being associated with high concentrations of each mineral. Added calcium also reduces the efficiency of phytase additions to pig rations (Lei et al., 1994).
The control of phosphorus metabolism is necessarily quite different from that of calcium. Provided that phosphorus is present in absorbable forms in the diet, it is, like other anions, extensively absorbed, even when supplied well in excess of need, and absorption from milk is almost complete (Challa and Braithwaite, 1989). The kidney and gut are both routes for the excretion of phosphorus that is surplus to requirement, the gut (by way of saliva) being the major route for excretion in grazing ruminants or those fed roughage diets, whereas the kidney is of greater importance in monogastrics and in ruminants fed diets that promote low salivary flow rates (processed, pelleted or concentrate diets). There is no tight hormonal control of inorganic phosphorus concentrations in the bloodstream and serum values range widely above and below the renal threshold of 2–3 mmol l21 in perfectly healthy animals.
The relationship between absorbed and ingested inorganic phosphorus is linear over wide ranges of intake and the slopes indicate AP of about 0.74 in weaned sheep (Braithwaite, 1986) and 0.83 in weaned calves (Challa et al., 1989). Furthermore, these high levels of AP can be attained with indigestible natural sources, such as straw (Ternouth, 1989) and dry, summer forage (Coates and Ternouth, 1992), though less so with bran (0.63; Field et al., 1984). The PP present in the form of inositol tetra-, penta- and hexa- phosphates in straw and seeds is extensively hydrolysed in the rumen by microbial phytase and phosphate is thus released (Reid et al., 1947; Nelson et al., 1976; Morse et al., 1992). There are marginal but quantitatively important increases in AP in the phosphorus-deficient animal (Scott et al., 1984, 1985;
Coates and Ternouth, 1992) and small decreases at excessive phosphorus intakes (Braithwaite, 1984b; Challa et al., 1989). Phosphorus is absorbed principally from the proximal small intestine (Bown et al., 1989; Yano et al., 1991).
Non-ruminants are dependent on the presence of phytases found either in the grains themselves or in intestinal secretions to utilize phytate phosphorus.
Undegraded phytate can be extensively converted to insoluble mineral–
phytate complexes before the site of phosphorus absorption is reached, thus lowering the amount absorbed. Older animals have a greater ability than younger to digest phytate. Adverse effects of calcium–phytate interactions on the absorption of manganese and zinc have been widely demonstrated (Biehl et al., 1995) and are considered in later chapters.
Ruminants also differ from non-ruminants in that large quantities of phos- phorus are secreted in saliva during the process of rumination and the major source of phosphorus flowing into the rumen is not the diet but the salivary secretions (Tomas et al., 1973). The principal influence on the amount of phosphorus secreted in saliva is the Pi in plasma, the relationship between the two variables being linear over the range 1–3 mmol Pil21 and equivalent to a doubling of salivary phosphorus output in cattle (Challa and Braithwaite, 1988; Challa et al., 1989). Phosphorus does not appear to be reabsorbed by the salivary gland, and parathyroid hormone (PTH) can only increase salivary phosphorus secretion when there is an ample supply (Wright et al., 1984).
The nature of the diet, however, has a major influence. As the roughage content of the diet increases, the partition of initially absorbed phosphorus between salivary secretion and urinary excretion shifts towards the salivary route (AFRC, 1991). The outcome and prediction of phosphorus partitioning in ruminants is of crucial importance in determining the actual or likely incidence of phosphorus deficiency and is still the subject of controversy (Ternouth, 1990; Scott et al., 1995). One problem lies in the difficulty of separating the two important determinants of salivary phosphorus secretion, dry-matter intake (DMI) and phosphorus intake. Without a phosphorus-free diet, the specific effect of DMI is only obtainable with diets of different phosphorus concentration fed at several different intakes. Endogenous faecal losses do increase with DMI in the short term (AFRC, 1991), but, if the diet is deficient in phosphorus, plasma and salivary phosphorus will decline with duration of feeding and FEP will gradually decline (Ternouth, 1989; AFRC, 1991; Coates and Ternouth, 1992) as the major homeostatic adjustment to deficiency. The physical forms of ingested roughage reported on so far do not appear to be important (Ternouth, 1989; Scott et al., 1995), but they did not include long roughage. Yano et al. (1991) cite unpublished data which indicate a doubling of salivary phosphorus flow when the length of hay being fed to sheep was increased from 1 to 6 cm. Because absorptive efficiency for salivary phosphorus is high (70–80%: Challa et al., 1989), the ruminant is able to recycle phosphorus very efficiently via saliva, and diets which stimulate secretion may improve the utilization of dietary phosphorus (Yano et al., 1991).
