Nutritional Value Of Dairy Products Of Ewe And Goat Milk
The composition of ewe and goat milks varies over a wide range because of genetic differences between species, between breeds within species and within breeds. These genetic differences have considerable influences on the cheese-making process and on human digestion of these milks. Furthermore, the stage of lactation, daily variation, season, parity, type of diet, physiological status, health of the udder and processing procedures change the contents and levels of major and minor constituents in the milks and its products. This provides, therefore, considerable potential to tailor-make ewe and goat milks according to the needs and preferences of consumers, and to provide an alternative to cow's milk, where this is economically or medically advantageous. But more research documentation is needed in this area.
The aim of this paper is to focus on properties and attributes of the milk and dairy products from ewes and goats as they contribute to human nutrition.
The composition of the milk of ewes and goats and factors affecting it has been reviewed comprehensively (Parkash & Jenness, 1968; Jenness, 1980; Anifantakis, 1986; Juarez & Ramos, 1986). Further important contributions have been published by Anifantakis et al. (1980), Merin et al. (1988), Casoli et al. (1989), Voutsinas et al. (1990), Espie & Mullan (1990), Simos et. al. (1991), Haenlein (1992), Peeters, et al. (1992), Park (1992; 1994), Sakul & Boylan (1992), Agnihotri & Prasad (1993), Bindal & Wadhwa (1993), Quiles et al. (1994), O'Connor (1994), Kalantzopoulos (1994) among others. However, only a few deal with the relation to human nutritional needs, which has been pointed out by Charlet (1981) "...the variation of composition of milk has not received the attention it deserves, except by a few workers". This is still largely true today and a 1st World Congress of Dairy Products in Human Health and Nutrition gave ewe and goat milk no recognition and deserved coverage, when it was held in Spain in 1993 (Serrano Rios et al., 1994).
Interest in the original properties of milk, as it comes from the farm, should be high, when it is consumed as fluid whole milk, partly skimmed or as yogurt. Dairy products, mainly cheeses (except those made from whey) contain only the casein and fat fractions of milk, but no whey proteins, nor lactose and soluble minerals, so interest may be limited here to the original composition of casein and fat only, and changes during cheese fermentation. Ewe milk, depending on region and economic conditions, is mostly processed into cheeses and yogurt. Goat milk on the other hand, in some countries, is consumed as fluid milk, even on a commercial basis, besides being processed into dairy products. Therefore, the characteristics of all components of goat milk are of considerable market interest.
Interest in the nutritive value of ewe milk is concerned mostly with the yield and evaluation of its cheeses and yogurt. Interest in the nutritive value of goat milk includes all fractions and how they may differ from those in the milk of other species. In order to sell goat and ewe milks and their products for human consumption, their needs and tastes, it is of considerable market advantage to know the factors that cause milk composition to vary and to what extend. This will be even more important in the future, when it becomes better known how to change original farm milk composition by manipulating e.g. the feeding of goats and ewes in order to tailor-make milk to the needs of diet conscious and disease afflicted consumers and their children, and to satisfy consumers with higher incomes, who have developed a sophisticated connoisseur taste for goat and ewe milk products.
Ewe and goat milk has considerable economic importance in some countries. The Mediterranean region produces 66 percent of the world's ewe milk (Table 1) and 18 percent of the world's goats milk (Table 2) (FAO, 1994). Of all milk produced by cows, buffaloes, ewes and goats combined, ewe milk makes up 1.5 percent and goat milk 2.0 percent of the world total, but in the Mediterranean region it is 11.7 percent and 3.3 percent, respectively. In at least 7 countries, including Greece, ewe milk or goat milk is more than 20 percent of all milk produced; and in at least 10 countries the combined production of ewe and goat milk is more than 20 percent of all milk in that country (Table 3 and 4) (FAO, 1994). Some countries, including Greece, have more than 1 ewe and goat combined per person (Table 3) and at least half of the countries with leading ewe and goat populations have more than 1 ewe and goat combined per hectare permanent pasture land, again Greece included.
The significance of ewe and goat milk for human nutrition in these countries varies widely (Table 4) from less than 5 kg all milk per person per year to more than 450 kg, assuming that the FAO statistics, which are very difficult to obtain in some countries, approximate the real conditions. The food supply for protein or calcium from all animal sources, including milk and dairy products, also varies greatly between these countries (Table 4), and averages in many countries far below the minimum daily requirements of 65 g protein and 800 mg calcium (NRC, 1968). This gives much support to the contention that improved ewe and goat milk production is one of the best strategies to relieve human starvation, undernutrition and malnutrition and therefore has great market growth potential, incentive and justification, especially in areas where pasture conditions, climate, mountainous terrain and economic conditions favor small ruminants.
