1. Introduction

For long time, only fresh camel milk was self-consumed by pastoralists and was regarded as a gift for the hosts coming under the tent of the nomads. Consequently, it was not considered a commodity and its sale was often taboo. Moreover, it did not undergo any transformation, except for fermentation ^[1] to prolong its shelf life in desert conditions where the cold chain could not be respected. The introduction of camel milk in regular market at national or even at international level is a recent feature^[2]. Such development of camel milk market was concomitant with a deepening of knowledge on its fine composition ^[3] and on its transformation processes allowing the marketing of a more diversified dairy products^[4] Recent findings are effectively available, allowing this important product renowned for its true or supposed “medicinal” virtues^[5] to put out camel milk from marginality.

Thus, the present paper is proposing a ‘state-of-art’ regarding knowledge on camel milk processing by focusing on 4 main dairy products having different success on market i.e., pasteurized milk, fermented milk, camel cheese, and camel milk powder. Other products will be rapidly evoked.

2. Pasteurized milk

Pasteurization of camel milk became commonly used technique in camel-countries. But still now, the conditions of pasteurization by each holder were decided often without taking in consideration the specificity of camel milk, the rules being mainly based on the standard issued from pasteurization of cow milk. Some data regarding the conditions of camel milk pasteurization in scientific literature were quite variables: 60⁰C for 30 minutes^[6]; 75⁰C for 15 seconds^[7]; 63⁰C for 30 minutes ^[8][9].

Indeed, the question of pasteurization’s procedure for camel milk should have its own conditions and indicators. A preliminary study showed for example that alkaline phosphatase (ALP), traditionally used for cow milk^[10], was not a convenient indicator of successful pasteurization of camel milk, because camel ALP is heat resistant showing still activity at 90⁰C ^[11]. Loiseau et al., ^[12] suggested to use glutamyltranspeptidase or leucine arylamidase as indicator of pasteurization for camel milk. If camel milk must be pasteurized at 72⁰C for 20 min, the most appropriate indicator could be gamma-glutamyl transferase (GGT) according to Wernery et al. ^[13]. But later in 2011, Lorenzen, et al. ^[14] concluded that GGT was still present in pasteurized camel milk, and probably lactoperoxidase (LPO) could be a more appropriate indicator of pasteurization.

The characteristics of camel milk flow in pipes during pasteurization process, the cleaning procedures, the conditions of transfer and of pumping need to be studied also. The behavior of fat globule and of casein micelle in camel milk is different from cow milk, giving absolute viscosity 1.72 mPa*s at 20⁰C, vs 2.04 mPa*s at same temperature in bovine milk. Thus, in dairy plant, the camel milk should be transferred not necessary at 20⁰C.

Some studies regarding behavior during heat treatment observed that camel milk could give an important amount of dry deposit on stillness steel plate during pasteurization process from 60 to 90⁰C for 1h or 2h^[15]. This study showed that such deposit is probably not protein origin, because free thiol groups are in lower quantity than for cow milk treatment. Probably camel milk is producing higher quantity of “milk stones”, the deposit of milk residues accumulated in insufficiently cleansed dairy equipment where bacteria can be multiplied, contributing to bad flavors in milk.

The rate of heat denaturation of whey proteins was twofold lower than for cow whey proteins^[16]. Because milk stability during heat treatment is the most important point and because the size of casein micelles could impact the milk preservation under homogenous solution, camel milk micelles size was measured before and after pasteurization. They are broader than that of cow and human milk. Some studies^[8][17] stated that pasteurization of camel milk could change chemical composition. The observation of camel whey protein shows that some proteins sensitively decrease after heat treatment, but in any case, less than for cows’ proteins. The pattern of camel whey proteins, and globally, the composition of proteins is not the same for camel and cow milk. Thus, major proteins of whey in bovine are serum albumin (SA), α-Lactalbumin (α-La), β-Lactoglobulin (β-Lg) and for camel are SA, α-La and 3 fractions which are not reported in cow milk ^{[16][18][19][20][21]}.