Some phosphorus is irreversibly lost via the faeces (FEP) by ruminants and the amount depends on the phosphorus concentration in the saliva (Braithwaite, 1984b; Challa et al., 1989), the volume of saliva produced and the precise efficiency of absorption. Since the latter is subject to genetic varia- tion in sheep, marked differences in FEp are found within (Field et al., 1984) and between (Field et al., 1986) breeds of sheep. When phosphorus supply is so inadequate that absorptive efficiency rises beyond the normally high level, there is likely to be an additional conservation of salivary phosphorus by reductions in FEP, which may sometimes be of crucial importance. Despite Salivary phosphorus secretion in ruminants
Faecal and urinary excretion
attempts to conserve phosphorus, FEP becomes the predominant source of faecal phosphorus (70–90%) on diets low in phosphorus. As phosphorus intakes rise, the capacity for faecal endogenous excretion becomes saturated and most of any excess over need is excreted in urine. On pelleted, energy- dense diets, which stimulate little salivary secretion, significant urinary phosphorus excretion may occur at levels of supply which fail to allow complete mineralization of bone. Theoretically, such urinary losses should be allowed for in devising requirements for optimum bone strength (Braithwaite, 1984b). However, such diets are never likely to provide insufficient phos- phorus for ruminants. Obligatory urinary losses of phosphorus are more likely to warrant attention and replacement in non-ruminants.
Another important mechanism for adjusting to inadequate dietary supplies of phosphorus involves the modulation of bone growth and mineralization of the skeleton. As was the case with calcium (see Chapter 4), there are differences between growing and mature animals. Weanling lambs given low-phosphorus diets can continue to increase their skeletal size without requiring more phos- phorus. In Field et al.’s (1975) study with diets low in phosphorus, weight of the fat-free skeleton increased by 19%during a 4-month period, while the phos- phorus content decreased by 11% (Table 4.3 on p. 79). The adjustment involved decreases in the amount of bone matrix in the limb bones and in the degree of matrix mineralization in cancellous bones. There may, however, be major differences between species in the extent to which such an adaptation can sustain growth. In the pig, as in other species, there is a substantial increase in the degree of mineralization of bone after weaning, bone ash con- tent increasing from around 45% to 55% between 15 and 85 kg LW in one study (Fig. 5.1; Reinhart and Mahan, 1986). That increase was seen in groups given diets sufficiently low in phosphorus to retard growth, indicating a higher priority to provide sufficient phosphorus to mineralize bone. Presumably, it is impossible for species with such high relative growth rates to find sufficient additional phosphorus by redistributing the pool of phosphorus in the skele- ton; instead, pigs deprived of phosphorus restrict growth. To describe bone mineralization in the pig as a ‘sensitive criterion’ of phosphorus status (Koch and Mahan, 1985) is somewhat misleading in such circumstances. The rela- tionship between growth and bone mineralization for a given species may be partly determined by serum Pi. Data from Reinhart and Mahan (1986) show clear relationships between growth rate and serum Piat each growth phase in the pig (Fig. 5.2), and the optimum serum Pi is over 2.5 mmol l21, a higher value than that which is considered optimal for growth in the lamb. The chick also shows a linear relationship between bone ash and serum Pi, up to values of around 2.5 mmol l21(Mohammed et al., 1991).
In mature animals of all species, the quiescent remodelling process can be awakened to allow the net withdrawal of substantial amounts of phosphorus,
Bone growth and mineralization in the young
Bone mineralization in the adult
and mobilization of stored phosphorus becomes more important than dietary phosphorus intake in determining animal health and production. It can be calculated that lactating cows and ewes need to mobilize only 0.7% of their skeletal reserves each day to sustain peak daily milk phosphorus outputs (Suttle, 1987). There are three distinctive features as far as phosphorus is concerned: firstly, the process does not appear to be under the same hormonal control as calcium, since PTH concentrations fall during phos- phorus deficiency (Somerville et al., 1985); secondly, bone resorption provides too little phosphorus relative to calcium (Ca) for milk production, since the Ca : P ratio in milk is only 1.3 : 1, as opposed to 2 : 1 in bone; and, thirdly, the utilization of stores is less efficient than for calcium, because more of the mobilized mineral will be lost via the faeces, despite the eventual decline in plasma phosphorus, salivary secretion and FEP.
It is arguable whether there is any specific and effective hormonal regulation of phosphorus metabolism. While PTH secretion improves the renal tubular reabsorption of phosphorus, the hypercalcaemia which usually accompanies phosphorus deficiency inhibits PTH secretion. While administration of vitamin D or its analogues often improves phosphorus absorption and reten- tion in pigs (Pointillart et al., 1986; Lei et al., 1994) and poultry (Mohammed et al., 1991; Biehl et al., 1995), such effects may be secondary to those on calcium, for two reasons: firstly, any improvement in calcium absorption Fig. 5.1. The effects of dietary P and age on the mineralization of limb bones in young pigs: note the large increases in bone ash from the starter to the finisher stage,
regardless of whether diets low (open symbol, 0.5, 0.4 and 0.3 g P kg21DM) or high in phosphorus (closed symbol, 0.7, 0.6 and 0.5 g P kg21DM for successive stages) were fed (data from Reinhart and Mahan, 1986).
