Blood, Milk and Meat Vitamin D in the Dromedary Camel

Iranian Journal of Applied Animal Science

مقاله 1، دوره 9، شماره 4، اسفند 2019، صفحه 585-595   

نوع مقاله: Review Article

نویسندگان

M. El Khasmi^{* 1}؛ B. Faye²

¹Laboratory of Physiopathology and Molecular Genetics, Ben M'Sik Faculty of Science, Hassan II University of Casablanca, BP 7955 Sidi Othmane, Casablanca, Morocco

²Center for International Cooperation in Agronomic Research for Development (CIRAD), Unité Mixte de Recherche Systèmes d’Elevage Méditerranéens et Tropicaux (UMR SELMET), Campus International de Baillarguet, TA C/dir B 34398 Montpellier, Montpellier, France

چکیده

In ruminants, circulating vitamin D levels may be influenced by photoperiod, nutrition, physiological stage, ambient temperature, attitude and season, whereas, in meat, vitamin D content may be impacted by vitamin D status of animal, ageing and cooking. The information on nutritional value of camel milk and meat is largely available, but, there are very few reports evaluating the vitamin D levels and their variations in blood and these products in the dromedary camel. In this context, this review proposes a gathering of current knowledge about the vitamin D in this species and discusses findings considering those obtained in other mammal animals.

کلیدواژه‌ها

blood؛ Milk؛ meat؛ oxidant stress؛ 25-hydroxyvitamin D

اصل مقاله

INTRODUCTION

In mammal species, the physiological control of phosphocalcic metabolism and skeletal remodeling is normally under regulation of systemic hormones (especially calcitonin and parathormone) and vitamin D (Holick, 2007). Vitamin D has a double origin: (i) exogenous origin for vitamin D₂ or ergocalciferol in plant, and for Vitamin D₃ or cholecalciferol in animal tissues and milk), (ii) endogenous origin by skin conversion of 7-dehydrocholesterol to vitamin D₃ in the presence of sunlight. Historically, vitamin D deficiency has been associated with osteomalacia, osteopenia, osteoporosis and muscle weakness, illustrating the crucial role of vitamin D in bone mineralization and calcium (Ca) absorption. It regulates the Ca and phosphorus (P) levels in the bloodstream and promotes the healthy growth and bone turnover. These actions are mediated by the vitamin D receptor (VDR), which is principally located in the nuclei of target cells. When the calcitriol binds to the VDR, this later acts as a transcription factor by modulating the gene expression of transport proteins (such as TRPV6 and calbindin), which can enhance the intestinal Ca absorption (Holick, 2007). Vitamin D may also play a protective role against hypertension, cardiovascular disease and some cancers and be an important modulator of the immune system by modulating the action of many genes. So, low levels of serum 25-hydroxyvitamin D (25-OH-D) seem to be associated with heart diseases, cancers, diabetes, immune deficiency, depression, neuro-degeneration and chronic pain (Holick and Chen, 2008). Vitamin D metabolism and status in camel was investigated by few authors. Yet, camels who are occupying an essential place in the rural life of the arid and semi-arid regions of Africa and Asia, are an important potential purveyor of milk and meat, in acceptable quantity and quality when other ruminants cease all production or fail to survive (Faye, 2014). Camel meat is known by lower levels of fat and cholesterol, higher amounts of essential amino acids, polyunsaturated fatty acids (PUFAs), but also minerals and vitamins including vitamin D, in comparison to other red meats (Kadim et al. 2006; El Khasmi et al. 2013a; Raiymbek et al. 2015). Camel milk is known also for its richness in some vitamins as vitamin C and D (Farah et al. 1992; Riad et al. 1994). Thus, highlighting physiological role of this hormone justifies its growing interest. The present review proposes a gathering of current knowledge about the vitamin D in the dromedary camel and discusses findings in light of those obtained in other mammalian animals.

 

Metabolism and role of vitamin D

The two major natural sources of vitamin D to most vertebrate animals and humans result from photochemical conversion of 7-dehydrocholesterol to vitamin D₃ by the action of ultraviolet light at wavelengths between 295 and 297 nm on the epidermal strata of the skin (Crissey et al. 2003), or from plants as a result of photochemical conversion of ergosterol to vitamin D₂. Once vitamin D is in the liver, it is converted to 25-OH-D (Holick, 2007). This metabolite is the major circulating form of vitamin D under normal conditions (Zerwekh, 2008). The 25-OH-D is converted to several polar metabolites. However, from all known vitamin D₂ and D₃ metabolites, only the function of 1, 25-dihydroxyvitamin D [1α,25(OH)₂D₃] or calcitriol (produced predominantly in the kidney) has been established. Calcitriol maintains the plasma calcium and phosphorus levels by increasing the expression of the epithelial calcium channel-TRPV6 and the intracellular calcium transporter-calbindin 9 K (Holick, 2007). In human, circulating levels of 25-OH-D are largely linked to the consumption of oily fish, margarine and foods containing vitamin D, exposure to sunlight (Zerwekh, 2008), epidermal concentration of 7-dehydrocholesterol, melanin pigmentation, latitude, season, and exposure time of day (Olmos-Ortiz et al. 2015). Exposure of rats to ultraviolet light leads to a 40-fold increase in vitamin D. In contrast, similar irradiation of dogs and cats does not significantly increase dermal vitamin D concentration (How et al. 1994). Most herbivores can produce vitamin D in response to ultraviolet irradiation of the skin, as indicated by the higher concentrations of serum vitamin D in shorn sheep compared with unshorn sheep (Hidiroglou et al. 1985). Furthermore, when transferred to lower altitudes or higher latitudes where solar radiation is much lower, serum vitamin D concentrations in llamas and alpacas decline to low levels, especially during winter (Van Saun et al. 1996). Baby lamas born in autumn/winter that had lower vitamin D concentrations were more likely to develop rickets than those born in summer (Van Saun et al. 1996). Vitamin D is transported in the plasma bound to the specific protein transcalciferin or to vitamin D-binding protein. The 25-OH-D₃ is a poor ligand for VDR, with an approximate 1% cross reactivity with these receptors compared with 1,25-(OH)₂D₃ when both are in their free state (Reinhardt et al. 1982). In addition, only about 0.03% of serum 25-OH-D₃ is free for cell entry (Schwartz et al. 2014). The actions of 1α, 25(OH)₂D₃ in multiple target tissues are mediated by the nuclear VDR, a phosphoprotein that binds the hormone with high affinity. Serum 25-OH-D level is the best marker of whole-body vitamin D status (Holick, 2007). Hypocalcemia induces the secretion of parathormone by the parathyroid gland, which reduces the excretion of Ca, inhibits phosphate reabsorption and stimulates the production of 1α,25(OH)₂D₃ in the kidneys. Then, calcitriol will increase the active phosphate transport in the intestines and stimulate Ca reabsorption in the kidney. The entry of Ca through the luminal membrane and the action of calbindin D9k which facilitates the transfer of cytoplasmic Ca across the basolateral membrane, are the major mediators of intestinal Ca absorption (Holick, 2007; Zerwekh, 2008). The 1α,25(OH)₂D₃ also stimulates osteoblast differentiation and gene expression biomarkers of bone turnover such as osteocalcin and osteoponine. When 1α,25(OH)₂D₃ is produced in large quantities, osteocytes secrete fibroblast growth factor 23 (FGF23) as inhibitor of phosphate reabsorption and calcitriol production in the kidney (Holick, 2007; Zerwekh, 2008).

