Abstract
Minerals in camel milk are presented among elements contributing to its reputation for health benefit to consumers Both major and trace minerals are not in exceptional quantity compared to other species except cations (K, Na, Cl) and probably iron and zinc. There is a lack of data regarding the effect of diet composition on mineral concentration of camel milk. The potential and expected therapeutic effect of a regular camel milk (CM) consumption on different diseases is a strong commercial argument usually justifying the high price of the product on market compared to cow milk (Konuspayeva et al., 2021). Making confusion between “health effect” and “medicinal virtues”, many scientists are looking for the bioactive components potentially explaining the beneficial impact of CM consumption on human health. Generally speaking, many review papers on “medicinal properties” of CM (for example, Abdelgader and Al-Haider, 2016; Hassen, 2020) emphasize the richness of this milk in some components as minerals and vitamins. Whether or not the mineral composition of CM is unique comparing to other domestic species is unknown. Yet, except for vitamin C, niacin (vitamin B3) and vitamin D, the concentrations of other vitamins are not so high or even can be in lower quantity than cow milk (Faye et al., 2019). The question of the mineral composition is obviously important to support the idea that CM is also exceptional in this matter. Thus, the objective of the present review was to provide up-to-date data on the mineral composition of CM based on available references. The number of references regarding mineral concentrations in CM is relatively limited compared to data available on cow or small ruminants’ milk. Moreover, a certain confusion occurred due to the variable analytical techniques that could change with the progress in sensitivity and accuracy of laboratory equipment for the last years, and with the units used by the authors for presenting their results. The most popular equipment to determine the minerals in milk is atomic absorption spectrophotometry or inductively coupled argon plasma-atomic emission spectrometer (ICP-AES). For some elements as iodine or molybdenum, colorimetric methods are preferred, but chromatographic methods have been also proposed. For selenium, fluorimetry was used formerly, and different types of spectrometry are used nowadays. For a better understanding, the present review displays the results, element by element and as far as it will be possible, an effort was done to convert all published data into similar units to make comparison easier. However, an important risk of contamination (especially with trace elements) could occur during sampling collection and preparation procedure with a potential high impact on the results. Such contaminations could explain sometimes high reported values, well above most of the available references. The main minerals in milk are calcium, phosphorus, magnesium, sodium, potassium, and chlorides. These minerals are generally electrically charged, and it is possible to distinguish the cations (positively charged as Ca++, Mg++, Na+, K+) from the anions (Cl−, PO43−). Some elements (Ca++, Mg++, PO43−) are associated with milk proteins, contributing notably to form casein micelles (colloidal particles) involved in cheese processing. Some minerals are diffusible (Na+, K+, Cl−) and contribute for example to the salty taste, especially when the camels are grazing halophytes. Although their global quantity in CM rarely overpasses 1 g/L, they can provide an important part of the requirements for the baby camel and for the consumers. In a previous meta-analysis compiling 121 references on CM composition (Konuspayeva, 2020), the mean value of total minerals in CM was 0.81 ± 0.19 g/L (0.58–2.48 g/L). The values of total calcium in CM are comprised between 0.3 and 2.57 g/L (Faye and Bengoumi, 2018). A part of this variability could be attributed to water repletion status. Indeed, camels are known for their ability to space out watering, and the dehydration status can influence milk calcium concentration (Yagil and Etzion, 1980). In a comparative study involving different camel species living in the same environment (Faye et al., 2008), calcium content in Bactrian CM appeared significantly higher (1.30 ± 0.29 g/L) than in dromedary milk (1.16 ± 0.27 g/L) while crossbreed Bactrian*dromedary presented intermediary value (1.23 ± 0.27 g/L). In China, Jirimutu et al., (2010) reported similar calcium concentrations