vet Adv 9:2123–2127
Mmereole FUC (2008) The effects of replacing groundnut cake with rubber seed meal on the haematological and serological indices of broilers. Int J Poult Sci 7:622–624
Monti G, Bertino E, Muratore MC, Coscia A, Cresi F, Silvestro L, Fabris C, Fortunato D, Giuffrida MG, Conti A (2007) Efficacy of donkey’s milk in treating highly problematic cow’s milk allergic children: an in vivo and in vitro study. Paediatr Allergy Immunol 18:258–264
Mori E, Fernandes WR, Mirandola RMS, Kubo G, Ferreira RR, Oliveira JV, Gazek F (2003) Reference values on serum biochemical parameters of the Brazilian donkeys (Equus asinus) breed. J Equine Vet Sci 23:356–364
Mori E, Mirandola RMS, Ferreira RR, Oliveira JV, Gacek F, Fernandes WR (2004) Reference values on haematologic parameters of the Brazilian donkeys (Equus asinus) breed. J Equine Vet Sci 24:271–276
Moyes CD, Fragoso N, Musyl MK, Brill RW (2006) Predicting postrelease survival in large pelagic fish. Trans Am Fish Soc 135:1389–1397
Mueller PJ, Jones MT, Rawson RE, Van Soest PJ, Hintz HF (1994) Effect of increasing work rate on metabolic responses of the donkeys (Equus asinus). Am Physiol Soc 77:1431–1438
Muñoz A, Ribeiro C, Santisteban R, Lucas RG, Castejon FM (2002) Effect of training duration and exercise on blood-borne substrates, plasma lactate and enzyme concentrations in Andalusian, Anglo-Arabian and Arabian breeds. Equine Vet J 34:245–251
Muñoz A, Riber C, Trigo P, Castejón F (2010) Hematology and clinical pathology data in chronically starved horses. J Equine Vet Sci 30:581–589
Muñoz A, Riber C, Trigo P, Castejón F (2012) Age and gender-related variations in haematology, clinical biochemistry, and hormones in Spanish fillies and colts. Res Vet Med 93:943–949
Muraro MA, Giampieto PG, Galli E (2002) Soy formulas and nonbovine milk. Ann Allergy Asthma Immunol 89:97–101
Nasyrova DI, Sapronova AY, Nigmatullina RR, Ugryumov MV (2006) Changes in blood plasma volume in rats during ontogenesis. Russ J Dev Biol 27:1062–3604
Okonkwo JC, Okonkwo IF, Ebyh GU (2011) Effect of breed, sex and source within breed on the haematological parameters of the Nigerian goats. Online J Anim Feed Res 1:8–13
Olaifa F, Ayo JO, Ambali SF, Rekwot PI (2012) Haemato-biochemical responses to packing in donkeys administered with ascorbic acid during the harmattan season. J Vet Med Sci http//www.ncbi.nlm.nih.gov/pubmed/23154452
Orozco CAG, Martins CB, D’Angelis FHDF, Oliveira JVD, Lacerda-Neto JCD (2007) Haematological values and total protein of Brasileiro de Hipismo and Breton mares during pregnancy. Ciênc Rural 37:1695–1700
Ovuru SS, Ekweozor IKE (2004) Haematological changes associated with crude oil ingestion in experimental rabbits. Afr J Biotechnol 3:346–348
Padalino B, Rubino G, Lacinio R, Petazzi F (2014) Observations on the hematology of Standardbred horses in training and racing in Southern Italy. J Equine Vet Sci 34:398–402
Pandey N, Kataria N, Kataria AK, Joshi A (2012) Ambient stress associated variations in metabolic responses of Marwari goat of arid tracts in India. J Stress Physiol Biochem 8:120–127
Petrov V, Lyutskanov M, Kanakov D (2011) Effects of spontaneous and experimental colibacteriosis on some haematological and blood biochemical parameters in weaned rabbits. Bulg J Vet Med 14:238–246
Piccione G, Assenza A, Fazio F, Giudice E, Caola G (2001) Different periodicities of some haematological parameters in exercise-loaded athletic horses and sedentary horses. J Equine Sci 12:17–23