The market of ewe and goat milks and their products has essentially three aspects:
Knowledge of the nutritive values of ewe and goat milks, what causes them to be different or to change, and comparison with cow's and human milks will help each of these markets. Some evidence from recent research with ewes and goats comprises this review.
FACTORS AFFECTING MILK COMPOSITION
Average genetic composition differences between species, ewe versus goat versus cow, and compared to human milk are considerable (Posati & Orr, 1976) in absolute and relative terms (Table 5, 6). Ewe milk is generally much higher in solids contents than goat, cow's or human milks, but composition categories and contents of individual minerals, fatty acids and amino acids vary in different directions between the species, and without relation to higher or lower solids contents. The high solids content of ewe milk makes it generally superior to goat or cow milk for processing into cheese and yogurt, because of higher yield and firmer processing quality without additives. However, this must be balanced in economic terms against lactation milk yield and lactation length of milking ewes, which is much less and shorter than for goats or cows. Nevertheless, published average data of milk of different species have to be used with caution, because within each species there are great genetic differences due to breeds and selected families, which can be used to market advantage.
Genetic differences in milk composition within species have a wide range for ewe milk fat from 4.6 percent to 12.6 percent (Casoli et al., 1989) and an average of 7.1 percent (Anifantakis, 1986); for ewe milk protein from 4.8 to 7.2 percent and an average of 5.7 percent, depending on breed. Other components follow these ranges. It must be emphasized that cow's milks, when ewe or goat milks are compared with them, also have a wide composition range due to breeds, e.g. average Holstein milk fat at 3.4 percent versus average Jersey milk fat at 5.1 percent, and milk protein from 3.3 percent to 3.9 percent (Anifantakis, 1986), besides other breeds. Goat milk composition likewise can have great differences, depending on breed, e.g. for milk fat from 2.3 percent to 6.9 percent (Juarez, 1986) and an average of 3.3 percent; for goat milk protein from 2.2 percent to 5.1 percent and an average of 3.4 percent. A major portion of this variation includes negative correlations between milk yield and composition, i.e. low yields have higher contents and vice versa.
Within species within breed one can identify through selective breeding considerable differences in milk composition. This includes genetic polymorphisms of milk proteins, which have commercial importance in cheese making, because they influence rennetability, cheese yield and flavor (Remeuf & Lenoir, 1986; Martin, 1993; Chianese et al., 1993; Heil & Dumont, 1993; Kalantzopoulos, 1994), and which have potential but yet poorly understood values in human nutrition (Haenlein, 1991). Genetic polymorphisms of beta-lactoglobulin, alpha-s-1-, beta- and kappa-casein affect firmness and viscosity of yogurt, rennet coagulation time, curd syneresis, heat stability, contents of casein, total solids, phosphorus and pH. Amino acid substitutions have been identified for the DNA sequences of caprine, ovine and bovine milk protein genes (Martin, 1993; Folch et al., 1994) and have been related to the different behavior of milk proteins in processing.
Some goat milk has low casein contents and unsatisfactory rennet coagulation ability, which affects cheese yield (Remeuf & Lenoir, 1986; Ambrosoli et al., 1988). Goat milk casein has the same four proteins, alpha-s-1, alpha-s-2, beta and kappa, as cow's milk casein, but genetic differences by breeds and individuals in alpha-s-1 casein range quantitatively from zero or "null type" ( O ) to "low types" ( F, D ) and "very high types" ( A, B, C ), with intermediate classes ( E ). Some goat and sheep breeds differ significantly in the frequencies of the polymorphic loci of milk protein types (Jordana et al., 1995) (Table 7), with considerable processing and nutritional consequences. Low alpha-s-1 casein types of goat milk have shorter coagulation time and weaker resistance to heat treatment than high types. Curd firmness at 30 minutes of high type milk is greater than that of low type milk. Contents of total solids, total proteins, casein and phosphorus are higher in high type milk and pH is lower. Longer coagulation time of high type goat milk is due to alpha-s-1-casein delaying curd formation by trapping calcium ions and withdrawing them from the proteolysis of kappa casein. High type has higher cheese yield, better curd firmness, which is associated with lower pH. Despite longer coagulation time, goat milk of the high alpha-s-1 casein type is more suitable for cheese making because of firmer curd, higher casein content, less intense goat flavor and smoother cheese texture, yet it may be that low type has the advantage in human digestion. Beta-casein types also affect cheese making properties of goat milk (Chianese et al., 1993) and alpha-s-1- and beta-casein loci need to be considered together in selection. Sheep's milk also has polymorphisms in its milk proteins, but this research is just beginning.