Heat resistance of camel milk could be revealed also by the heat coagulation time^[22]. Compositional difference plays important role on heat resistance, in particularly, the absence of β-lg, the different ratio in casein complex (higher quantity of αs1-, αs2-, β-caseins and lower quantity κ-casein compared to cow milk^[23]) and the presence in higher quantity of other whey proteins. Whey proteins include three proteins fractions described as common fractions of immunoglobulins (IgG1, IgG2, IgG3), α-lactalbumin, lactophorin which is closely related to the bovine proteose peptone component 3 (PP3), the innate immunity Peptido-Glycan Recognition Protein (PGRP) and the Whey Acidic Protein (WAP)^[24].

Regarding sterilization of camel milk by Ultra High Temperature (UHT) treatment, the situation appears quite blocked. Still now no possibilities to produce UHT camel milk directly occurs. All private companies are looking to find solution, but until now, there was no answer how to overcome this obstacle. After UHT treatment, camel milk presents a separation on two phases. To stabilize camel milk proteins after UHT treatment, different protocols as addition of chemicals (sodium hydroxide, calcium chloride, ĸ-casein from cow, sodium dihydrogen phosphate anhydrous, disodium hydrogen orthophosphate or EthylenDiaminTetraAcetic salt) were tested but with disappointing results ^[25] . Further and in-depth studies need to be implemented before to be able producing UHT camel milk. However, it is possible to get sterilized milk after reconstitution of liquid milk using camel milk powder. Moreover, ultrafiltration for making camel concentrated skim milk was tested experimentally^[26].

Camel milk pasteurization is achieved at industrial scale, and pasteurized camel milk can be proposed directly to consumers within a shelf-life of around a week. Some dairy plants had a long experience to produce pasteurized camel milk. However, further research is necessary, especially to study the rheological properties of raw and pasteurized camel milk, poorly documented up to now.

3. Fermented milk

The fermentation process is commonly used for the preservation of food. The process of milk fermentation, including camel milk, is a traditional ancestral method all over the world. It consists of the transformation of lactose into lactic acid by the natural microflora in milk dominated by lactic bacteria and in some cases by yeasts. For understanding this process, numerous investigations on microflora of raw camel milk were performed. As many fermented products from camel milk are produced by spontaneous fermentation for centuries, it is the key point to start our analysis of literature by global microflora (pathogenic or not) of raw camel milk. The high diversity of camel milk microflora has important technological interest, this microflora playing a main role both for antimicrobial activity and on acidification which is essential for fermented products and cheese processing. However, due to the antimicrobial properties of camel milk proteins in higher quantity than in cow milk^[27], and, in some cases, to the low hygienic status of the camel milk samples, the acidification process appears slower than for cow milk^[28]. The starters used in camel milk processing for fermentation or cheese making (mesophilic, thermophilic or their mixtures) lead to an acidification rate at 37°C between 33 and 79% lower than for cow milk ^[29].

The microflora biodiversity leads to a rich diversity of fermented beverages prepared from camel milk. Moreover, fermented form is one of the oldest ways of consumption of camel milk. Camel milk producers living in different regions of the world have their own varieties of fermented product with their specific taste, texture, and flavor. Nowadays each camel country describes their traditional fermented milk by microbiological, physico-chemical, chemical properties and sometimes volatile organic compound profiles. The most known fermented camel milks described in the literature are shubat in Kazakhstan^[30] and China^[31], khoormog in Mongolia ^[32], garris in Sudan^[33][34], suusac in Kenya^[35], laben (lben) in Arabic countries^[36], ititu and dhanaan in Ethiopia^[37][38]. Other traditional fermented beverages based on the mixture of camel milk and water are available in Mauritania under the name of zrig^[39], in Morocco as Lfrik^[40], and chal in Iran and Turkmenistan ^[41].

