Consequences of Nutritional Excesses and Deficiencies in Developmental Orthopedic Diseases and/or Osteoarticular Diseases

2. Consequences of Nutritional Excesses and Deficiencies in Developmental Orthopedic Diseases and/or Osteoarticular Diseases

Although most osteoarticular diseases are multi-factorial, the pathophysiology of each disease appears to be influenced by nutrition (Table 2). Excesses of energy and/or calcium contribute to hip dysplasia, elbow dysplasia and osteochondrosis.

Malnutrition during Growth

Slight underfeeding, with respect to energy intake, may slow the growth of puppies but will not influence the adult size of the dog. After a period of inhibited growth due to malnutrition or illness of short duration, the animal will grow at a greater rate than average for its age.

Overnutrition during Growth

In young animals, unlike adults, excessive energy intake does not cause a substantial increase in fat deposition, but rather, a more rapid rate of growth. As long as there is an adequate protein and essential fatty acid supply, it does not appear to matter for growing dogs if the proportion of energy comes from carbohydrate, fat or protein. If the diet supplies sufficient amounts of specific nutrients, the amount of energy will regulate the rate of growth within the genetic possibilities (Grøndalen & Hedhammar, 1982).

Pathophysiological Consequences of Excessive Energy Intake

Puppies should not be fed to achieve maximum weight gain as this will reduce the period of growth. Overnutrition in growing puppies causes a more rapid growth in bone length and a more rapid gain in body weight, when compared with normal or restricted feeding (Riser & Shirer, 1964; Hedhammar et al., 1974; Kasstrom, 1975; Tvedten et al., 1977; Lavelle, 1989; Meyer & Zentek, 1991; Kealy et al., 1992). Heavy body weight will overload the juvenile skeleton and its support system. This may contribute to the development of a variety of multi-factorial diseases in ad libitum fed dogs including osteochondrosis (Hedhammar et al., 1974; Lavelle, 1989), hip dysplasia (Hedhammar et al., 1974; Kasstrom, 1975) and fragmentation and fissures of the coronoid process (Grondalen & Hedhammar, 1982) (Figure 2).

Rottweiler puppies with an abnormal stance due to carpal laxity. During the period of fast growth, mostly between 1 - 3 months of age, dogs may reveal abnormal angulation of the carpal joint, probably due to a discrepancy between the increase in body weight and the carpal support. Bandaging for 10 days will allow the carpus to gain strength and restore the normal posture of the dog. (© HAW Hazewinkel).

High growth rates have been observed in young dogs that are:

• Bitch-fed puppies versus hand-reared puppies
• Receiving ad libitum palatable commercial food versus meal-restricted energy intake
• Fed unrestricted energy enriched diets versus time-restricted food intake.

Figure 2. Evolution of osteoarticular complaints related to the over-consumption of energy. The rate of growth is directly influenced by the energy supply. Surplus energy consumption accelerates the attainment of adult weight. The resulting overload on the still immature joints increases the risk of osteoarticular pathology.

Not all these studies specifically researched hip joint development or status, but in those where this was the case, a detrimental effect from overnutrition was observed (Riser & Shirer, 1964; Hedhammar et al., 1974; Kasstrom, 1975; Lavelle, 1989; Kealy et al., 1992).

Clinical Consequences of Excessive Energy Intake in Large Breed Puppies

The original study (Hedhammer et al., 1974) was performed on 12 pairs of Great Danes raised on food rich in protein, calcium, phosphorus and energy. Skeletal diseases including osteochondrosis and delayed skeletal modeling were observed more frequently in the dogs fed ad libitum, whereas the dogs that received restricted feeding (i.e., 2/3 of the amount of the ad lib group) showed less severe signs.

In a controlled study of Great Danes with high food intake of more balanced commercial foods, the ad libitum fed dogs revealed more frequent osteochondrosis of the shoulder compared to the dogs fed 60% of the ad libitum amount (Lavelle, 1989).

Another study showed overload of the skeleton in puppies by either overnutrition through feeding a basal food enriched with rice ad libitum or by stimulating high body weight through the use of sand belts in the scapular region (Meyer & Zentek, 1991). After 6 months, both the ad libitum fed dogs and the load bearing dogs had skeletal problems. This highlights the adverse effects of excess weight during growth of large breed puppies (Figure 2).

A study, unique in its design and long term follow up has been published by Kealy et al., (1992), in which 48 Labrador Retrievers, originating from seven different litters, were divided into two groups at the age of eight weeks. Dogs of one group were allowed to eat a dry dog food ad libitum, whereas sex-matched littermates received 75% of the amount of food consumed by littermates. The pair mates were both housed in the same indoor cage with an outdoor run to standardize other environmental influences, except for 15 minutes during feeding. Other reports, in comparable studies, found that restricted-fed dogs approach the body weight and size of ad libitum fed dogs after 6 months of age (Hedhammar et al., 1974; Lavelle, 1989).