 

Vitamin D and phosphocalcic metabolism

It is largely known that vitamin D plays a major role in bone mineralization and Ca balance and a deficit in vitamin D is associated with rickets in children, and exacerbation of osteoporosis and osteomalacia in adults. Moreover, several researches showed that vitamin D plays an important role as an agent preventing or delaying the onset of certain autoimmune (diabetes type I) and proliferative diseases (solid cancers, leukemia, psoriasis) (Holick, 2007). The measurement of circulating levels of 25-OH-D is a more reliable biomarker of vitamin D status, so, according to Horst et al. (1983), vitamin D deficiency in bovine species could lead to circulating rates below 5 ng/mL. In the dromedary camel, the circulating levels of vitamin D metabolites were 10 to 15 times higher than those of sheep and cattle, without any significant change in calcemia or phosphatemia (Table 1). In ovine species and their newborns, the minimum daily intake of vitamin D required to prevent rickets are respectively 5.6 and 6.7 IU/kg birth weight (NRC, 1985).

 

Table 1 Circulating levels of vitamin D and its metabolites in domestic ruminants

 

 

Cases of rickets related to vitamin D deficiency have been reported in newborn lamb (Van Saun, 2004), sheep (Bonniwell et al. 1988) and llamas (Van Saun et al. 1996). In young camel, this vitamin deficiency is the primary cause of rickets consecutive to hypophosphatemia (Kistral- Boneh et al. 1990). In addition, decreased bone mineral density is largely associated with a decrease in serum vitamin D and may predispose some alpacas to post traumatic fractures (Parker et al. 2002). According to Van Saun et al. (1996), the hypophosphatemia and vitamin D deficiency observed in camelids could be corrected by treatment with a supplement of vitamin D. In addition, in North Africa, the phosphorus deficiency observed in camel species is responsible for Krafft disease, which had been described for long time (Kchouk and Durand, 1958) and leads to arthritis and periarticular exostoses, then to musculoskeletal disorders followed by paralysis (Faye and Bengoumi, 2000).

 

Vitamin D and lactation

Higher rates of vitamin D metabolites were observed in lactating camels and their newborns compared with the empty non-lactating female for similar, unchanged, calcemia in both animal groups (Riad et al. 1994; El Khasmi et al. 2000). The higher plasma levels of 25-OH-D and 1α,25(OH)₂D, could probably potentiate the processes of phosphocalcic assimilation and accelerate the resorption phenomenon of the mother's bone, to meet the requirements for lactogenesis. Liesegang et al. (2006) reported in goat and sheep that circulating levels of 1α,25(OH)₂D₃ became very high in the first postpartum week, indicating an activation of bone remodeling which is able to compensate the Ca transfer from maternal skeleton to milk. In addition, the high absorption coefficients measured during lactation in camel by comparison to those observed in other domestic ruminants (Faye and Bengoumi, 2000), may be explained by the high levels of 1α,25(OH)₂D₃ (El Khasmi et al. 2000) to survive in the desert with low resources of Ca and P. In 4- to 6-month-old camels, the use of the stable strontium assay for functional exploration of intestinal Ca absorption has shown that intravenous injection of 1α,25(OH)₂D₃ stimulates the calcium absorption (El Khasmi et al. 2003). This brings us back to associating hypercalcemia in the newborn camel, and maintenance of calcium homeostasis in lactating camel, at their high levels of 25-OH-D and 1α,25(OH)₂D₃. Circulating levels of 1α,25(OH)₂D₃ in cattle (Naito et al. 1983; Rajaraman et al. 1997) and camel neonates (El Khasmi et al. 2000) increased significantly during the first postpartum days, probably as a result of increased biosynthesis of this metabolite in response to active intestinal phosphate absorption in newborn. Moreover, in newborn calves that received vitamin D (54.00 IU at a rate of 13.500 IU/week), Nonnecke et al. (2009) observed a positive correlation between plasma levels of Ca and those of 1α,25(OH)₂D₃. In domestic ruminants, treatment with vitamin D, 25-OH-D or 1α,25(OH)₂D₃ at pharmacological doses, by oral or parenteral way during few days before parturition, increases simultaneously the intestinal reabsorption of Ca and the circulating levels of calcitriol, which could prevent postpartum hypocalcemia secondary to milk production (Okura et al. 2004; Taylor et al. 2008). In addition, hypercalcemic and hyperphosphatemic effects have been observed following intramuscular injection of 1α-OH-D in cattle (Riad et al. 1987) and camel (Riad et al. 1994), and intravenous administration of 1α,25(OH)₂D₃ in the latter species (El Khasmi et al. 2001a). The degree of neonatal renal maturity to convert 25-OH-D to 1α,25(OH)₂D₃ varies among species. Thus, in lamb, tritiated 25-OH-D, administered just after birth, was metabolized to 1α,25(OH)₂D₃ only after the 18th postnatal day (Collignon et al. 1996). However, in the case of camel, the levels of 1α,25(OH)₂D₃ start to increase in the bloodstream as early as the 7^th day of life, indicating a degree of early maturation of renal function, in the synthesis of 1α,25(OH)₂D₃. This metabolite is one of the major determinants of the regulation of phosphocalcic metabolism and bone mineralization. To maintain milk production, the daily requirement of Ca in early lactation is about 100 g in cow (Allen and Samson, 1985). Vitamins D₃ and D₂ also can be supplemented in the ruminant diet by commercially available crystalline forms (Wolter, 1988). During this physiological stage, domestic ruminants respond to an exogenous supply of 1α,25(OH)₂D₃ by hypercalcemia, hyperphosphatemia and increase of phosphocalcic excretion by the mammary glands (Okura et al. 2004; Yamagishi et al. 2005; Namioka et al. 2008). Indeed, camels in third lactation that received 1α,25(OH)₂D₃ intravenously, showed a significant increase in the concentration and excretion of Ca and P in milk (El Khasmi et al. 2001a). Similarly, according to Riad et al. (1994), in lactating camel the intramuscular injection of 1α-OH-D stimulates the secretion of both Ca and P in milk. The effects of metabolites of vitamin D observed to maintain milk production in female, could be direct on the mammary gland, and not due to hypercalcemia and hyperphosphatemia consecutive to the treatment. In fact, in the same species, it was demonstrated that intravenous infusion of Ca gluconate (7 mg Ca/kg body weight) for 30 min, has no effect on mammary excretion of Ca and P (Riad et al. 1994). On the other hand, in cattle, specific receptors to calcitriol were demonstrated in mammary glands and their number increases dramatically during lactation (Colston et al. 1988). The effects of vitamin D on the mammary glands in camels are like those reported in cattle (Hidiroglou et al. 1985) and goats (Bengoumi et al. 1996). Finally, according to Smith et al. (1987), the status of vitamin D in the newborn lamb is positively correlated with that of its mother, and is also linked with the consumption of colostrum during the first days of lactation (Gay and Besser, 1991).