Amino acid substitutions in milk proteins can also be responsible for flavor and its intensity (Rystad et al., 1990). The amino acid threonine is considered the most important precursor of acetaldehyde, which is the main volatile aroma compound in yogurt. The higher level of glycine in goat milk compared to other species milks may reduce acetaldehyde production from threonine by inhibiting the enzyme threonine aldolase. Ultrafiltration removal of glycine increased acetaldehyde production in goat milk. Addition of threonine resulted in increased acetaldehyde production in goat or cow's milk, but goat milk had less. Goat milk with added threonine had less production of lactic, more pyruvic, acetic and less orotic acids; and there are other amino acid differences between goat and cow's milk (Rystad et al., 1990).
STAGE OF LACTATION
Within species within breed it is the stage of lactation, regardless of species or breed that has the greatest influence on milk composition. Days in milk during lactation regressed on ewe milk component contents had coefficients up to 0.71 (Casoli et al., 1989). Many components in ewe or goat milk as in cow's milk, especially fat and protein, are high in colostrum in early lactation, much lower thereafter until they rise again markedly at the end of lactation, when yields are low (Anifantakis & Kandarakis, 1980). Fat contents in goat milk changed from 2.7 percent in mid-lactation to 4.6 percent during the last week 42 of lactation, protein contents from 3.0 percent to 4.2 percent (Voutsinas et al., 1990). Mineral contents also increased with stage of lactation, Ca from 135 to 150 mg/100 g; P from 99 to 122; Na from 50 to 56; Mg 13 to 15; except K decreased from 170 to 144; and citrate from 145 to 81 mg/100 g.
Between morning and evening milkings on the same day the gross composition of milk may also change (Simos et al., 1991), which again may be confounded with milk yield levels, when the milking interval between evening and morning milking has more or less hours than between morning and evening milking. Fat contents of evening goat milk averaged 5.1 percent after 14 hours of milking interval, morning milk 5.3 percent after 10 hours, total protein contents were 3.54 percent versus 3.58 percent, and total solids were 13.94 percent versus 14.30 percent, respectively. In studies with milking intervals of 8 and 16 hours the differences were 0.39 percent fat and 0.05 percent protein, respectively (Merin et al., 1988).
There are also clear seasonal differences in milk composition of the major and minor components (Renner, 1982), but they are confounded with climate and diet effects. Winter climate can affect milk yields and composition, and both are negatively correlated. Winter feeding is providing usually different proportions and qualities of grazing, hays, silage and supplements, which influence milk composition considerably. Milk C18:0, C18:1, C18:2, C18:3 fatty acids have been found to increase in summer, while C4 to C16 fatty acids were reduced significantly. The seasonally limited production of ewe and goat milk has stimulated interest in overcoming this handicap by various means, including hormonal induction of lactation (Alifakiotis et al., 1980). Normal milk contents of fat, lactose, chloride, total solids, acidity and pH have been obtained.
Differences due to parity, number of lactation or age of animal can be significant in gross milk composition, but this is also confounded with milk yield levels (Casoli et al., 1989). Average fat contents of ewe milk changed linearly from 1st to 6th parity from 6.8 percent to 7.4 percent and total protein contents from 5.8 percent to 6.2 percent for the Massese breed in Italy. Parity seems to have little effect on contents of amino acids, fatty acids or minerals (Casoli et al., 1989).
TYPE OF DIET AND PHYSIOLOGICAL STATUS
Regardless of genetics, the composition of the daily diet and its amount in relation to production requirements can cause significant changes in milk composition (Moran-Fehr, 1981; Haenlein, 1995). In general terms, 3 percent of bodyweight is a minimum requirement of daily dry matter intake for most goats, but high producers will need at least 5 percent. In order to cover nutrient needs of high production, the energy and protein density of the daily feed intake must increase, because of the limitation of the rumen in volume capacity. Roughages like grass, hay or silages are mostly low in energy and protein density because of high fiber and/or water contents. Starchy supplements like cereal grains or fats and fatty seeds from sunflowers or roasted soybeans increase the energy density of the daily diet, and oil meals increase the protein density. Goats and ewe like other ruminants require a daily minimum of long fiber in the diet to prevent acidotic rumen conditions, which lead to fatal parakeratosis and enterotoxemia, or at least to laminitis, significantly depressed milk fat contents, but also possibly increased milk protein contents (Merin et al., 1988).