However, in most of the cases, the fermentation process is occurring spontaneously by using previously fermented milk to inoculate raw milk^[42]. Microflora in fermented product is consequently more diversified than raw milk samples^[43]. For example, traditional suusac (Kenyan fermented camel milk) contained 45 LAB and 3- yeasts identified by API50CHL and API20AUX. Such complex microflora ecosystem in fermented milk could lead to very variable final products, hardly compatible with the necessity to get product with standard organoleptic quality. For example, shubat which is prepared mainly by Kazakh people from Kazakhstan, Uzbekistan, Russia, Xinjiang region of China and Western part of Mongolia, is made by spontaneous fermentation leading often to the production of gas and foam, and sometimes giving particularly very acid product provoking some reluctance from urban consumers^[44]. Moreover, spontaneous fermentation can be affected by the presence of pathogenic strains of E. coli because the initial pH is not sufficient to suppress their growth^[45].

To solve these problems, a convenient way is the use of starter cultures, i.e., a preparation containing limited numbers of identified live microbial strains (single or mixed) inoculated in raw milk. Such management of controlled fermentation can lead to expected sensorial properties of the final product by contributing to flavor and texture adapted to the urban consumers’ taste. It contributes also to propose a standardized and safer product on the market. Unfortunately, despite the high biodiversity of camel milk microflora, starters cultures used in camel industry are mainly from bovine milk. However, industrial transfer remains difficult and requires supplementary studies regarding technological properties of the numerous strains available in natural fermented milk^[46]. Yet, beyond the commercial interest for the development of fermented milk with standardized organoleptic properties, there is also the public health benefit of such products thanks to their potential probiotic effect.

4. Camel cheese

Technical innovations regarding fermented camel milk are applied on a beverage known from prehistoric times to extend its shelf-life ^[47]. At reverse, the making of camel cheese itself was an innovation. Indeed, the difference in casein proportions (notably the low part of κ-casein) between cow and camel milk should explain the clotting difficulties observed in this last: 3-4% of κ-casein only vs 13-15% in cow's milk^[48]. Moreover, bovine chymosin used in dairy industry does not allow the optimal clotting of casein micelles from camel milk, leading to a weak curd. Thus, obtaining a firm coagulum was the first challenge of the camel scientists and dairy factories processing camel milk^[49].

The first trials for making camel cheese were achieved in the years 80 by using bovine rennet enriched in chloride and calcium phosphate and Rhizomucor miehei as coagulant (commercialized under the name of Camifloc ®), but the coagulum remained fragile and brittle ^[50]. Different vegetal coagulants were tested also as extracts from Zingiber officinale or from Moringa oleifera^[51] as well as abomasum extracts from young or adult camel^[52]. The solution to get a firm curd followed the sequencing of camel chymosin achieved by Kappeler, et al. ^[48] by introducing the coding gene for camel chymosin into a mould (Aspergillus niger). Later, this recombinant enzyme was produced by Chr. Hansen© at industrial scale and marketed from 2008 under the trade name Chymax-M1000®. However, if getting a good curd was a necessary condition, it was not sufficient to get a “good” cheese adapted to the consumers’ preference for taste, especially because most of the camel cheese making were set-up by scientists in their laboratory rather by cheese technicians in dairy plants, except in Mauritania^[53].

The variety of possible cheese being considerable, many trials are necessary to propose a large panel of products to the consumers. Different cheeses based on technology of gruyere ^[54], mozzarella^[55] or feta and halloumi making^[56] were tested, but the texture, the taste and flavor of the final product were not corresponding to the bovine equivalent. Indeed, the behavior of the camel “proteinic-lipidic matrix” during cheese processing differs from cattle milk. Such discrepancies between the milk from different dairy species require more fundamental investigations on rheological properties, and for understanding the changes during the different steps of acidification, coagulation, draining, brining, and refining as well as the effect of various starters and thermal treatment ^[49].

