Comparative effect of organic and inorganic selenium supplementation on selenium status in camel

1 Introduction

To maintain camel health and efficient production, it requires that essential dietary nutrients be provided in appropriate amounts. Nutritional importance of selenium in camels was reported (Faye and Seboussi, 2009). The selenium imbalance is a common feature in Saudi Arabia both in human (Al-Saleh et al., 2006) and in livestock leading to sudden death in young animals by heart failure, white muscle disease and low reproductive performance in adult males and females (El-Neweehy et al., 2001). In spite of a lack of epidemiological data in camel, the selenium deficiency appears widely observed in the Arabian Peninsula (El Khouly et al., 2001; Faye and Seboussi, 2009). In Saudi Arabia, a previous study has shown the beneficial impact of diet enriched with barley, naturally rich in selenium, for improving selenium status in camel (Althamna et al., 2011). Yet, most of the Saudi camel farmers in Al-Jouf area did not distribute oral selenium supplementation to their animals, but rather used non-organic selenium solution by injection in pregnant or new-born camels based on formula set up for cattle and small ruminants. However, the effect of such unique injection at the end of pregnancy is quite insufficient for a significant improvement of the selenium status of the new-born, especially on the level of selenium in milk (Faye et al., 2013).

In all species, including man, the selenium status in serum or plasma is closely depending on the selenium intake and absorption in digestive tract (Haldimann et al., 1998). Elsewhere, it has been shown in recent studies that camel response on serum selenium concentration was very sensitive to oral selenium supplementation compared to other species (Faye and Seboussi, 2009; Seboussi et al., 2009). Especially, a comparative study involving camels and cows having comparable weight and fed with the same diet and supplemented orally with 2 mg of selenium per day under selenite form has shown that serum selenium was 2-fold in cow while it was 10-fold in camel after supplementation (Bengoumi et al., 1998). However, organic selenium which is now the main form of selenium supplementation for livestock in many countries has never been tested in camel contrary to cattle (Guyot et al., 2007), sheep (Davis et al., 2008), goat (Kachuee et al., 2013), pig (Horky et al., 2013), horse (Jancikova et al., 2013) or rats (Sochor et al., 2012), and its effect on selenium in serum and milk around the parturition was never assessed in camel.

The objective of this study was to compare the effect of supplemented selenium source provided to pregnant and lactating camels on measures of selenium status in the dam around parturition and newborn calf.

2 Material and methods

3 Results

As the feed intake was approximately 6 kg D.M of alfalfa and that the totality of barley and wheat bran was ingested (no refusals), the selenium intake provided by the basal diet according to selenium content in the different components of the feeds was approximately 1.20 mg per day (i.e. 0.12 mg/kg for 10 kg DM intake approximately). According to the mean weight (Life Weight-LW: 615 kg) of the animals, the selenium intake due to the diet corresponded to 2.4 μg/kg LW (with a range of 1.66–2.92 μg/kg LW). There was no significant difference between the groups regarding mean parity, breed, mean body weight at calving, gestation length and calf weight at delivery.

3.1

3.1 Selenium in serum

On average, all groups included, the serum selenium concentration in dam was 7.83 ± 3.74 μg/100 mL with significant higher values at d-30 (11.56 ± 1.84 μg/100 mL) followed by a fall up to 5.85 ± 2.38 at d1 then 5.59 ± 2.67 at d30, 7.60 ± 3.89 at d60 and 6.75 ± 2.9 μg/100 mL at d75 (P < 0.001). There was no difference at d-30 between the 3 groups, then the group Se-org was significantly higher at delivery (d1) and d30 (P < 0.05). At d60, serum selenium concentration in the control group was significantly lower than the supplemented groups (P < 0.01). At d75, the 3 groups were different (P < 0.001) with a higher value for the group Se-org, intermediate value for the group Se-Inorg and a still lower value in the control group (Fig. 1).

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Figure 1

Change (mean and SD) in selenium concentration in camel dam serum around the parturition (□ control group without supplementation, ■ group receiving inorganic selenium under bolus form, △ group receiving organic selenium).

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The mean selenium concentration in calf serum at parturition (all groups included) was not significantly different than in the mother at d1 (5.13 ± 2.56 vs 5.85 ± 2.38 μg/100 mL), and significantly higher (P < 0.01) from d30 (8.71 ± 2.97), d60 (10.56 ± 2.2) and d75 (10.57 ± 1.93 μg/100 mL). Selenium concentration in calf serum was significantly lower (P < 0.001) in the control group up to d60 (Fig. 2).

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Figure 2

Change (mean and SD) in selenium concentration in camel calf serum after parturition (□ control group without supplementation, ■ group receiving inorganic selenium under bolus form, △ group receiving organic selenium).