in milk from wild Bactrian (Camelus b. ferus) and from Bactrian (Camelus bactrianus): 1.43 ± 0.05 g/L vs. 1.23 ± 0.08 to 1.83 ± 0.19 g/L according to different farms. Some other variation factors were investigated as the camel breeds (Mehaia et al., 1995; Al-Haj et al., 2022), the degree of intensification in farming systems (Alwan and Zwaik, 2014) with contradictory results. The physiological stage is also linked to a variation of calcium content in milk. For some authors, calcium is increasing at the end of lactation (Mal et al., 2007), but the colostrum collected at parturition contained more calcium than that of 10 d postpartum milk: 1.75 ± 0.16 g/L vs. 1.21 ± 0.17 g/L (El-Khasmi et al., 2001). However, in a monitoring of minerals in Arvana camel (dromedary) throughout the lactation (Konuspayeva et al., 2010), the maximum value of milk calcium was observed at early lactation (1.43 g/L), and the minimum at the lactation peak (0.70 g/L). Monthly variation was also reported in Jordan dromedaries (Haddadin et al., 2008), probably linked to lactation stage of the dairy camels as their reproduction cycle is seasonal: indeed, the beginning of lactation occurring in winter, the highest concentration was observed in January while the peak of lactation occurring in summer, the lowest was observed in August (Figure 1). Monthly changes of calcium and phosphorus concentration in CM from Jordan (calculated from Haddadin et al., 2008). There are few data regarding the impact of heat treatment on calcium content in CM. Recently, Al-Haj et al., (2022) found significant differences in calcium content between heat-treated and raw CM samples. Moreover, heat treatment decreasing the concentration of ionic calcium, it induces an inhibition of rennet coagulation (Metwalli and Hailu, 2020). However, the same calcium level was observed in pasteurized CM at 72 °C for 5 min compared to raw milk. Contrary to cow milk, calcium in CM seems more stable after heat treatment at 80 °C for 60 min (Felfoul et al., 2016). The addition of calcium during rennet coagulation of CM was not necessary to improve curd, whatever source – calcium phosphate or calcium chloride – as there was no impact on the coagulation yield. Compared to milk from other species, results were not always coherent. Globally, CM is containing comparable calcium concentration (0.70 ± 0.09) than in cow (0.66 ± 0.04), goat (0.75 ± 0.07), and sheep milk (0.82 ± 0.01 g/L) (Al-Wabel, 2008). However, in Egypt, if calcium content in CM (1.20 ± 0.07) is like in cow milk (1.11 ± 0.04), goat (1.30 ± 0.02), and buffalo milk (1.63 ± 0.05 g/L) contained significantly more (Soliman, 2005). On the other hand, in old references, lower calcium values were found in CM (0.40–0.94 g/L) than in goat milk (1.33 g/L). Quite questionable higher calcium content in goat milk compared to CM was reported also recently: 12.82 vs. 1.16 g/L. So, even if CM is regarded as an important source of calcium, the amount in this mineral is not exceptional compared to other milk origin. The total quantity of phosphorus in CM is lower than calcium. Literature data give a range of 0.34 to 1.00g/L (Faye and Bengoumi, 2018). A narrow range was revealed in older references 0.86–1.39 g/L. Variation factors as farming system were also investigated by different authors, and reverse to calcium, it was found significant higher phosphorus concentration in milk from intensive farm than in Bedouin system. Regarding the effect of lactation stage, Mal et al., (2007) found similar pattern than for calcium, i.e., lower concentration in early lactation (0.42 ± 0.05) than in late (0.47 ± 00.5 g/L) and El-Khasmi et al., (2001) reported higher content in colostrum at parturition (1.1 ± 0.014 g/L), than 10th day postpartum (0.82 ± 0.10 g/L). In the study of Konuspayeva et al., (2010), the changes throughout the lactation were parallel to calcium, the maximum value (1.16 g/L) being observed at early lactation and minimal (0.57 g/L) at the peak of lactation. Consequently, the ratio Ca/P was relatively constant and correlation between P and Ca values, highly significant (Konuspayeva et al., 2008). Heat treatment of raw CM for processing seems to have no impact on phosphorus content (Metwalli and Hailu, 2020). As for calcium, phosphorus is in higher concentration in Bactrian milk (1.08 ± 0.18) than in dromedary milk (0.91 ± 0.19 g/L) with significant seasonal variation, values in summer being significantly lower than in spring and winter (Konuspayeva et al., 2008). In