Comparison of the changes observed in the “proteinic-lipidic matrix” of camel and cow milk during cheese processing is a common feature in scientific literature to understand their respective “behavior’s” specificity. However, the comparison is of low interest when the gross composition of each specific milk differs significantly. To avoid this, Konuspayeva et al.^[56] adjusted cow milk for obtaining the same fat and total protein concentrations. Although they got similar cheese raw yields (7.4±0.15 vs 7.3±0.55 kg/100kg for camel and cow milk, respectively) and calcium recovery, camel cheese presented higher recovery in total nitrogen, and cow cheese in fat. Significant differences were observed also in lactoserum composition: camel lactoserum contained more fat and total nitrogen (9.0±1.73 g/kg and 9.21±0.23 g/kg, respectively) compared to cow (7.7±1.61 g/kg and 7.30±0.02 g/kg, respectively) despite similar dry matter (68.9±3.2 and 68.1±1.15% in camel and cow whey, respectively).

Two main technological difficulties in camel cheese processing are occurring: (i) the continuous removing of serum from curd, and (ii) the slow acidification of the curd. Indeed, contrary to cow cheese where ripening is started after curdling with rapid appearance of crust formation, camel cheese is characterized by a weak crusting and a continuous loss of wet, due to serum release, leading often to very dry curd what hinders correct ripening. Such behavior can be favorable for some types of cheese (as Feta type), but not for hard cheese^[49]. Starters as thermophilic ones containing Lactobacillus helveticus, and L. lactis or Streptococcus thermophilus, known for their high-acidifying power can be used also to improve acidification process^[56]. However, as for the management of fermentation to get specific fermented products, camel cheese manufacturing is not using starters made with lactic bacteria isolated from camel milk. The challenge for scientists and cheese makers could be the identification of LAB strains specific to camel milk allowing to provide typic aroma of cheese and to enrich the camel cheese variety proposed to the consumers.

Up to now, scientists and cheesemakers aim to make cheese by using the same methodology than for cow cheese. But when Feta or Mozzarella-type cheese are prepared with camel milk, the results are often disappointing because taste, texture and consistency appear far away from the same cheese made with cow milk. In the Middle East, where the consumers prefer products with neutral taste, it is difficult to expect the development of cheese with strong character as in Western Europe. To achieve products adapted to the local consumers, different trials were reported to propose for example spread cheese^[57] or white soft cheese^[58][59].

The industrial development of camel cheese making is limited not only by the technological difficulties, but also by the hygienic quality of raw milk, notably because it is difficult to coagulate camel milk after pasteurization forcing manufacturers to work with raw milk. The use of halloumi-type cheese technology^[56] is an interesting alternative because the coagulum is pasteurized in lactoserum for 10 minutes at 80°C after pressing. A second difficulty is linked to the cost of camel cheese due to the high price of the primary matter^[60]. An alternative could be the valorization of lactoserum which represents 88 to 90% of the initial milk volume.

5. Camel milk powder

As said in introduction, the contribution of camel milk to international dairy market is very recent and was possible thanks to the development of powder milk production which is the best way to preserve this highly perishable product for later consumption. Moreover, camel milk being produced often in remote places far away from consumption basin, it is the only solution to transport high quantity of milk by removing the water it contains (88 to 90% of the weight). The advantage is also the conservation of the nutritive value of liquid milk. To make camel milk powder, two main modern technologies were used: spray-drying (hot-drying) and lyophilization (freeze-drying).

The spray-drying method seems preferable to make camel milk powder for a better reconstitution of liquid milk, but the investment for dairy industry is more important as it requires the procurement of a costly milk drying tower and sprayer. However, the powder obtained by freeze-drying (lyophilization) could be used by agro-food industries (pastry and chocolate factories).

Nevertheless, the main limit is that drying is consuming high level of energy. In dairy industry, spray-drying process has a higher energy demand per tonne of end product, even if recent technical improvement and novel equipment has decreased the energy consumption per ton of finished product. Moreover, the high investment to get and to use a drying tower for making milk powder requires a sufficient volume of raw matter which is only possible in certain contexts as big camel dairy farm or collecting centres with a large network of camel farms.