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3.2

3.2 Selenium in milk

On average, all groups included, the higher milk selenium concentration (P < 0.001) was observed in colostrum (4.62 ± 2.68 μg/100 mL) and tends to decrease gradually in milk: 1.87 ± 0.72 at d30, 1.58 ± 0.55 at d45, 1.39 ± 0.35 at d60, 1.25 ± 0.36 at d75, then 1.20 ± 0.30 at d90. The highest value was observed in colostrum of Se-Org group (7.27 ± 2.89 μg/100 mL). The difference between Se-Org group and the two other groups was significant at d1 (P < 0.001) and d30 (P < 0.05). From d45, no difference was observed (Fig. 3). There was no significant difference in the milk composition (%) between the control, Se-Inorg and Se-Org groups, for total protein (2.6 ± 0.06, 2.9 ± 0.10 and 2.9 ± 0.2, respectively), fat (3.6 ± 0.5, 3.3 ± 0.3 and 3.1 ± 0.6, respectively), lactose (3.7 ± 0.09, 4.2 ± 0.14 and 4.1 ± 0.27, respectively) and ash (0.65 ± 0.02, 0.75 ± 0.02 and 0.73 ± 0.05, respectively).

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Figure 3

Change (mean and SD) in selenium concentration in camel milk after parturition (□ control group without supplementation, ■ group receiving inorganic selenium under bolus form, △ group receiving organic selenium).

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3.4

3.4 Somatic cell count

Considering all the experiments and all milk samples, SCC values varied from 10,000 (limit of detection of the SCC counter) to 416,000 cells/mL. Only the value reported at d30 is significantly higher than at d90 (P < 0.05). On average all groups included, SCC changed irregularly from 50,430 cells/mL in colostrum to 61,820 cells/mL in milk after 2 months of lactation with important fluctuations (Fig. 4). However no significant difference was observed throughout the experiment between the 3 groups of camels: 33,310 ± 50,757 cells/mL in the control group vs 45,844 ± 44,141 cells/mL in the Se-Inorg group and 50,443 ± 48,693 cells/mL in the Se-Org group.

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Figure 4

Change in somatic cell count (in log) in camel milk after parturition (□ control group without supplementation, ■ group receiving inorganic selenium under bolus form, △ group receiving organic selenium).

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4 Discussion

The diet was globally poor in selenium (0.12 mg/kg) and did not provide enough quantity for a lactating animal which is considered to be 0.5–1 mg/kg/day for camel (Faye and Seboussi, 2009). According to the mean live weight of the camels in our experiment, the diet provided 1.6–2.9 μg/kg LW which is lower than that recommended (10–20 μg/kg LW) for camel (Faye and Seboussi, 2009). Besides, some cases of heart failure in camel calves were observed previously in the farm. The vitamin E content in the diet corresponded to the requirements for dairy cattle. In most of the studies on camel, there was no correlation between selenium and vitamin E status in plasma concentration (Seboussi et al., 2008; Seboussi et al., 2009). However, a high level of Se selenium seemed to depress the vitamin E level in plasma (Faye and Seboussi, 2010) as it was observed in horse affected by selenosis (Crain, 2007).

The mean concentration of whole blood/serum selenium reported in the literature for camel was around 10 μg/100 mL, value considered as sufficient for the maintenance of suitable metabolic functions (Faye and Seboussi, 2009). The values reported in our study at the beginning of the experiment (11.56 ± 1.78 μg/100 mL) were quite comparable to the observations of Hamliri et al. (1990) in Morocco on whole blood, Barri and Al-Sultan (2007) in Saudi Arabia on serum, Seboussi et al. (2008) in Emirates on serum, and Liu et al. (1994) in China on whole blood of Bactrian camel. However, lower values were reported on whole blood in Sudan (Abdel Rahim, 2005), and on serum in Morocco again (Bengoumi et al., 1998) and in Iran (Nazifi et al., 2009; Pourjafar et al., 2012). In fact, a high variability was observed generally with a range between 1.2 and 20 μg/100 mL. In a recent paper, Abdelrahman et al. (2013) reported a significant difference between two camel breeds in Saudi Arabia with a higher value for Malhah breed (14.7 μg/100 mL on average) than for Wadhah breed (7.3 μg/100 mL). In our experiment, the groups were heterogeneous regarding the breed and no difference was observed at the beginning of the trial (d-30): 12.3 for Hamrah, 11.4 for Wadhah, 10.4 for Malhah, and 8.2 μg/100 mL for Safrah. Moreover, in most of the publications, the selenium status of the diet is not known and the analytical procedures are not described. Globally, selenium status in camel is poorly documented.