Piccione G, Grasso F, Fazio F, Giudice E (2008) The effect of physical exercise on the daily rhythm of platelet aggregation and body temperature in horses. Vet J 176:216–220
Pritchard JC, Burn CC, Barr ARS, Whay HR (2009) Haematological and serum biochemical reference values for apparently healthy working horses in Pakistan. Res Vet Sci 87:389–395
Quiñonero J, García-Santamaría C, María-Dolores E, Armero E (2009) Physiological indicators of stress in gestating sows under different cooling systems. Pesq Agrop Bras 44:1549–1552
Rajion MA, Saat IM, Zulkifli I, Goh YM (2001) The effects of road transportation on some physiological stress measures in goats. Asian-Australas J Anim Sci 14:1250–1252
Rose RJ, Hodgson DR (1994) Haematology and biochemistry. In: Rose RJ, Hodgson DR (eds) The athletic horse: principles and practice of equine sport medicine. WB Saunders, Philadelphia, pp 63–76
Rossel S, Marshall F, Peters J, Pilgram T, Adams MD, O’Connor D (2008) Domestication of the donkey: New data on timing, processes and indicators. Proc Natl Acad Sci 105:3715–3720
Rovira S, Muñoz A, Benito M (2007) Hematologic and biochemical changes during canine agility competitions. Vet Clin Path 36:30–35
Ruiz G, Rosenmann M, Cortes A (2004) Thermal acclimation and seasonal variations of erythrocyte size in the Andean mouse Phyllotis xanthopygus rupestres. Comp Biochem Physiol 139:405–409
Sattar A, Mirza RH (2009) Haematological parameters in exotic cows during gestation and lactation under subtropical conditions. Pak Vet J 29:129–132
Satué K (2004) Hematología en la yegua Pura Raza Española de Estirpe Cartujana. Doctoral Thesis. Departament of Animal Medicine and Surgery. CEU-Cardenal Herrera University, 154 pp
Satue K, Blanco O, Munoz A (2009) Age-related differences in the haematological profile of Andalusian broodmares of Carthusian strain. Vet Med-Czech 54:175–182
Satué K, Hernández A, Lorente C, O’Coonor JE (2010a) Immunophenotypical characterization in Andalusian horse:variations with age and gender. Vet Immunol Immunopathol 133:219–227
Satué K, Muñoz A, Blanco O (2010b) Pregnancy influences the hematological profile of Carthusian broodmares. Pol J Vet Sci 13:393–394
Satué K, Muñoz A, Montesinos P (2011). Seasonal variations in the erythrogram in pregnant Carthusian mares. Proceedings of 13th Conference of the European Society of Veterinary Clinical Pathology, 9th Conference of Association Des Eleveurs De Chevaux, Des Cavaliers Et Des Propertaires, 12th American College of Clinical Pharmacy and American Society for Veterinary Clinical Pathology, 31 August - 3 September, Dublin, Ireland, Pp. 65–73
Scharf BA (2008) Comparison of thermoregulatory mechanisms in heat sensitive and tolerant breeds of Bos taurus cattle. MSc thesis, University of Missouri-Columbia
Semple JW, Italiano JE, Freedman J (2011) Platelets and the immune continuum. Nat Rev Immunol 11:264–274
Sgorbini M, Bonelli F, Rota A, Baragli P, Marchetti V, Corrazza M (2013) Haematology and clinical chemistry in Amiata donkey foals from birth to 2 months of age. J Equine Vet Sci 33:35–39
Silanikove N (2000) Effects of heat stress on the welfare of extensively managed domestic ruminants. Livest Prod Sci 67:1–18
Šimpraga M, Šmuc T, Matanović K, Radin L, Shek-Vugrovečki A, Ljubičić I, Vojta A (2013) Reference intervals for organically raised sheep: effects of breed, location and season on hematological and biochemical parameters. Small Rumin Res 112:1–6
Singh MK, Gupta AK, Yadav MP (2005) The donkey: its role and the scope for better management. Livest Int 9:18–20
