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# Blood, Milk and Meat Vitamin D in the Dromedary Camel

Mohammed El Khasmi, Bernard Faye

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## To cite this version:

Mohammed El Khasmi, Bernard Faye. Blood, Milk and Meat Vitamin D in the Dromedary Camel. Iranian Journal of Applied Animal Science, 2019, 9 (4), pp.585-595. hal-02544444

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# Blood, Milk and Meat Vitamin D in the Dromedary Camel

## Review Article

M. El Khasmi<fnref n="1" />* and B. Faye<fnref n="2" />

Received on: 4 Feb 2019

Revised on: 28 Apr 2019

Accepted on: 30 Apr 2019

Online Published on: Dec 2019

*Correspondence E-mail: mohammed.elkhasmi@univh2c.ma

© 2010 Copyright by Islamic Azad University, Rasht Branch, Rasht, Iran

Online version is available on: www.ijas.ir

## ABSTRACT

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.

## KEY WORDS

blood, milk, meat, oxidant stress, 25-hydroxyvitamin D.

## INTRODUCTION

In mammal species, the physiological control of phospho-calcic 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

<footnote n="1">¹ Laboratory of Physiopathology and Molecular Genetics, Ben M'Sik Faculty of Science, Hassan II University of Casablanca, BP 7955 Sidi Othmane, Casablanca, Morocco</footnote>

<footnote n="2">² Center 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</footnote>
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 llamas born in autumn/winter that had lower vitamin D con-

centrations 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><caption>**Table 1** Circulating levels of vitamin D and its metabolites in domestic ruminants</caption><thead><tr><th>Compounds</th><th>Species</th><th>Values</th><th>References</th></tr></thead><tbody><tr><td rowspan="2">Vitamin D, ng/mL</td><td>Cow</td><td>4.01±0.79</td><td>Cho et al. (2006)</td></tr><tr><td>Calf</td><td>3.34±1.43</td><td>Foote et al. (2004)</td></tr><tr><td rowspan="8">25-hydroxyvitamin D<sub>3</sub><br>(25-OH-D), ng/mL</td><td>Beef</td><td>35.2±7.8</td><td>Rivera et al. (2005)</td></tr><tr><td>Cow</td><td>88±7.1</td><td>Cho et al. (2006)</td></tr><tr><td>Calf</td><td>62.66±16.74</td><td>Foote et al. (2004)</td></tr><tr><td>Heifer</td><td>40-50</td><td>Carnagey et al. (2006)</td></tr><tr><td>Calf (birth)</td><td>45.7</td><td>Weiss et al. (2015)</td></tr><tr><td>Camel</td><td>390±45</td><td>El Khasmi et al. (2013a)</td></tr><tr><td>Lactating camel (1<sup>st</sup> day)</td><td>480±59.7</td><td>El Khasmi et al. (2000)</td></tr><tr><td>Newborn camel (15 days)</td><td>176.4±19.6</td><td></td></tr><tr><td rowspan="10">1,25-dihydroxy-vitamin D<br>[1,25(OH)<sub>2</sub>D], pg/mL</td><td>Sheep</td><td>50-60</td><td>Ross et al. (1989)</td></tr><tr><td>Cow</td><td>10-100</td><td>Horst et al. (1983)</td></tr><tr><td>Periparturient Cow</td><td>36.8±9.8</td><td>Yamagishi et al. (2005)</td></tr><tr><td>Cow 1<sup>st</sup> postpartum day</td><td>96.6±25.9</td><td></td></tr><tr><td>Calf (birth)</td><td>149.0</td><td>Weiss et al. (2015)</td></tr><tr><td>Non pregnant camel</td><td>835±45</td><td>Riad (1995)</td></tr><tr><td>Lactating camel</td><td>301±209</td><td>El Khasmi et al. (2000)</td></tr><tr><td>Newborn camel (7 days)</td><td>1215±248</td><td></td></tr></tbody></table>

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 ef-
fects 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 me-
tabolized 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 blood-
stream as early as the 7th 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 deter-
minants 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 re-
spond to an exogenous supply of 1α,25(OH)₂D₃ by hyper-
calcemia, hyperphosphatemia and increase of phosphocal-
cic excretion by the mammary glands (Okura et al. 2004;
Yamagishi et al. 2005; Namioka et al. 2008). Indeed, cam-
els in third lactation that received 1α,25(OH)₂D₃ intrave-
nously, 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 hyper-
phosphatemia 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 calcit-
riol were demonstrated in mammary glands and their num-
ber 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 vi-
tamin 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 No-
vember 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 photope-
riod (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 steroido-
genic 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 sup-
plementation 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. Fur-
thermore, 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 in-
volving Ca²⁺/K⁺ channels on the plasma membrane.