No age effect was reported (Faye et al., 2008). At reverse, the physiological status could be responsible for important variation in serum selenium concentrations. The fall in serum Se observed at parturition in our study was not reported in the experiment achieved in Emirates on pregnant and lactating camels (Seboussi et al., 2009). However, a significant decrease of gluthatione-peroxidase (GSH-Px), metallo-enzyme generally highly correlated to selenium, was decreased after parturition by these authors in camel and in sheep by White et al. (1989). Such post-partum decrease probably linked to lactation stress was reported for serum Se in sheep (Travnicek et al., 2007). One reason of the decrease in Se in the mother serum after delivery, independently of Se form received by the animals could be attributed to the active placental transfer of Se and to the milk selenium excretion. Indeed, the quantity of selenium was higher in colostrum emphasizing the efficiency of maternal transfer through the milk (Faye et al., 2011) just after the parturition.

The camels receiving organic Se presented the highest Se values both in serum and in colostrum compared to camels receiving non-organic Se. Similar results were observed in cattle (Gunter et al., 2013), in goat (Kachuee et al., 2013) and sheep (Davis et al., 2006) emphasizing a better efficiency of organic-selenium supplementation on blood and milk status of the supplemented animals. It is interesting to note that the ratio Se-Org/control at d1 was similar in serum-dam (1.51), in serum calf (1.85) and quite higher in milk (2.69). The organic form of Se is regarded as a more efficient form for the transfer from the mother to her calf, notably by colostrum (Guyot et al., 2007). The better transfer of Se under seleno-methionine form through the milk is due to its efficient incorporation in milk proteins (Anan et al., 2009).

The ratio of Se-Org group/Se-Inorg group at d1 was also similar in mother Se-serum (2.10) and in milk (1.96) but the ratio in camel calf (1.06) did not reflect the difference observed in mother and in milk contrary to the observation of Seboussi et al. (2009) who stated a similar proportion in serum dam, serum calf and milk between the group receiving sodium selenite and the control group. Yet, Weiss et al. (1984) suggested that selenium concentration in blood serum of the dam near parturition can be used as an indicator of serum selenium status of the neonatal calf. The significant correlation between Se serum in mother and in calf was already reported by Seboussi et al. (2009).

Regarding the concentration of selenium in camel milk (on average 2.08 ± 1.76 μg/100 mL), it appeared quite lower than in the previous study of Seboussi et al. (2009) which was on average 8.64 μg/100 mL in the camel without supplementation. Few references were available on selenium content in camel milk. Al-Awadi and Srikumar (2001) reported low values (1.39 μg/100 mL) but without mentioning the lactation stage. In cow milk, the selenium concentration could vary from 1.94 to 5.37 μg/100 mL with Se dietary selenium between 0.15 and 0.40 ppm (Juniper et al., 2006). In the review by Alaejos and Romero (1995), Se concentration in milk was regarded as decreasing in order from human to sheep, then goat, then cow. According to our results, Se in camel milk was comparable to ewe milk (Davis et al., 2008), but more analyses are necessary in different Se supplementation contexts to establish convenient references for camel milk.

The organic Se supplementation appears more efficient than the non-organic form to increase the selenium content in colostrum and in milk up to one month. Similar observation was done by Gunter et al. (2013) in cattle. Ortman and Pehrson (1999) reported that Se concentrations in milk were increased by more than 190% in cows fed with seleno-yeast compared to cows fed with sodium selenite or selenite. This proportion is quite comparable to our findings which suggest a more efficient incorporation of Se in milk, especially in proteins (Alaejos and Romero, 1995).

In all groups, and in spite of the maintenance of Se supplementation, the selenium concentration in milk decreased regularly up to a mean value of 1.0 μg/100 mL approximately, according to a similar trend observed by Seboussi et al. (2009) as it is shown in comparison (Fig. 5). Similar findings were reported by Salman et al. (2013) in dairy cattle. After 7 days post-partum, the Se content in milk decreased by 60%, 42% and 35% in the control, inorganic and organic groups, respectively (Salman et al., 2013). In our trial, the decrease after 30 days was more important in organic group (65%) compared to inorganic (61%) and control (45%). Other authors reported higher Se content in colostrum compared to normal milk in dairy cattle (Weiss and Hogan, 2005). Salman et al. (2013) reported 3.0, 2.4 and 2.5 times greater Se concentration in cow colostrum, in Se-yeast, sodium selenite and control groups, respectively. Those values are comparable to our results: 2.9, 2.6 and 1.8, respectively. In ewe, Davis et al. (2006) reported higher Se concentration in colostrum compared to milk at 28 days and 56 days post-partum, whatever the level of Se supplementation (given under selenite form). However, this trend is not described in all references. For example, in goat, Petrera et al. (2009) did not describe such a trend in Se concentration in milk after delivery. Selenium in milk being mainly associated to the protein fraction (Debski et al., 1987), the decrease in Se concentration in milk might be linked to the change in total protein content after parturition as it is suggested by the data of Musaad et al. (2013) regarding the milk composition of the camels from our experiment (Fig. 6). The casein fraction of milk contains the most important part (60%) of selenium in cow (Debski et al., 1987), but this proportion could change with the species. Camel milk contains less casein than cow milk, but other fractions could play an important role, notably the whey proteins. In colostrum, the most abundant fraction from whey protein is the immunoglobulins. Data on Se in camel colostrum are lacking, but it is stated that selenium could stimulate immuno-protection of the new-born (Rock et al., 2001).