dromedary milk and in another climatic context (Haddadin et al., 2008), the lowest value in phosphorus was observed in August (0.61 g/L), and the highest in December (0.99 g/L) (Figure 1). The phosphorus content in milk is the main discriminating component allowing to distinguish Bactrian milk from dromedary milk (Faye et al., 2008). Such difference could be attributed to the higher fat content in Bactrian milk, notably in phospholipids. The ratio Ca/P, at least in camels (Bactrian and dromedary) from Kazakhstan where the 2 species are cohabiting, appears the lower among all other specific milk (Figure 2). Ratio Ca/P in milk from different species including different camel species from Kazakhstan (KZ) and other dromedaries (estimated from literature data). In comparative studies, phosphorus content in CM appears generally lower than in cow, goat, and buffalo milk: 0.81 ± 0.031 vs. respectively 0.95 ± 0.072, 1.10 ± 0.016, and 1.11 ± 0.026 g/L (Soliman, 2005). The lower phosphorus values in CM compared to goat were confirmed later: 0.87 vs. 1.31 g/L. In a recent comparative study (Khaldi et al., 2022), phosphorus recorded in Gharbi sheep milk was 1.45 ± 0.19 vs. 1.18 ± 0.24 in goat and 0.58 ± 0.18 in Maghrebi CM. Thus, as for calcium, the concentration of phosphorus in CM is not exceptional. Magnesium concentrations in CM varied between 45 and 200 mg/L. For example, 130 ± 11 to 116 ± 16 mg/L in different Saudi camel breeds (Mehaia et al., 1995), 73 ± 3.2 to 110 ± 5.7 mg/L according to different farming systems (Alwan and Zwaik, 2014) or 90 ± 8.6 mg/L in Jordan with a monthly range of 77–98 (Haddadin et al., 2008). As for the other cations, magnesium concentration is higher in colostrum (236 ± 31) than in milk: 112 ± 22 mg/L (El-Khasmi et al., 2001). However, in Kenya, slightly lower values in early lactation were reported compared to late lactation: 118.2 ± 2.2 vs. 135.8 ± 3.1 mg/L (Oselu et al., 2022). In Chinese Bactrian camel, a range of 58.5–96.7 mg/L was reported (Chen et al., 2020). In their comparative data regarding wild and domestic Bactrian camels, Jirimutu et al., (2010) found more magnesium in the first: 111.3 ± 2.6 vs. 63 ± 1 to 92.5 ± 2 mg/L in different camel farms. Compared to other species, magnesium appears in lower quantity. For example, 67 ± 14 in camel vs. 295.6 ± 7.9 in buffalo, 134.2 ± 2.4 in cow, and 138.7 ± 1.1 mg/L in goat milk (Soliman, 2005). However, in recent results, Chen et al., (2020) did not find statistical differences between magnesium content in camel (79.6 ± 33.2), goat (92.5 ± 12.0), cow (83.2 ± 10.3), buffalo (58.5 ± 11.3), and yak milk (96.7 ± 12.3 mg/L), contrary to Felfoul et al., (2016): 83 ± 0.0 vs. 120 ± 1.0 mg/L in camel and cow respectively. Globally, with a range of 97–146 mg/L, cow milk contains more magnesium than camel milk. Contrary to cations, the concentrations in anions appear more important in CM. The range of sodium in CM is 220–690 mg/L (Faye and Bengoumi, 2018), but values up to 902 ± 92 mg/L were cited (Bengoumi et al., 1998). For Al-Haj and Al-Kanhal (2010), mean sodium value in CM was 590 ± 160 mg/L. The variation factors are obviously the same than for cations: sodium content is higher in late lactation compared to early lactation: 815.9 ± 20.8 vs. 682 ± 12 mg/L (Mal et al., 2007). Similar figure was reported by Oselu et al., (2022), but not by Alwan and Zwaik (2014) where the physiological changes were not significant. With an average of 575 ± 118 mg/L all over the year, a marked monthly variability was observed (Haddadin et al., 2008) with higher values in summer (Figure 3). Monthly changes of sodium and concentration in CM from Jordan (calculated from Haddadin et al., 2008). In their comparison between farming Alwan and Zwaik (2014) found higher sodium concentrations in milk than from intensive Such difference could be by the of in while the diet in intensive is of CM in is more Compared to other species, CM contains more more in Bactrian milk compared to cow or goat milk et al., Similar pattern was reported (Chen et al., ± mg/L for CM vs. ± ± ± and ± Similar was observed by including sheep milk. Although CM contained more sodium than other species, the differences were marked in the of ± in CM vs. ± in buffalo, ± in cow, ± in goat, and ± mg/L in human milk. content in CM is generally the values being comprised between and mg/L (Faye and Bengoumi, 2018), but concentrations above mg/L are cited (Bengoumi et al., Mal et al., 2007). no difference was important throughout lactation or