Hormonal regulation
lessens opportunities for calcium to form unabsorbable phytates in the gut;
and, secondly, any improvement in retention of calcium in the skeleton must be accompanied by retention of phosphorus. There are differences between species in endocrine responses to phosphorus depletion. Increases in renal 1a-hydroxylase activity and plasma 1,25-(OH)2D3 have been reported in the phosphorus-depleted pig and chick (for review, see Littledike and Goff, 1987), but there is no such response in sheep (Breves et al., 1985). One possible explanation for a lesser role of vitamin D in regulating phosphorus Fig. 5.2. Relationship between serum inorganic phosphorus (Pi), growth and appetite in growing pigs: note that feed intake reaches a plateau before growth rate as Pirises, suggesting a specific effect of phosphorus deprivation on growth (data from Reinhart and Mahan, 1986); open circle, low P; closed circle, high P; dietary Ca varies.
metabolism in ruminants is that phytate does not present an obstacle to phosphorus absorption; another is the greater reliance which ruminants can place on skeletal sources of phosphorus. Increases in intestinal calbindin can occur in the phosphorus-depleted pig without changes in the circulatory levels of 1,25-(OH)2D3 (Pointillart et al., 1989), and any influence of vitamin D on phosphorus metabolism may again be secondary to that on calcium.
The remarkable demineralization of the skeleton induced by parasitic nematode infections of the sheep’s gut was outlined in Chapter 4; here, the specific effects on phosphorus metabolism will be dealt with. Infections of the small intestine (e.g. by Trichostrongylus colubriformis) can reduce the absorption of dietary and endogenous phosphorus by about 40% and induce hypophosphataemia, but infections of the abomasum (e.g. by Ostertagia circumcincta) have little or no effect (Wilson and Field, 1983). Combined infections have similar phosphorus-depleting effects, which last up to 17 weeks (Fig. 5.3; Bown et al., 1989). Although food intake was reduced by 60%, this alone did not induce phosphorus deficiency, because the ryegrass/
clover diet contained a respectable 3.3 g P kg21 DM and was sufficient to maintain normal plasma phosphorus levels in pair-fed controls. While the sustained, dual infectious challenge was severe (generally 12,000 infectious larvae kg21 herbage DM) in comparison with conditions commonly encountered on intensively grazed temperate pastures, it is likely that seasonal nematode infections often increase phosphorus requirements and may reduce the capacity to withstand later seasonal shortages in dietary phosphorus supply (Suttle, 1994).
Gut parasites as phosphorus antagonists
Fig. 5.3. Effects of prolonged dual infection of the abomasum and small intestine by parasitic nematodes on plasma inorganic phosphorus (Pi) concentrations in lambs (Bown et al., 1989).
Phosphorus is the second most abundant mineral in the animal body and about 80% is found in the bones and teeth. As with calcium, the formation and maintenance of bone are quantitatively the most important function, and the changes in bone structure and composition that result from phosphorus deprivation are in most respects the same as those described for calcium deprivation in Chapter 4. Phosphorus, however, is required for the formation of the organic bone matrix as well as the mineralization of that matrix. The 20% of phosphorus not present in the skeletal tissues is widely distributed in the fluids and soft tissues of the body, where it serves a range of essential functions. Phosphorus is a component of deoxy- and ribonucleic acids, which are essential in cell growth and differentiation; as phospholipid, it contributes to cell-membrane fluidity and integrity; as phosphate, it helps to maintain osmotic and acid–base balance; and it plays a vital role in a host of metabolic functions, including energy utilization and transfer via AMP, ADP and ATP, with implications for glucogenesis, fatty acid transport, amino acid and protein synthesis and the activity of the sodium/potassium (Na+/K+) pump.
Disturbances of glycolytic metabolism have been noted in the erythrocytes from phosphorus-deficient cattle (Wang et al., 1985). In ruminants, the requirements of the rumen and caecocolonic microflora are also important, and microbial protein synthesis may be impaired on low-phosphorus diets (Petri et al., 1989; Ternouth and Sevilla, 1990b). Phosphorus is further involved in the control of appetite, in a manner not yet fully understood, and in the efficiency of feed utilization (Ternouth, 1990). Phosphorus is arguably the most potent of all the mineral elements.
The clinical sequelae of phosphorus deprivation are accompanied or preceded by biochemical changes in the blood and tissues.
The chemical changes in the bones that precede or accompany the structural changes associated with phosphorus dysfunction are apparent from two early experiments with pigs and sheep. Growing pigs fed for 6 weeks on a synthetic milk diet containing 2.0 g P kg21 had bones which were less well mineralized than those of comparable animals receiving phosphorus- supplemented diets (Table 5.1). In a longer experiment (14–18 months) with growing sheep fed on a moderately phosphorus-deficient diet, the ash concentration of the ribs and vertebrae was some 20% lower and that of the long bones over 8% lower than that of similar bones from sheep supple- mented with phosphate (Stewart, 1934/35). Reductions occur in both the ash and organic-matter content of the bone in phosphorus-deprived pigs (Koch and Mahan, 1985) and lambs (Field et al., 1975), so that ash percentage