In another publication, it was concluded that low concen-
trations of vitamin D (<50 nmol/L) were associated with
decreased number and quality of spermatozoa in semen
(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 pe-
riod) than in summer (El Khasmi et al. 2011; Farh et al.
2018), suggesting that vitamin D doesn't appear to contrib-
ute 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, inter-
action of photoperiod (intensity, duration, wavelength) with
other factors (ambient temperature, nutrition, housing, lati-
tude) and hormonal status (thyroid and corticosterone lev-
els) (Zia-Ur-Rahman et al. 2007) can influence the repro-
ductive 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, vita-min 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 influ-enced 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 con-centration 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 lim-ited (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 concentra-tions of 25-OH-D₃ and 1,25-(OH)₂D₃ leading to an in-crease 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 colos-trum and sixth milking day were correlated with their con-centrations 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 estab-lishing 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 vita-min D, and the circulating levels of 25-OH-D are more in-fluenced 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 concentra-tions 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-D<25 nmol/L) was 36.5% in Morocco, Turkey 41.3% and 19.3% in Nederland (Van 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 signifi-cantly higher in summer than in winter, meat, liver and kid-ney 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), myoglo-bin 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><caption>**Table 2** Milk levels of vitamin D₃ and 25-hydroxyvitamin D₃ (25-OH-D₃) in mammal species</caption><thead><tr><th>Item</th><th>Stage</th><th>Values</th><th>Species</th><th>References</th></tr></thead><tbody><tr><td rowspan="2">Vitamin D<sub>3</sub> (pg/mL)</td><td>1<sup>st</sup> milking colostrum</td><td>471</td><td rowspan="2">Cow</td><td rowspan="2">Weiss et al. (2015)</td></tr><tr><td>6<sup>th</sup> milking day</td><td>324</td></tr><tr><td rowspan="5">25-OH-D<sub>3</sub> (ng/mL)</td><td>1<sup>st</sup> milking colostrum</td><td>1.021</td><td rowspan="2">Cow</td><td rowspan="2">Weiss et al. (2015)</td></tr><tr><td>6<sup>th</sup> milking day</td><td>0.458</td></tr><tr><td>1<sup>st</sup> milking colostrum</td><td>8.9±0.6</td><td rowspan="2">Camel</td><td rowspan="2">El Khasmi et al. (2001b)</td></tr><tr><td>7<sup>th</sup> milking day</td><td>1.2±0.3</td></tr><tr><td>Milk</td><td>97-159</td><td>Women</td><td>Specker et al. (1985)</td></tr></tbody></table>

<table><caption>**Table 3** 25-hydroxyvitamin D₃ levels in liver, kidney and muscle of domestic animals</caption><thead><tr><th>Tissues</th><th>Species</th><th>Values</th><th>References</th></tr></thead><tbody><tr><td rowspan="5">Liver (ng/g)</td><td>Cow</td><td>0.27-0.53<br>4.5±2.6</td><td>Koshy and Van Der Slik (1977)<br>Cho et al. (2006)</td></tr><tr><td>Calf</td><td>2.59±0.73</td><td>Foote et al. (2004)</td></tr><tr><td>Pig</td><td>0.44</td><td>Mattila et al. (1995)</td></tr><tr><td>Camel</td><td>7.071±1.003</td><td>El Khasmi et al. (2013a)</td></tr><tr><td>Cow</td><td>0.51-0.98<br>4.2±2.0</td><td>Koshy and Van Der Slik (1977)<br>Cho et al. (2006)</td></tr><tr><td rowspan="2">Kidney (ng/g)</td><td>Calf</td><td>3.02±1.13</td><td>Foote et al. (2004)</td></tr><tr><td>Camel</td><td>6.154±1.067</td><td>El Khasmi et al. (2013a)</td></tr><tr><td rowspan="8">Muscle (ng/g)</td><td>Cow</td><td>0.15-0.34<br>1.83±0.24</td><td>Koshy and Van Der Slik (1977)<br>Cho et al. (2006)</td></tr><tr><td>Heifer</td><td>0.6±0.1</td><td>Carnagey et al. (2006)</td></tr><tr><td>Calf</td><td>1.68±0.37</td><td>Foote et al. (2004)</td></tr><tr><td>Beef</td><td>0.9-0.10<br>0.0-9.0</td><td>Wertz et al. (2004)</td></tr><tr><td>Pig</td><td>1.0-23.0</td><td>Health Canada (2012)</td></tr><tr><td>Lamb</td><td>1.0-61.0</td><td></td></tr><tr><td>Camel</td><td>4.24±1.04</td><td>El Khasmi et al. (2013a)</td></tr></tbody></table>

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 5th or 7th 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 ef-
fects of environmental stress, such as physiological, hema-
tological, 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 dif-
ferences 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 hor-
mones and testosterone were higher in winter (rutting pe-
riod) 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 pal-
ate, 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 cam-
els (Mohamed, 2008), the circulating levels of vitamin D
are not influenced by age, but vary depending on the sea-
son. In the dromedary, the highest levels were detected dur-
ing 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 varia-
tions are much more pronounced in calves and young cam-
els 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 char-
acterized 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.

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