 

Vitamin D and reproduction

The breeding season of the Moroccan camels begins in November and ends in April, with decreasing then increasing daylight, while the non-breeding season is in summer which is strongly related to the increasing length of the photoperiod (Sghiri, 1988). In camel, activity of the leydig cells, becomes maximal during rutting season and is less active in non-breeding season with a resulting reduction in steroidogenic activity by the testes (Agarwal and Khanna, 1990). Investigations have suggested that vitamin D and the VDR are critical for the maintenance of reproduction and fertility in mammals (Corbett et al. 2006; Menegaz et al. 2009). So, Audet et al. (2009) reported that vitamin D supplementation enhanced the ejaculate volume but had no effect on sperm production or quality in boars. In human species, the 1α,25(OH)₂D₃ has specific receptors which predominates on the head/nucleus and mid-piece of the spermatozoa (Corbett et al. 2006), and appears to be a modulator of placental steroidogenesis (Barrera et al. 2007) and of follicle-stimulating hormone (FSH) secretion (Zofkova et al. 1989). In experimental cryptorchid mouse, Hirai et al. (2009) noted that 1α,25(OH)₂D₃ contributes to spermatogenesis by upregulating certain specific genes in sertoli’s cells and suggested that vitamin D supplementation may have implications for managing male infertility. Furthermore, in vitamin D-deficient male rats with incomplete spermatogenesis and degenerative testicular changes, Menegaz et al. (2009) suggested that calcitriol may play a critical role for the maintenance of normal reproduction via a genomic mechanism that can be triggered by protein kinase A (PKA) (PKA), as well as to a rapid response involving Ca²⁺/K⁺ channels on the plasma membrane. In another publication, it was concluded that low concentrations of vitamin D (Dabrowski et al. 2015). In a previous study in camel, we reported, that circulating level of 25-OH-D was lower in winter season (rutting period) than in summer (El Khasmi et al. 2011; Farh et al. 2018), suggesting that vitamin D doesn’t appear to contribute directly or indirectly to the psychological-neurological-endocrinology of camel reproduction. The higher circulating levels of 25-OH-D observed in our dromedary camels during the non-rutting period (summer) may be explained by the increasing daylight. In fact, interaction of photoperiod (intensity, duration, wavelength) with other factors (ambient temperature, nutrition, housing, latitude) and hormonal status (thyroid and corticosterone levels) (Zia-Ur-Rahman et al. 2007) can influence the reproductive performance of several mammalian species (Arthur, 1992). Melatonin has been proposed as the pineal hormone, and its timed administration replicates the effect of day length on seasonal breeding for example, in hamster (Cutty et al. 1981), sheep (Zaraazga et al. 1998) and camel (Al-Qarawi and Elmougy, 2008). However, although photoperiodic variations have a strong influence, there is some evidence suggesting that the suprachiasmatic nucleus is an important structure regulating circadian and seasonal rhythms of most biological functions and may be sensitive to changes in ambient temperature (Pando and Sassone-Corsi, 2001). In bovine species, vitamin D status is more linked with the consumption of foods, vitamin D supplementation, degree of skin pigmentation, and sunlight exposure than diet (Holick and Chen, 2008; Zerwekh, 2008). However, in camelids (Sumar, 1996) and other ruminants (Brown, 1994), the sexual activity which is essentially androgen induced phenomenon, is largely influenced by the nutritional status.

 

Milk vitamin D

Camel's milk includes proteins, fatty acids, minerals and vitamins resulting in a positive impact on human health (Elagamy, 2006; Konuspayeva et al. 2011). Generally, milk contains about 3 times less vitamin D than circulating concentration of vitamin D and 100 times less vitamin D than the circulating concentration of 25-OH-D (Greer et al. 1984). In the dromedary camel, milk is rich in 25-OH-D especially during the colostral phase, which is a non-negligible source of vitamin D, for the newborn camel in an environment where phosphocalcic resources are very limited (El Khasmi et al. 2001b; El Khasmi et al. 2005) (Table 2). In humans, it was suggested that conversion of vitamin D₃ into 25-OH-D₃ is reduced at high intakes of vitamin D₃ (Heaney et al. 2008). However, supplementing cows with 25-OH-D₃ in combination with a negative anionic diet for the last 13 d of gestation enhanced their serum concentrations of 25-OH-D₃ and 1,25-(OH)₂D₃ leading to an increase of 25-OH-D₃ content in colostrum and milk and in the serum of the neonatal calf (Weiss et al. 2015). So, in lactating cows, concentrations of this metabolite in colostrum and sixth milking day were correlated with their concentrations in serum (Weiss et al. 2015). There are several reports reviewing the influence of diet, Ultraviolet exposure and processing on vitamin D content in bovine milk. However, despite the significance of establishing the level of this vitamin in nutritional milk products (Holick et al. 1992), no study was carried out in the camel.

 