A more intensive feeding system can be appropriately devised with a complete diet of hay, silage and concentrates mixed together loose (TMR, Total Mixed Ration) or in a pelleted or cubed form (Cavani et al., 1991). This causes usually higher milk yields, changes in milk fat and protein contents and also different cheese making properties.
Energy shortage in the diet can change the fatty acid composition of milk fat towards more medium-chain fatty acids, while daily milk yield may decrease and fat content increase (Moran-Fehr, 1981). When grain concentrate supplementation makes up more than 50 percent of the daily dry matter intake by goats, decreased chewing, less rumination and a shortage of salivation of rumen contents occurs (Kawas et al., 1991). To prevent a decreased rumen pH, the feeding of buffers like sodium bicarbonate and magnesium oxide is beneficial. This has been shown in several studies, where yields were even increased while restoring milk fat contents to normal levels (Hadjipanayiotou, 1988). Increasing energy density by adding fat within narrow limits to the diet, can increase yield of milk, fat, total protein and casein contents (Moran-Fehr, 1981). Also the type of protein in the diet and its rumen degradability can affect milk yield, contents of fat, protein, and processing properties (Andrighetto & Bailoni, 1994).
Nutritional physiology and endocrine status of the animal affects milk yield and composition over short or longer time periods. This has been demonstrated for the effect of estrogens during estrus (Haenlein & Krauss, 1974). Somatotropin also will increase milk yield, milk fat content, short-chain and medium-chain fatty acids significantly, while decreasing milk protein percentage, long-chain fatty acids and net energy balance (Disenhaus et al., 1995).
A widely accepted rapid monitor of udder health is the somatic cell count in milk. However, milk secretion in goats is apocrine, while in cows it is merocrine, which explains why goat milk may have very high counts of somatic cells, especially in late lactation milk or in the last strippings of milk, without any relationship to mastitis (Park & Humphrey, 1986; Haenlein, 1993). In cow's milk it has been demonstrated that the relative and absolute casein content is related negatively to somatic cell counts (Haenlein, 1974). Generally, subclinical or clinical mastitic infections cause the milk contents of casein, lactose and cheese yields to decrease, milk serum albumin, immunoglobulins and salt (NaCl) contents to increase.
Even before cheese precipitation from milk and the effects of fermenting of cheese, the various methods of processing, heating and freezing can have profound influences on milk composition. Heating is applied during pasteurization, UHT processing, condensing and powder production, which will denature milk proteins to varying degrees and affect flavors (O'Connor, 1994). Freezing is of economic interest because of the seasonal nature of goat and ewe milk production, and because these milks have greater economic importance than cow's milk in some countries (Kalantzopoulos, 1994) (Table 1, 2, 4). During frozen storage, oxidation of ewe milk occurred and free fatty acid contents increased because milk lipase was not completely inactivated (Anifantakis et al., 1980). Proteins and bacterial counts may remain stable, and taste and flavor scores do not change. In freezing of cheeses the pH and proteolysis may change (Fontecha et al., 1994). Fermentation during yogurt processing and cheese ripening also causes significant changes in the composition of the products due to proteolysis, lipolysis, glycolysis, development of flavor compounds and liberation of non-protein N-compounds, free amino acids, free fatty acids and ammonia as extensively documented by Anifantakis (1991) (Table 8).
COMPARATIVE NUTRITIONAL ADEQUACY
When milk is consumed as it becomes available from the animal or if its composition is changed in production and processing, a principal question in the pediatric and popular literature is how adequate is that milk for infant or general human needs (Schrander et al., 1993; Andersson & Draussin, 1993; O'Connor, 1994). It must be understood that in general:
(1) milk is the main and hard-to-replace source of dietary Ca in human nutrition regardless of whether it is from ewes, goats or cows;
(2) milk was never meant to be an adequate source of some minerals like Fe or vitamins like C, B12, or folate, which are routinely and cheaply supplemented to daily infant diets from other sources anyway.
With that understanding, milk from ewes or goats can meet at least as well or better significant portions of the daily nutrient requirements of humans (Mack, 1953; Desjeux, 1993) (Table 9). A typical serving size of milk is 1 cup with 245 ml content, which is used as a standard in the USA for comparison of nutrient intake (Gebhardt & Matthews, 1991; NRC, 1968). The minimum daily requirements of 800 mg calcium, not considering the higher needs of pregnant and lactating women or adolescents, are barely met by 3 cups of cow's milk, while goat milk covers this amply and of ewe milk only 2 cups would be required. The same is true for meeting the needs of essential amino acids, except for methionine, phenylalanine, magnesium, thiamine and niacin, as far as requirements are known. Of course, equivalent amounts of yogurt or cheese can be substituted for meeting nutrient needs with milk.