are (Mal et al., with higher values at late lactation. same increasing was reported in from early to late lactation (Oselu et al., 2022), whatever the farming system (Alwan and Zwaik, higher level of was observed from to (Figure i.e., when most of the camels are in late lactation. at the end of summer is 2 higher than in winter from to mg/L (Haddadin et al., 2008). Contrary to most of the in camel colostrum was than in milk: ± vs. ± mg/L respectively and data been found between other For example, for Chen et level in Bactrian CM ± is lower than in goat ± cow ± and yak milk ± 200 buffalo milk ± presented lower Yet, in another et al., 2010), Bactrian CM contained high level of potassium, between ± and ± mg/L according to different farms. but with questionable values (Al-Wabel, 2008), CM comparable values to that of sheep milk and significantly higher than cow and goat milk. In Egypt, found slightly significant difference between level on camel ± cow ± buffalo ± and goat ± There are few data regarding chloride in CM. values range mg/L, but lower values were reported dehydration (Figure chloride content in milk by as well as while sodium by (Yagil et al., 1980). changes in main minerals in CM after 2 of and of 10 d dehydration by 2 during summer (calculated from and Etzion, 1980). to the sensitivity of the during the of a seasonal variation was observed with lower values in summer of intensive than in The comparison between species is the high variability in camel linked to its status. The of camel in looking for is the main for the higher concentrations in milk chloride compared to cow or buffalo milk and is generally that CM contains also high of trace especially iron and zinc. is based on a limited number of elements are necessary in quantity in the diet and in of milk is of the to the Globally, regarding of trace elements in milk, data are and rarely on mineral change according to different variation factors as diet physiological stage, or health status. Moreover, the analytical were not between references and could explain some of the in the published it is not to the and a high variability in available data is content in CM from to (Faye and Bengoumi, but more values are in the For example, in ± (Bengoumi et al., while values were found in et al., 2008). In Bactrian camel, a mean value of was There are few data regarding the effect of on the CM mineral status. On camels trace element et did not significant change in the milk content between and camels Regarding the comparative studies, an confusion is to old references (for example in CM is comparable to that of goat milk while in no difference was found with cow, goat, and sheep milk. In their and Bengoumi, that CM contained 12 more than cow milk vs. and found more in CM ± than in cow ± buffalo ± and goat milk ± 1.0 quantity of in CM was also found by compared to small vs. in goat and in while cow milk was In the recent study of Chen et in on Bactrian camel, the between species was as yak ± camel ± buffalo ± milk ± and the cow milk ± For other authors, CM is the regarding content in milk is highly variable according to authors Thus, the values are not and probably the results reported in the literature are on the analytical and potential being in zinc. A range of was In CM from different of a mean of was with significant variation, and range between camel from to content also according to lactation stage with a significant to throughout the lactation to and according to the farming the milk collected in system being ± than in intensive ± (Alwan and Zwaik, However, there were no seasonal (Haddadin et al., 2008). The effect of in diet of camel was by et al., with a of concentration in milk from to In Kazakhstan et al., 2008), concentration in higher quantity in milk compared to raw milk from the same Similar were done regarding in camel compared to raw milk: vs. on average and 2016). concentration and by a 5 during Contrary to in camel colostrum is in higher concentration ± than in milk ± and In most of the comparative and seems to be in higher concentration than in other et that CM contained more than cow milk: vs. respectively. Such difference was confirmed on Bactrian camel et al., Jirimutu et al., et al., However, for content in CM ± was lower than in goat milk ± For concentration in CM was ± vs. ± 10 ± ± similar were reported by Chen et In the of et al., in CM was ± i.e., 2 the values of other Although most authors the richness of CM in some references did not results (Al-Wabel, 2008). is of