Meat vitamin D

Meat stands for strength, health and wealth, but it’s content of vitamin D was generally low, difficult to measure and had not been indicated at the beginning of food composition (Williams, 2007). A few numbers of foods (fish, meat, milk, eggs and dairy products) may naturally contain vitamin D, and the circulating levels of 25-OH-D are more influenced by vitamin D supplementation, sun exposure and diet (Holick and Chen, 2008). Among the compounds of camel meat, 25-OH-D is found at concentrations similar to those of other livestock, which could be a significant source of this vitamin for the populations in desert regions (El Khasmi et al. 2013a; El Khasmi et al. 2018; Tabite et al. 2018). In fact, in man, the circulating vitamin D concentrations are lower in vegetarians than in meat and fish eaters (Crowe et al. 2011). According to American Institute of Medicine Committee, a serum 25-OH-D level of 20 ng/mL is required for normal bone metabolism and overall health (Yetley et al. 2009). The prevalence of vitamin D deficiency (serum 25-OH-DVan Der Meer et al. 2008). Without doubt, in human, vitamin D is of great importance for health and therefore, recommendations for its intake have recently been increased considerably. In the dromedary camel, the levels of 25-OH-D₃ (ng/g) in muscle, liver and kidney were respectively 4.241 ± 1.045; 7.071 ± 1.003 and 6.154 ± 1.067 (El Khasmi et al. 2013b) and were close to those reported for meat of cattle (Foote et al. 2004; Cho et al. 2006) but slightly higher than those reported in other domestics species (Table 3). In the camel, although serum levels of 25-OH-D₃ were significantly higher in summer than in winter, meat, liver and kidney levels of 25-OH-D₃ showed no seasonal variation (Bargaa et al. 2015). According to studies conducted in New Zealand, the values (mg/100 g) of vitamin D₃ and 25-OH-D₃ were respectively 0.10 and 0.45 in beef and 0.04 and 0.93 in sheep (Cali et al. 1991). In an adult woman of 70 kg total vitamin D is 14,665 IU, 65% as vitamin D and 35% as 25-OH-D (Heaney et al. 2009). Nearly three-quarters of vitamin D is found in fats, while the 25-OH-D in the body was divided as follows: 20% in muscle, 30% in serum, 35% fat and 15% in other tissues. According to Schmid and Walther (2013), the content of vitamin D in muscle is generally much lower (up to 10 μg/g). The camel is an important source of red meat especially in arid and semiarid areas which adversely affect the performance of other meat animals (Kadim et al. 2006). The camel meat is rich in PUFAs (Kadim et al. 2006), myoglobin and other heme compounds (Hb) that could act as pro-oxidants and thus promote the oxidation of lipids (Maqsood and Benjakul, 2011). Lipid oxidation of meat takes place just after the slaughter of the animal, generates undesirable products, and causes the degradation of fat-soluble vitamins and essential fatty acids.

 

Table 2 Milk levels of vitamin D₃ and 25-hydroxyvitamin D₃ (25-OH-D₃) in mammal species

 

 

Table 3 25-hydroxyvitamin D₃ levels in liver, kidney and muscle of domestic animals

 

 

Also, it interferes with the integrity and safety of foods through the formation of potentially toxic compounds such as malondialdehyde (MDA) (Kanner, 2007). The treatment of meat by cooking or cold storage improves its quality but may also lead to the oxidation of its lipids and proteins and impact its nutritional and sensory qualities (Hur et al. 2004). In the dromedary camel, ageing time of meat influenced significantly its quality characteristics and antioxidant status from the 5^th or 7^th postmortem day of refrigerated storage, without any variation of proteins, fat and 25-OH-D contents (Tabite et al. 2018). In addition, in the same species, during cold storage of meat for 10 postmortem days, the levels of 25-OH-D total showed no significant variation. Vitamin D status impacts skeletal muscle function, metabolism and hypertrophic growth and muscle fiber composition and size (Ceglia and Harris, 2013). Vitamin D might influence the postmortem muscle pH values and consequently its water holding capacity (WHC). In fact, previous studies in beef steers and pork reported that dietary vitamin D₃ supplementation increased pHu and WHC, decreased drip loss, squeezable water and cooking loss (Wilborn et al. 2004) and participated in antioxidant activity (Duffy et al. 2018). During cold storage of raw or cooked meat, drip loss, cooking loss and MDA increased significantly, however 25-OH-D showed no significant variation during all storage times (Tabite et al. 2018). Compared to raw meat, cooked meat showed a significant increase of 25-OH-D and MDA levels on days 3, 5, 7 and 10 postmortem storage (El Khasmi et al. 2018). The 25-OH-D levels in raw and cooked meat, was positively correlated with pH and negatively correlated with redness, drip loss and MDA. Vitamin D status may impact skeletal muscle function, metabolism, hypertrophic growth, fiber composition and size (Ceglia and Harris, 2013). In addition, previous studies in beef steers and pork reported that dietary vitamin D₃ supplementation increased ultimate pH and water holding capacity, decreased the drip loss, squeezable water and cooking loss of meat (Wilborn et al. 2004) and participated in antioxidant activity (Duffy et al. 2018).

 

Impact of stress

In domestic animals, several factors like handling, loading, movement, immobilization, transport, food and water privation, heat, etc may compromise the welfare of animals and increase their vulnerability to disease (Broom, 2014). Several important indicators are used in evaluating the effects of environmental stress, such as physiological, hematological, biochemical and hormonal responses. The dromedary camel was very sensitive to stress induced by road transportation (El Khasmi et al. 2015; Lemrhamed et al. 2018) and winter season (Bargaa et al. 2016). However, in the dromedary camel, plasma levels of 25-hydroxyvitamin D were not affected by road transportation (El Khasmi et al. 2010). Furthermore, in old and young stressed camels (transported), the mean value of plasma levels of 25-hydroxyvitamin D showed no significant differences compared to control animals (non transported) (El Khasmi et al. 2009). In fact, under road transportation stress, the magnitude of cortisol response was higher in old camels than in young ones, without any variation of plasma 25-hydroxyvitamin D levels with age (El Khasmi et al. 2009). Concerning the impact of season on vitamin D levels in camels, although circulating levels of cortisol, thyroid hormones and testosterone were higher in winter (rutting period) than in summer (non-rutting period) (Farh et al. 2018). In contrary, circulating levels of 25-OH-D are higher in summer than in winter (395±25 ng/mL vs 304±22 ng/mL) (El Khasmi et al. 2011). The dromedary camel is largely known to be a seasonal breeder and its reproduction is characterized by a seasonal activity where the breeding season is confined to the cool winter months of the year. The rutting period might be considered as stressful situation during which, the male is very aggressive and presents some behavioral reactions like the extrusion of the soft palate, and becomes very vocal (Marai et al. 2009).

 

Impact of season

Huge seasonal variations in vitamin D status were observed in all domestic species and humans (Mc Dowell, 1989). In llamas and alpacas (Smith and Van Saun, 2001), and camels (Mohamed, 2008), the circulating levels of vitamin D are not influenced by age, but vary depending on the season. In the dromedary, the highest levels were detected during the period from February to July, while lowest levels were observed during the period from August to January (Mohamed, 2008). In the camel, the serum 25-OH-D levels (ng/mL) in summer and winter are 443 ± 96 and 276 ± 13, respectively (Shany et al. 1978). The seasonal variations of vitamin D in the blood were also reported in sheep (Smith et al. 1987) and horse (Maenpaa et al. 1988). These variations are much more pronounced in calves and young camels aged one year (Smith and Van Saun, 2001). On the other hand, the content of vitamin D in bovine milk had showed significant variations during the season, with lower values in winter and higher levels in summer (Kurmann and Indyke, 1994). Variations in circulating concentrations of vitamin D in different species of camel, could be explained by the degree of coat color, as is for llamas and alpacas (Smith and Van Saun, 2001), or Arabi and Anafi camels (Mohamed, 2008). The month of birth, light intensity (Van Saun et al. 1996) and physiological status (lactation, neonatal development) (Riad et al. 1994; El Khasmi et al. 2000) were able to influence the status of vitamin D.