The main problem with camel milk during high-temperature heat treatment, as happens during spraying, is the denaturation of proteins (especially whey proteins), which explains the difficulty to obtain UHT milk. To keep powder milk in the best possible conditions, and to facilitate the solubility of the powder to replenish the liquid milk, the surface composition of the powder is essential^[61]. This surface of spray-dried emulsion is naturally composed mainly of fat (mostly triglycerides), but is composed also of proteins. Thus, the denaturation of serum proteins at high temperature increases the fatty surface part of the powder and makes it difficult to replenish liquid milk. For a better emulsion during this reconstruction, it is proposed to perform an "encapsulation" by sodium caseinates that ensure a stability of the powder. Such encapsulation is improved with the presence of lactose. For example, surface fat decreases from 30 to less than 5% if lactose is 1:1 related to sodium caseinate.

In the following description (Table 1), possible improvements are reported to obtain a quality powder of stable quality due to the specificities of camel milk.

Table 1. Possible improvements to get camel milk powder with high quality

6. Other products

6.1. Yogurt

Ample literature is available on the possibility of making yoghurt with camel milk ^[62][63]. Several strains of conventional lactic bacteria have been tested such as Lactobacillus bulgaricus or Streptococcus thermophilus^[64], but also L. acidophilus, L. casei and Bifidobacteria ^[65].

However, the manufacture of camel milk yoghurt poses a texture problem, the product appearing sticky and ultimately unpleasant to the palate^[66]. Indeed, the viscosity of the product does not change during the gelling process compared to the milk of other dairy species. To obtain a better texture, trials with the addition of gelatin, alginate or calcium were attempted^[67] or using ferments producing exo-polysaccharides ^[68]. The application of high-pressure treatment could have positive effect on the texture, but no trials have been conducted to date with camel milk^[69].

Other authors have attempted to improve the manufacture of camel milk yoghurt by mixing with milk from other species ^[70] or by introducing 0.75% biosynthesised xanthan, however with medium results in terms of organoleptic properties^[71]. In any case, the final product corresponds at best to a "drinking yoghurt" without having the taste qualities, even when natural or synthetic aromas are added ^[72]. These difficulties explain why there is not really industrial production of camel milk yoghurt at present.

6.2. Butter and sweet

The fat in camel milk contains less than 0.5% butyric acid^[73] compared to almost 5% in cow's milk. In addition, fat cells are smaller than in cow's milk^[74]. As a result, butter yield is low^[75] and with disappointing organoleptic property^[75][76]. To obtain fat cells at the time of butter production, it is necessary to make vigorous hot shaking (22-23°C), which allows to recover about 80% of the fat ^[75]. Ghee (clarified butter), a popular product in India, has also been attempted from camel milk^[77] but in addition to very low yield compared to buffalo or cow's milk, the final product has been found to be more susceptible to rancidity. Transformation into butter therefore does not seem fundamentally interesting in the context of an industrial valuation of camel milk. In fact, apart from trials in Ethiopia where butter consumption, including rancid for certain recipes, is popular, the production of camel butter has little future.

Making ice creams with different flavours is an easy technology. Ice-cream made of camel milk are commercialized in the United Arab Emirates, Morocco or Kazakhstan. The same technology is used than for other milks. Ice cream is very popular among consumers and, above all, with less reluctance than for other products. However, very few studies on texture and sensory properties have been conducted^[78].

There is no reference on processing camel milk into sweets. However, traditional products are available. For example, in Kazakhstan, a caramel called Balkailmak is obtained after a long thermal treatment of about ten hours at boiling temperature. The introduction of milk powder in chocolate as proposed in the Emirates can be recalled also.

7. Conclusion

The "modernized" processing of camel milk is a recent feature compared to the milk from other dairy species. However, the technologies used to transform milk into pasteurized or fermented products, cheese or yoghurt, powder or various sweets face to two main challenges: (i) the systematic application of already proven technologies for cow's milk is not necessarily suitable for camel milk, and requires adaptations based on more fundamental research on the behavior of milk components during processing; (ii) the transfer of laboratory results already relatively numerous to industrial scale remains insufficient, especially for products such as cheese or yoghurt, and requires additional technical and economic analyses. The worldwide keen interest for camel milk, which is largely due to its expected health effect for consumers, is prompting basic research and development to continue investigations in order to translate technological innovations into products available on a large scale.