UNIQUE NUTRITIONAL VALUES
Beyond meeting daily nutrient requirements, it is of special interest that goat and ewe milks have unique properties, which distinguish them from cow's milk and make them a valuable alternative not just for infants but also for adults and especially nursing mothers (Baldo, 1984; Host et al., 1988; Razafindrakoto et al., 1993) (Figure 1). Growing interest in goat milk has produced some publications, which document unique nutritional values of goat milk compared to cow's milk (Mack, 1953; Kosikowski, 1985; Haenlein, 1992). Similar research about ewe milk properties is still needed (Steinkamp, 1995). The high solids content of ewe milk enables production of superior yogurt compared to cow's and most goat milks. In order to produce acceptable yogurt viscosity from cow's milk, firming agents or as much as 5 percent skim milk powder are usually added, which however can increase greatly the lactose content of yogurt to undesirable levels in view of today's' consumers' concern with lactose intolerance (Kosikowski, 1985).
The incidence of cow's milk allergy has been found to be about 8 percent or even more in 1-year old infants (Host et al., 1988), but goat milk can be a successful treatment in most cases of direct or indirect cow milk allergy (Walker, 1964; Brenneman, 1978; Grezesiak, 1989). Goat milk fed to undernourished infants or children with digestive malnutrition has been found to be at least equal or even a superior substitute to cow's milk (Hachelaf et al., 1993; Razafindrakoto et al., 1993) (Figure 1).
A well-known difference for goat milk is the predominantly smaller size fat globule compared to cow's milk, which has been credited with easier digestion (Fevrier et al., 1993). Less well appreciated is the qualitative and quantitative difference in milk proteins of cow's versus goat milk, especially alpha-s-1-casein in goat milk with its softer curd formation compared to cow's milk (Ambrosoli et al., 1988). This may be the reason, why the popular literature is full of reports of benefits derived from better digestion of goat milk compared to cow's milk.
An especially interesting difference of ewe and goat milks compared to cow's milk is in their basic milk fat composition (Posati & Orr, 1976; Babayan, 1981) (Table 5). Goat and ewe milk exceed cow's milk significantly in most short, medium chain, mono-unsaturated, poly-unsaturated and essential fatty acids (Table 5 and 6), which are valuable to today's health conscious consumer. Medium chain fatty acids (MCT) (C6 to C14), in particular have different human metabolic properties than long chain fatty acids. MCT, especially caprylic (C8:0) and capric (C10:0) have become accepted treatment for patients with malabsorption symptoms, a variety of metabolic disorders, cholesterol problems and infant malnutrition, because of their unique roles of providing energy to the human metabolism instead of lipids to adipose tissues, and because of their ability to limit and dissolve serum cholesterol (Kalser, 1971; Tantibhedhyangkul & Hashim, 1978). The contents of essential fatty acids also differ in ewe and goat milks compared to human milk, which could be of significance to nursing infants (Wright & Bolton, 1989; Jackson & Gibson, 1989) (Table 5, 6, 9). It has been found that mothers of infants with atopic eczema had an abnormal composition in their milk fatty acid profiles, especially concerning linolenic acid (C18:3). Also it has been found that commercial milk formulae do not contain sufficient amounts of long-chain polyunsaturated fatty acids to cover the requirements of nursing infants. It can be predicted that the commercial natural foods and food supplements industry is soon focusing its efforts on the role of different fatty acids in human nutrition, and the goat and ewe milk industry may be well advised to join this market opportunity.
The composition of ewe and goat milk in relation to human needs and in comparison to cow's milk needs much more research in order to document their unique values, to justify their existence and the higher cost of producing these milks compared to cow's milk (Kosikowski, 1985; Steinkamp, 1995). Besides the differences in milk proteins, which have commercial importance in cheese making and medical significance in digestion and allergies, the considerable differences in milk lipid composition have not been studied much in relation to human nutrition. Therefore, goat or ewe butter, ghee and related products, with their enriched concentration of MCT and other fatty acids, have considerable market potential (Hachelaf et al., 1993), and their unique roles in nutrition and medicine should be a thankful area for researchers to explore (Haenlein, 1992). To further establish the uniqueness of ewe and goat milks will go far in strengthening the small yet ancient dairy sheep and dairy goat industry not only in the Mediterranean countries but around the world.
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(1) Includes all milk from cows, buffaloes, ewes and goats.
(1) Includes all milk from cows, buffaloes, ewes and goats.
(1) Includes all milk from cows, buffaloes, ewes and goats.
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