 

CONCLUSION

The anatomy of the camel (Camelus dromedarius) is characterized by long legs and long neck requiring a large amount of Ca and P. This species is living in ecosystems marked by high level of sun light which could be regarded as favorable for an important biosynthesis of one vitamin playing a pivotal role in the metabolism of these minerals. The data collected in scientific literature could suggest the possibility to use dietary vitamin D supplementation in the dromedary camel as a natural synthetic source of vitamin D in the meat of this species, especially in environment with less sun light.

مراجع

Agarwal S.P. and Khanna N.D. (1990). Endocrine profiles of Indian camel under different phases of reproduction. Workshop: Is it possible to improve the reproductive performance of the camel. Pp. 77-100 in Proc. Unité de Coordination pour l’Elevage Camelin, Paris, France.

Allen W.M. and Samson B.F. (1985). Milk fever and calcium metabolism. J. Vet. Pharmacol. Ther. 8, 19-29.

Al-Qarawi A.A. and Elmougy S.A. (2008). Seasonality and the melatonin signal in relation to age as correlated to the sexual cycle of the one-humped male camel (Camelus dromedarius). Biol. Rhythm Res. 39, 131-142.

Arthur G.H. (1992). An overview of reproduction in the Camelids. Pages 169-171 in Proc. 1^st Int. Camel Conf., Dubai, United Arab Emirates.

Audet I., Bérubé N., Bailey J.L., Laforest J.P. and Matte J.J. (2009). Effects of dietary vitamin supplementation and semen collection frequency on reproductive performance and semen quality in boars. J. Anim. Sci. 87, 1960-1970.

Bargaa R., El Khasmi M., Farh M., Tahri E., El Abbadi N., Abouhafs R. and Faye B. (2015). Seasonal variation of 25-hydroxyvitamin D₃ levels in meat of Moroccan one humped dromedary camels (Camelus dromedarius). Veterinariâ. 42, 115-117. 

Bargaa R., Lektib I., Barka K., Riad F., El Abbadi N., Belhouari A., Hammoumi A. and El Khasmi M. (2016). Seasonal variations of heamatological profile and its correlations with thyroid and adrenal gland hormones in male Moroccan camel (Camelusdromedarius). Int. J. Agric. Environ. Sci. 1, 8-14.

Barrera D., Avila E., Hernández G., Halhali A., Biruete B., Larrea F. and Díaz L. (2007). Estradiol and progesterone synthesis in human placenta is stimulated by calcitriol. J. Steroid Biochem. Mol. Biol. 103, 529-532.

Bengoumi M., Davicco M.J., Coxam V., De Lafarge F. and Barlet J.P. (1996). Effect of 1 alpha hydroxycholecalciferol on calcium and phosphorus concentration in goat milk. Small Rumin. Res. 21, 45-49.

Bonniwell M.A., Smith B.S., Spence J.A., Wright H. and Ferguson D.A. (1988). Rickets associated with vitamin D deficiency in young sheep. Vet. Rec. 122, 386-388.

Broom D.M. (2014). Welfare of transported animals: Factors influencing welfare and welfare assessment. Pp. 23-38 in Livestock Handling and Transport. T. Grandin, Ed. CABI, Wallingford, United Kingdom.

Brown B.W. (1994). A review of nutritional influences on reproduction in boars, bulls and rams. Reprod. Nutr. Dev. 34, 89-114.

Cali J.J., Hsieh C.L., Francke U. and Russell D.W. (1991). Mutations in the bile acid biosynthetic enzyme sterol 27-hydroxylase underlie Cerebrotendinous xanthomatosis. J. Biol. Chem. 266, 7779-7783.

Carnagey K.M., Huff-Lonergan E.J., Trenkle A., Wertz-Lutz A.E., Horst R.L. and Beitz D.C. (2006). Use of 25-hydroxyvitamin D₃ and vitamin E to improve tenderness of beef from the longissimus dorsi of heifers. J. Anim. Sci. 86, 1649-1657.

Ceglia L. and Harris S.S. (2013). Vitamin D and its role in skeletal muscle. Calcif. Tissue Int. 92, 151-162.

Cho Y.M., Choi H., Hwang I.H., Kim Y.K. and Myung K.H. (2006). The tenderness of beef from cull native Korean cows and manipulated dietary cation-anion difference on 3 Effects of 25-hydroxyvitamin D. J. Anim. Sci. 84, 1481-1488.

Collignon H., Davicco M.J. and Barlet J.P. (1996). Calcitonin mRNA expression and plasma calciotropic hormones in fetal lambs. Domest. Anim. Endocrinol. 13, 269-276.

Colston K.W, Berger U., Wilson P., Hadcocks L., Naeem I., Earl H.M. and Coombes R.C. (1988). Mammary gland 1,25 dihydroxyvitamin D₃ receptor content during pregnancy and lactation. Mol. Cell. Endocrinol. 60, 15-22.

Corbett S.T., Hill O. and Nangia A.K. (2006). Vitamin D receptor found in human sperm. Urology. 68, 1345-1349.

Crissey S.D., Ange K.D., Jacobsen K.L., Slifka K.A., Bowen P.E., Stacewicz-Sapuntzakis M., Langman C.B. and Sadler W. (2003). Serum concentrations of lipids, vitamin D metabolites, retinol, retinyl esters, tocopherols and selected carotenoids in twelve captive wild felid species at four zoos. J. Nutr. 133, 160-166.

Crowe F.L., Steur M., Allen N.E., Appleb P.N., Travis R.C. and Key T.J. (2011). Plasma concentrations of 25-hydroxyvitamin D in meat eaters, fish eaters, vegetarians and vegans: results from the EPIC-Oxford study. Public Health Nutr. 14, 340-346.

Cutty G.B., Goldman B.D., Doherty P. and Bartke A. (1981). Melatonin prevents decrease in plasma PRL and LH levels in male hamsters exposed to a short photoperiod. Int. J. Androl. 4, 281-290.

Dabrowski F.A., Grzechocinska B. and Wielgos M. (2015). The Role of vitamin D in reproductive health- a Trojan horse or the golden fleece? Nutrients. 7, 4139-4153.

 

Duffy S.K., Kelly A.K., Rajauria J., Jakobsen J., Clarke L.C., Monahan F.J., Dowling K.G., Hull G., Galvin K., Cashman K.D., Hayes A. and O’Doherty J.V. (2018). The use of synthetic and natural vitamin D sources in pig diets to improve meat quality and vitamin D content. Meat Sci. 143, 60-68.

Elagamy E. (2006). Camel milk. Pp. 297-344 in Handbook of Milk of Non-bovine Mammals. Y.W. Park and G.F. Haenlein, Eds. Blackwell Publishing, Ames, Iowa.