Sneddon JC, Boomker E, Howard CV (2006) Mucosal surface area and fermentation activity in the hind gut of hydrated and chronically dehydrated working donkeys. J Anim Sci 84:119–124
Stanger KJ, Ketheesan N, Parker AJ, Coleman CJ, Lazzaroni SM, Fitzpatrick LA (2005) The effect of transportation on the immune status of Bos indicus steers. J Anim Sci 83:2632–2636
Starkey P, Starkey M (2004) Regional and world trends in donkey populations. In: Starkey P, Fielding D (Eds). Donkeys, people and development. A resource book of the Animal Traction Network for Eastern and Southern Africa (ATNESA), (ACP-EU Technical Centre for Agricultural and Rural Cooperation (CTA), Wageningen, The Netherlands, http://www.atnesa.org/donkeys-starkey-populations, retrieved 2010-08-19
Tafaro A, Magrone T, Jirillo F, Martemucci G, D’alessandro A, Amati L, Jirillo E (2007) Immunological properties of donkey’s milk: its potential use in the prevention of atherosclerosis. Curr Pharm Des 13:3711–3717
Tibbo M, Jibril T, Woldemeskel M, Dawo F, Aragaw K, Rege JEO (2004) Factors affecting haematological profiles in three Ethiopian indigenous goat breeds. Int J Appl Res Vet Med 2:297–309
Tomenenendalova J, Vodicka R, Uhrikova I, Doubek J (2014) Determination of haematological and biochemical parameters of Przewalski horses (Equus Przewalskii) kept by the Prague zoo. Vet Med-Czech 59:11–21
Uluisik D, Keskin E, Ozaydin T (2013) Age and gender related changes in hematological parameters of thoroughbred foals. Biotech Histochem 88:345–349
Vleck CM, Vertalino N, Vleck D, Bucher TL (2000) Stress, corticosterone, and heterophil to lymphocyte ratios in free-living Adelie penguins. Condor 102:392–400
Von Vietinghoff S, Ley K (2008) Homeostatic regulation of blood neutrophil counts. J Immunol 181:5183–5188
Walsh SR, Cook EJ, Goulder F, Justin TA, Keeling NJ (2005) Neutrophil‐lymphocyte ratio as a prognostic factor in colorectal cancer. J Surg Oncol 91:181–184
Yaqub LS, Kawu MU, Ayo JO (2013) Influence of reproductive cycle, sex, age and season on haematologic parameters in domestic animals: a review. J Cell Anim Biol 7:37–43
Zazula AD, Précoma-Neto D, Gomes AM, Kruklis H, Barbieri GF, Forte RY, Faria Neto JR (2008) An assessment of neutrophils/lymphocytes ratio in patients suspected of acute coronary syndrome. Arq Bras Cardiol 90:31–36
Zinkl JG, Mae D, Merida PG, Farver TB, Humble JA (1990) Reference ranges and the influence of age and sex on haematologic and serum biochemical values in donkeys (Equus asinus). Am J Vet Res 51:408–413
Zobba R, Ardu M, Niccolini S, Cubeddu F, Dimauro C, Bonelli P, Pinna Parpaglia ML (2011) Physical, hematological, and biochemical responses to acute intense exercise in polo horses. J Equine Vet Sci 31:542–548
Conflict of interests
The authors have not declared any conflicts of interest.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
Open Access This article is distributed under the terms of the Creative Commons Attribution License which permits any use, distribution, and reproduction in any medium, provided the original author(s) and the source are credited.
About this article
Cite this article
Zakari, F.O., Ayo, J.O., Rekwot, P.I. et al. Effect of age, sex, physical activity and meteorological factors on haematological parameters of donkeys (Equus asinus). Comp Clin Pathol 25, 1265–1272 (2016). https://doi.org/10.1007/s00580-014-2026-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00580-014-2026-3