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Figure 5

Post-partum changes in mean selenium concentration of mother (□) and calf serum (◊) and in milk ■ according to present results (A) and revisited data of Seboussi et al. (2009) (B).

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Figure 6

Post-partum changes in total milk protein ■ and milk selenium (□) concentrations in the camels from our experiment (data on milk protein from Musaad et al. (2013)).

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In the conditions of our trial, the Se-Org supplementation appeared to have a more efficient milk transfer than for non-organic. However, the negative correlation between selenium in milk and Se-serum in calf was surprising. It was not observed in the experiment of Seboussi et al. (2009). Moreover, this negative correlation was observed within each group. However, this negative correlation could be explained by the priority given to the maintenance of a suitable metabolism function in mother organism after the colostrum phase which allows an important supply of selenium for the new-born calf. In the same date, the correlation remained significantly positive for colostrum. Guyot et al. (2007), reported higher concentrations in Se-serum in calf suggesting that placental transfer of Se during pregnancy might be more efficient than through milk. Moreover, supplementation with inorganic Se could have a substantial effect when animals are fed with low Se diet, but the impact would be less with higher Se diet (Salman et al., 2013). In consequence, the amplitude of the increase in milk-Se might change according to the Se content in diet.

The Se status is also regulated by the fecal excretion which represents 55–75% of the excreted Se according to the level of supplementation in camel (Faye and Seboussi, 2009). As well as in dairy cattle (Juniper et al., 2006), and in camel (Seboussi et al., 2008), fecal Se excretion increased when animals were supplemented, but in our study, this increase was reported at d30. No difference was observed after 2 months post-partum in spite of the difference observed in serum. However, in milk also, there was no difference in Se excretion between groups after 2 months. The Se-fecal concentration in our study (56.9–177.8 g/kg according to the groups and dates) was lower than values reported by Seboussi et al. (2008) (562–603 g/kg according to level of supplementation in sodium selenite in non-pregnant, non lactating camels) and in 2009 (239–941 g/kg according to the level of supplementation in sodium selenite in lactating camels). In these two previous studies, the Se fecal concentration was measured in feces collected on animals supplemented with higher level of selenium in the diet and for a longer time. However, as for these previous studies and contrary to Juniper et al. (2006) in cattle, no linear effect was clearly observed between Se excretion and dietary selenium. The higher excretion in organic supplemented camels compared to inorganic supplemented ones, at least at d30, would suggest that the Se requirement was better reached with organic Se.

In camel, somatic cell count determination is not commonly used, but as for other species, could be used as indirect diagnostic tool for detecting uninfected and infected quarters (Saleh and Faye, 2011). Elsewhere, beneficial effect of better Se status after Se supplementation was described in cow, even if inconsistent results were reported (Hemingway, 1999). After intramammary inoculation with a strain of Staphyloccocus aureus in dairy cow, SCC was lower throughout the 7-day period post-inoculation in supplemented cows (with inorganic Se) compared to non-supplemented animals (Kruze et al., 2007). In our study, the variability within group was too important to observe any difference although the SCC values were in the normal range for a camel with only 3.5% of samples above 200,000 cells/mL and one sample above 400,000 cells/mL. In fact, SCC is a multifactorial response and the udder infection status is the predominant factor for explaining the observed variability rather than the Se status of the animal (Kruze et al., 2007; Nagy et al., 2013).

5 Conclusion

The more efficient effect of supplementation with organic selenium compared to non-organic was confirmed in camel as it was stated by several authors in other ruminating animals. Such supplementation in animals living in highly-deficient areas as the Arabian Peninsula, where the economical importance of camel is great, must be encouraged. In particular, organic selenium allows a better protection of the new-born camel by a higher Se transfer into milk just after parturition and by a better bioavailability of Se. As the young camels are often affected by sudden death syndrome linked to selenium deficiency, a convenient supplementation of the mother at the end of pregnancy and at the beginning of lactation has to be promoted in the camel farms. Moreover, as the Se supply by milk decreases regularly after delivery, the supplementation must be renewed in young camels after weaning, especially in deficient areas.