El Khasmi M., Riad F., Safwate A., Bengoumi M., Hidane K., Davicco M.J., Coxam V., Faye B. and Barlet J.P. (2000). Évolution comparée de quelques paramètres minéraux, de l’ostéocalcine, du 25(OH)D et du 1,25(OH)₂D chez la chamelle du Sud marocain et son chamelon nouveau-né. Rev. Elev. Med. Vet. Pays Trop. 53, 115-119.

El Khasmi M., Riad F., Safwate A., Farh M., Faye B., El Abbadi N., Lalaoui K., Coxam V., Davicco M.J. and Barlet J.P. (2001a). Influence de la 1α, 25-dihydroxyvitamine D₃ sur l'excrétion mammaire du calcium et du phosphore chez la chamelle allaitante. Rev. Elev. Méd. Vét. Pays Trop. 54, 277-280.

El Khasmi M., Riad F., Safwate A., Hidane K., Faye B., Davicco M.J., Coxam V. and Barlet J.P. (2001b). Postpartum evolution of mammary secretion of minerals and 25-hydroxyvitamin D in lactating camels (Camelus dromedarius). J. Camel Pract. Res. 8, 131-135.

El Khasmi M., Riad F., Safwate A., Farh M., Belhouari A., Hidane K., El Abbadi N., Faye B. and  Coxam V. (2003). Exploration of intestinal absorption and renal excretion of calcium by stable strontium test in camels (Camelus dromedarius). J. Camel Pract. Res. 10, 131-134

El Khasmi M., Riad F., Safwate A., El Abbadi N., Farh M., Faye B. and Coxam V. (2005). La chamelle allaitante face au stress calcique: une fonction endocrine adaptée aux conditions désertiques. Secheresse. 16, 261-267.

El Khasmi M., Riad F., Safwate A., Tahri E., Farh M., El Abbadi N., Bengoumi M., Coxam V. and Faye B. (2009). Effects of age on transportation and preslaughter stress responsiveness in Moroccan dromedary camels. Pp. 810-811 in Proc. 11^th Int. Symp. Rumin. Physiol., Clermont-Ferrand, France.

El Khasmi M., Riad F., Safwate A., Tahri E., Farh M., El Abbadi N., Coxam V. and Faye B. (2010). Effects of preslaughter stress on meat quality and phosphocalcic metabolism in Camels (Camelus dromedarius). J. Camelid Sci. 3, 33-38.

El Khasmi M., Riad F., Safwate A., Tahri E., Farh M., El Abbadi N., Coxam V. and Faye B. (2011). Seasonal variation of circulating levels of 25-Hydroxyvitamin D in Moroccan dromadary camels (Camelus dromedarius). Emirates J. Food Agric. 23, 368-374.

El Khasmi M., Bergaâ R., Riad F., Safwate A., Tahri E., Farh M., El Abbadi N., Abouhafs R. and Faye B. (2013a). Meat levels of 25-hydroxyvitamin D₃ in Moroccan one-humped dromedary camels (Camelus dromedarius). Emirates J. Food Agric. 25, 267-273.

El Khasmi M., Chakir Y., Riad F., Safwate A., Tahri E., Farh M., El Abbadi N., Abouhafs R. and Faye B. (2013b). Effects of transportation stress during the hot-dry season on some haematological and physiological parameters in Moroccan dromedary camels (Camelus dromedarius). J. Life Sci. (USA). 7, 13-22.

El Khasmi M., Chakir Y. Bargaâ R., Barka K., Lektib I., El Abbadi N., Belhouari A. and Faye B. (2015). Impact of transport distance on stress biomarkers levels in dromedary camel (Camelus dromedarius). Emirates J. Food Agric. 27, 507-512.

El Khasmi M., Tabite R., Barka K., Farh M., El Abbadi N., Riad F., Tahri E., Abouhafs R. and Faye B. (2018). Impact of cooking and refrigerated storage on 25-hydroxyvitamin D levels, quality characteristics and lipid peroxidation of the camel meat. Pp. 1-3 in Proc. 5^th Conf. Int. Soc. Camelid Res. Dev., Laâyoune, Morocco.

Farah Z., Rettenmaier R. and Atkins D. (1992). Vitamin content of camel milk. Int. J. Vitam. Nutr. Res. 62, 30-33.

Farh M., Lektib I., Bargaa R., El Abbadi N., Riad F., Tahri E., Safwate A. and El Khasmi M. (2018). Hormonal profile in rutting and non-rutting periods in dromedary camel (Camelus dromedarius). Rev. Mar. Sci. Agron. Vét. 6, 390-398.

Faye B. (2014). The camel today: Assets and potentials. Anthropozoologica. 49, 167-176.

Faye B. and Bengoumi M. (2000). Le dromadaire face à la sous-nutrition minérale: un aspect méconnu de son adaptabilité aux conditions désertiques. Sécheresse. 11, 155-161.

Foote M.R., Horst R.L., Huff-Lonergan E.J., Trenkle A.H., Parrish F.C. and Beitz D.C. (2004). The use of vitamin D₃ and its metabolites to improve beef tenderness. J. Anim. Sci. 82, 242-249.

Gay C.C. and Besser T.E. (1991). Colostrum and feeding management of the dairy calf during the first two days of life. Pp. 242-247 in Large Animal Clinical Nutrition. J.M. Naylor and S.L. Ralston, Eds. Mosby-Year Book, Inc., St. Louis, Missouri.

Greer F.R., Hollis B., Cripps D.J. and Tsang R.C. (1984). Effects of maternal ultraviolet-B irradiation on vitamin D content of human milk. J. Pediatr. 105, 431-433.

Health Canada. (2012). The Canadian Nutrient File. Nutrition Research Division, Canada.

Heaney R.P., Armas L.A., Shary J.R., Bell N.H., Binkley N. and Hollis B.W. (2008). 25-hydroxylation of vitamin D₃: Relation to circulating vitamin D₃ under various input conditions. Am. J. Clin. Nutr. 87, 1738-1742.

Heaney R.P., Horst R.L., Cullen D.M. and Armas L.A. (2009). Vitamin D₃ distribution and status in the body. J. Am. Coll. Nutr. 28, 252-256.

Hidiroglou M., Williams C.J. and Proulx J.G. (1985). Plasma vitamin D₃ response in cattle and sheep exposed to ultraviolet radiation. Int. J. Vitam. Nutr. Res. 55, 41-46.

Hirai T., Tsujimura A., Ueda T., Fujita K., Matsuoka Y., Takao T., Miyagawa Y., Koike N. and Okuyama A. (2009). Effect of 1,25-dihydroxyvitamin D on testicular morphology and gene expression in experimental cryptorchid mouse: Testis specific cDNA microarray analysis and potential implication in male infertility. J. Urol. 181, 1487-1492.

Holick M.F. (2007). Vitamin D deficiency. New England J. Med. 357, 266-281.

Holick M.F. and Chen T.C. (2008). Vitamin D deficiency: A worldwide problem with health consequences. Am. J. Clin. Nutr. 87, 1080-1086.