the most important trace elements for the as their requirements are high and milk of the is the source of for other data regarding iron content in CM are highly variable between references with contradictory regarding the comparison with milk from other species (Faye and Bengoumi, 2018). For example, between the data of and and that of and the is in a ratio of and respectively. In the old of et even lower value was Generally speaking, the lack of in analytical methods could contribute to a certain of published results. of the recent references, values in Bactrian camel, ± et al., 2008), ± (Konuspayeva et al., 2008). In comparison to dromedary milk, Bactrian CM presented higher iron concentration to iron as a potential element to the specific of the milk (Faye et al., ± for Bactrian vs. ± for There is a lack of variability and of the effect of iron et al., contains more iron than milk: ± 2 vs. ± and but with stable quantity throughout the 2008). As the between species is not For some authors, CM contains more iron than other milk and 2005). In few references, goat milk contained more iron than CM. In Bactrian camel, CM contained 5 more iron than in cow and than in goat milk et al., However, Chen et (2020) found iron in CM ± than cow ± and yak milk ± but more than goat ± and buffalo milk ± 2.4 For CM was the milk compared to all other domestic Thus, like for other the that CM is in iron and for be into richness is on the context and the are based on milk from different is in probably it is not a of its Moreover, data from the literature are not from 2008) to 1998). colostrum contained more ± than milk ± and The are no significant difference et al., 2008), more in CM than in cow and human milk and In the comparative study of Chen et content in CM ± was comparable to that of cow ± buffalo ± and goat milk ± 3.1 yak milk significant higher value ± Thus, the richness of CM in as by some review is not references are available on content in but the same could be done on the high variability in the available In their on in camels different of and found values in a range of to with an average of ± in camels vs. ± in However, lower values ± 2.4 were reported by and The of in camel was regarded as as the mean value in colostrum was ± in baby camels from vs. ± in (Faye and is higher content was observed in colostrum compared to camel with (Faye et al., colostrum contained higher concentration ± to ± at postpartum (Faye et al., there was no regarding comparison between species, except in Chen et al., (2020) where in CM appeared significantly lower ± than in cow milk ± and similar to goat ± and buffalo milk ± but higher than yak milk ± However, camel appears to (Faye and data are available on other trace elements in CM and most of the values are reported of the context stage, mineral in the Regarding molybdenum, CM concentration is references are available also on other specific milk, the was in CM in (Chen et al., 2020) and comparable values, ± and ± 10 respectively that is higher than in other species and was in Bactrian camel and wild Bactrian CM ± in et The other trace elements in milk by Chen et al., (2020) were ± 0.29 ± ± and ± Compared to other species, CM contained more In the of and mean value for was higher but not and were also in CM (Chen et al., 2020), but they are more than of many review papers regarding CM the mineral composition is not different from cow milk. The main of the mineral composition of CM is its richness in Na, and and probably iron and zinc. However, due to the lack of regarding the effect of some notably the level of minerals in it is to a camel or Moreover, the variability in analytical and the lack of accuracy in the used by authors, in highly contradictory results, to some published data as highly important effort be done by the to a status of the mineral composition of CM potentially explaining some of the attributed health of of at Konuspayeva is a of the of and in for in Saudi at the in and the where on the composition and processing of camel milk. out on this in and with for the and in the of and at in is also of is a at of on the of the of the camel milk in the of in and in for and of as of for in for as of study on camel mineral in of camel scientists and of the for and on present of In in Saudi as in a camel at and camel of 45 and 12 and Bengoumi, and January in in the as a including a of in been of and for more than at the and in more than and the in as of and health in the and the same at the for the with the of the for