Holick M.F., Shao Q., Liu W.W. and Chen T.C. (1992). The vitamin D content of fortified milk and infant formula. New England J. Med. 326, 1178-1181.

Horst R.L., Hove K., Littledike E.T., Reinhardt T.A., Uskokovic M.R. and Partridge J.J. (1983). Plasma concentrations of 1,25-dihydroxyvitamin D, 1,24R,25-trihydroxyvitamin D₃, and 2,25,26-trihydroxyvitamin D₃ after their administration to dairy cows. J. Dairy Sci. 66, 1455-1460.

How K.L., Hazewinkel H.A.W. and Mol J.A. (1994). Dietary vitamin D dependence of cat and dog due to inadequate cutaneous synthesis of vitamin D. Gen. Comp. Endocrinol. 96, 12-18.

Hur S.J., Ye B.W., Lee J.L., Ha Y.L., Park G.B. and Joo S.T. (2004). Effects of conjugated linoleic acid on color and lipid oxidation of beef patties during cold storage. Meat Sci. 66, 771-775.

Kadim I.T., Mahgoub O., Al-Marzooqi W., Al-Zadijali S., Annamalai K. and Mansour M.H. (2006). Effects of age on composition and quality of muscle longissimus thoracisof the Omani Arabian camel (Camelus dromedarius). Meat Sci. 73, 619-625.

Kanner J. (2007). Dietary advanced lipid oxidation end products are risk factors to human health. Mol. Nutr. Food Res. 51, 1094-101.

Kchouk M. and Durand M. (1958). Quelques dosages chimiques dans le sang des dromadaires de Tunisie. Arch. Institut. Pasteur. Tunis. 35, 3-4.

Kistral-Boneh E., Froom P. and Harari G. (1990). Fibrous osteodys-trophy in dromedary camels (Camelus dromedarius). J. Zool. Wildlife Med. 30, 577-583.

Konuspayeva G., Faye B. and Loiseau G. (2011). Variability of vitamin C content in camel milk from Kazakhstan. J. Camelid Sci. 4, 63-69.

Koshy K.T. and Van Der Silk A.L. (1977). High performance liquid chromatographic method for the determination of 25-hydroxycholecalciferol in the bovine liver, kidney, and muscle. J. Agric. Food Chem. 25, 1246-1249.

Kurmann A. and Indyk H. (1994). The endogenous vitamin D con-tent of bovine milk: Influence of season. Food Chem. 50, 75-81.

Lemrhamed A., Farh M., Riad F., El Abbadi N., Tahri E.H., Belhouari A., Faye B. and El Khasmi M. (2018). Evaluation of stress responses induced by the loading density in dromedary camel (Camelus dromedarius). Emirates J. Food Agric. 30, 803-808.

Liesegang A., Risteli J. and Wanner M. (2006). The effects of first gestation and lactation on bone metabolism in dairy goats and milk sheep. Bone. 38, 794-802.

Maqsood S. and Benjakul S. (2011). Comparative studies on molecular changes and pro-oxidative activity of haemoglobin from different fish species as influenced by pH. Food Chem. 124, 875-883.

Marai I.F.M., Zeidan A.E.B., Abdel-Samee A.M., Abizaid A. and Fadie A. (2009). Camel’s reproductive and physiological performance traits as affected by environmental conditions. Trop. Subtrop. Agroecosys. 10, 129-149.

Mattila P.H., Piironen V.I., UusiRauva E.J. and Koivistoinen P.E. (1995). Contents of cholecalciferol, ergocalciferol, and their 25-hydroxylated metabolites in milk products and raw meat and liver as determined by HPLC. J. Agric. Food Chem. 43, 2394-2399.

Mc Dowell L.R. (1989). Vitamins in Animal Nutrition: Comparative Aspects to Human Nutrition. Academic Press, San Diego, United States.

Menegaz D., Rosso A., Royer C., Leite L.D., Santos A.R. and Silva F.R. (2009). Role of 1alpha, 25(OH)₂vitamin D₃ on alpha-[1-(14)C] MeAIB accumulation in immature rat testis. Steroids. 74, 264-269.

Mohamed S.E. (2008). Statut en vitamine D chez les dromadaires (Camelus dromedarius). Res. J. Biol. Sci. 3, 446-447.

Naito Y., Watanabe E., Oshibe A., Sato R. and Murakami D. (1983). Plasma level of 1,25-dihydroxyvitamin D in neonatal calves. Nippon Juigaku Zasshi 45, 533-535.

Namioka T., Yamagishi N., Okura N., Akasaka S., Abe T., Chida H., Sat S. and Naito Y. (2008). Transdermal absorption of 1,25-dihydroxyvitamin D₃ in cattle. Jpn. J. Vet. Clin. 31, 1-5.

Nonnecke B.J., Reinhardt T.A. and Waters W.R. (2009). Short communication: The preruminant calf as a model for characterizing the effects of vitamin D status in the neonate. J. Dairy Sci. 92, 5692-5696.

NRC. (1985). Nutrient Requirements of Sheep. National Academy Press, Washington, D.C., USA.

Okura N., Yamagishi M., Naito Y., Kanno K. and Koiwa M. (2004). Technical note: Vaginal absorption of 1,25(OH)₂D₃ in cattle. J. Dairy Sci. 87, 2416-2419.

Olmos-Ortiz A., Avila E., Durand-Carbajal M. and Díaz L. (2015). Regulation of calcitriol biosynthesis and activity: Focus on gestational vitamin D deficiency and adverse pregnancy outcomes. Nutrients. 7, 443-480.

Pando M.P. and Sassone-Corsi P. (2001). Signaling to the mammalian circadian clocks: In pursuit of the primary mammalian circadian photoreceptor. Sci. STKE. 107, RE16.

Parker J.E., Timm K.I., Smith B.B., Van Saun R.J., Winters K.M., Sukon P. and Snow C.M. (2002). Seasonal interaction of serum vitamin D concentration and bone density in alpacas. Am. J. Vet. Res. 63, 948-953.

Raiymbek G., Kadim I., Konuspayeva G., Mahgoub O., Serikbayeva A. and Faye B. (2015). Discriminant amino-acid components of Bactrian (Camelus bactrianus) and Dromedary (Camelus dromedarius) meat. J. Food compos. Anal. 41, 194-200

Rajaraman V., Nonnecke B.J. and Horst R.L. (1997). Effects of re placement of native fat in colostrum and milk with coconut oil on fat-soluble vitamins in serum and immune function in calves. J. Dairy Sci. 80, 2380-2390.

Reinhardt T.A., Horst R.L., Littledike E.T. and Beitz D.C. (1982). 1,25-Dihydroxyvitamin D₃ receptor in bovine thymus gland. Biochem. Biophys. Res. Commun. 106, 1012-1018.

Riad F. (1995). Endocrine regulation of hydroelectrolytic and phosphocalcic metabolism in the camel. MS Thesis. Hassan II-Mohammedia Univ., Casablanca, Morocco.

Riad F., Bengoumi M., Davicco M.J., Safwate A. and Barlet J.P. (1994). Influence of 1 alpha-hydroxycholecalciferol on calcium and phosphorus concentration in camel milk. J. Dairy Res. 61, 567-571.

Riad F., Lefaivre J. and Barlet J.P. (1987). 1,25-dihydroxycholecalciferol regulates salivary phosphate secretion in cattle. J. Endocrinol. 112, 427-430.

Rivera J.D., Bachman S.E., Hubbert M.E., Branine M.E., Horst R.L., Williams S.N. and Galyean M.L. (2005). Serum and tissue concentrations of vitamin D metabolites in beef heifers after buccal dosing of 25-hydroxyvitamin D₃. J. Dairy Sci. 88, 1364-1369.

Ross R., Halbert K. and Tsang R.C. (1989). Determination of the production and metabolic clearance rates of 1,25 dihydroxyvitamin D₃ in the pregnant sheep and its catheterized fetus by primed infusion technique. Pediatr. Res. 26, 633-638.

Schmid A. and Walther B. (2013). Natural vitamin D content in animal products. Adv. Nutr. 4, 453-462.

Schwartz J.B., Lai J., Lizaola B., Kane L., Markova S., Weyland P., Terrault N.A., Stotland N. and Bikle D. (2014). A comparison of measured and calculated free 25(OH) vitamin D levels in clinical populations. J. Clin. Endocrinol. Metab. 99, 1631-1637.

Sghiri A. (1988). Evaluation of the breeding performance of a camel herd Laayoune (Camelus dromedarius). MS Thesis. Agronomic and Veterinary Institute Hassan II, Rabat, Morocco.

Shany S., Yagil R. and Berlyne G.M. (1978). 25-hydroxycholecalciferol levels in camel, sheep and goat. Comp. Biochem. Physiol. 59, 139-140.

Smith B.B. and Van Saun R.J. (2001). Seasonal changes in serum calcium, phosphorus, and vitamin D concentrations in llamas and alpacas. Am. J. Vet. Res. 62, 1187-1193.

Smith B.S., Wright H. and Brown K.J. (1987). Effect of vitamin D supplementation during pregnancy on the vitamin D status of ewes and their lambs. Vet. Rec. 28, 199-201.

Specker B.L., Valanis B., Hertzberg V., Edwards N. and Tsang R.C. (1985). Sunshine exposure and serum 25-hydroxyvitamin D concentrations in exclusively breast-fed infants. J. Pediatr. 107, 372-376.

Sumar J. (1996). Reproduction in llamas and alpacas. Anim. Reprod. Sci. 42, 405-415.

Tabite R., Barka K., Farh M., Riad F., El Abbadi N., H. Tahri E., Belhouari A., Faye B. and El Khasmi M. (2018). Effect of postmortem ageing on quality parameters, contents of proteins, lipids and 25-hydroxyvitamin D, and oxidative stability in the camel meat during cold storage. J. Agric. Sci. Technol. A. 8, 323-332.

Taylor M.S., Knowlton K.F., Mc Gilliard M., Seymour W.M. and Herbein J.H. (2008). Blood mineral, hormone, and osteocalcin responses of multiparous Jersey cows to an oral dose of 25-hydroxyvitamin D₃ or vitamin D₃ before parturition. J. Dairy Sci. 91, 2408-2416.

Van Der Meer I.M., Boeke A.J., Lips P., Grootjans-Geerts I., Wuister J.D., Devillé W.L., Wielders J.P., Bouter L.M. and Middelkoop B.J. (2008). Fatty fish and supplements are the greatest modifiable contributors to the serum 25-hydroxyvitamin D concentration in a multiethnic population. Clin. Endocrinol. 68, 466-472.

Van Saun R.J. (2004). Vitamin D-responsive rickets in neonatal lambs. Canadian Vet. J. 45, 841-844.

Van Saun R.J., Smith B.B. and Watrous B.J. (1996). Evaluation of vitamin D status of llamas and alpacas with hypophos-phatemic rickets. J. Am. Vet. Med. Assoc. 209, 1128-1133.

Weiss W.P., Azem E., Steinberg W. and Reinhardt T.A. (2015). Effect of feeding 25-hydroxyvitamin D₃ with a negative cation-anion difference diet on calcium and vitamin D status of periparturient cows and their calves. J. Dairy Sci. 98, 5588-5600.

Wertz A.E., Knight T.J., Trenkle A., Sonon R., Horst R.L., Huff-Lonergan E.J. and Beitz D.C. (2004). Feeding 25-hydroxyvitamin D3 to improve beef tenderness. J. Anim. Sci. 82, 1410-1418.

Wilborn B.S., Kerth C.R., Owsley W.F., Jones W.R. and Frobish L.T. (2004). Improving pork quality by feeding supranutritional concentrations of vitamin D₃. J. Anim. Sci. 82, 218-224.

Williams P. (2007). Nutritional composition of red meat. Nutr. Diet. 64, 113-119.

Wolter R. (1988). Besoins vitaminiques des ruminants. INRA Prod. Anim. 1, 311-318.

Yamagishi N., Ayukawa Y., Lee I., Oboshi K. and Naito Y. (2005). Calcium metabolism in cows receiving an intramuscular injec-tion of 1,25-dihydroxyvitamin D₃ combined with pros-taglandin F (2 alpha) closely before parturition. J. Vet. Sci. 6, 165-167.

Yetley E.A., Brule D., Cheney M.C., Davis C.D., Esslinger K.A., Fischer P.W.F., Friedl K.E., Greene-Finestone L.S., Guenther P.M., Klurfeld D.M., L’Abbe M.R., McMurry K.Y. and Starke-Reed P.E. (2009). Dietary reference intakes for vitamin D: Justification for a review of the 1997 values. Am. J. Clin. Nutr. 89, 719-727.

Zaraazga L.A., Malpaux B., Bodin B. and Chemineaux P. (1998). The large varibalility in melatonin blood levels in ewes under strong genetic influence. Am. J. Physiol. 274, 607-610.

Zerwekh J.E. (2008). Blood biomarkers of vitamin D status. Am. J. Clin. Nutr. 87, 1087-1091.

Zia-Ur-Rahman N.A., Bukhari S.A., Akhtar N. and Haq I.H. (2007). Serum hormonal, lectrolytes and trace elements profiles in the rutting and non-rutting one humped male camel. Anim. Reprod. Sci. 101, 172-178.

Zofková I., Scholz G. and Stárka L. (1989). Effect of calcitonin and 1,25(OH)2- vitamin D₃ on the FSH, LH and testosterone secretion at rest and LHRH stimulated secretion. Horm. Metab. Res. 21, 682-685.