The restricted fed Labrador puppies in Kealy's study had an average body weight of approximately 20 kg, being 78.3 ± 5.35% (mean ± SD) of that of the ad libitum fed pair mates, at the age of 30 weeks. The difference in mean body weight of the 2 groups was even more apparent at the age of 2 years.

Growth and Proteins

The assumption that a high protein content might be harmful for large-breed puppies is wrong. There is no scientific evidence supporting an undesirable effect of proteins for growth and especially, ossification (Nap et al., 1991). On the contrary, a rather high protein content in the diet helps to reinforce the palatability and to restrict the fat content without including a high level of carbohydrates.

The quality of dietary proteins has to be excellent. The quantity to include in the diet depends obviously on their biological value and on the digestibility of protein sources. Generally, the protein-caloric ratio should be higher in a puppy-diet compared to an adult dog diet.

At 30 weeks of age, measurement of the Norberg angle on radiographs of all dogs revealed statistically significant differences (p<.0.05) in joint laxity. These differences were still significant at 2 years of age (Kealy et al., 1992). This long term study with 24 pairs of littermates, raised under the same environmental conditions, demonstrates a considerably higher incidence of HD in the group of overfed dogs when compared with the group fed 25% less.

In Labrador puppies, an appropriate diet during growth helps limit weight gain in the adult dog. (© Renner).

Influence of the Protein Content of the Diet

Since a high protein diet (30% DMB) did not increase the frequency or severity of skeletal abnormalities in giant breed dogs (as compared with control dogs fed isoenergetic diets) (Nap et al., 1993b), it may be concluded that it is excess body weight during rapid growth, rather than the high protein content of diet, that can be deleterious for skeletal development. In this study, performed in Great Danes, no differences in occurrence or severity of osteochondrosis occurred when compared with the normal or low protein fed dogs (Nap et al., 1991).

Overnutrition in Adults

In most Western countries, the major nutrition-related clinical problems in canine orthopedics are due to excessive energy intake which will be stored as body fat in the normal dog. Obesity is a common disease and the prevalence in dogs is approximately 28 - 44% (Edney & Smith, 1986). Osteoarticular disorders are often associated with obesity. It is not clear if the high body weight precedes orthopedic problems including osteoarthrosis, herniated intervertebral disc disease and cruciate ligament rupture. The mechanical effect of increased body weight might cause a shear or tear of stabilizing structures and an overload of the articular cartilage.

There have been a few studies investigating the relationship between ad libitum fed vs restricted fed dogs and osteoarthritis (OA). In two groups of Labradors, litter mates of the same gender were pair fed, i.e., one group ad libitum, the other 75% of the ad libitum amount. Housing, food and maintenance were the same, except for the amount of food and as a consequence the body weight which was an average 32 kg for the ad libitum dogs and 23 kg for the restricted fed dogs. At 5 years of age, 12 of 23 of the ad libitum fed dogs and 3 of 23 of the restricted fed dogs had OA of the hip joints. By 8 years of age, 12 of 23 of the ad libitum fed dogs and 2 of 23 of the restricted fed dogs had OA in multiple joints (Kealy et al., 1997; Kealy et al., 2000; Smith et al., 2001). OA in multiple joints (including hips, elbows and shoulders) was seen more frequently in overweight dogs than in slim litter mates (Kealy et al., 1997).

The pathophysiology behind the high incidence of OA in over-weight dogs can be mechanical, but also hormonal as a decreased growth hormone level was demonstrated in these overweight dogs (Hazewinkel et al., 1999).

Insufficient Calcium Intake

Young animals have a high requirement for calcium to mineralize newly formed cartilage and osteoid. In Great Danes the daily calcium deposited in the skeleton can be as high as 225 - 900 mg calcium/kg body weight (Hazewinkel et al., 1991). During growth, the calcium requirement largely depends on the stage of growth (i.e., the age of the puppy) and its growth rate (i.e., the expected adult size and weight).

In miniature Poodles, 3.3 g calcium per kg diet (DMB) [corresponding to 140 mg per kg BW per day] did not cause any skeletal abnormalities. In comparison, Great Dane puppies receiving 5.5 g calcium per kg diet (DMB) [150 - 250 mg per kg BW per day] in the same research setting, with the research diet right after weaning, developed severe osteoporosis with pathological fractures (Hazewinkel et al., 1985; Nap et al., 1993) with a growth rate exceeding that of the control puppies fed with a diet containing 11 g calcium per kg diet (DMB) [300 - 500 mg per kg BW per day] (Figure 3).

Excess Calcium Intake

Clinical Observations (Figure 3)

The series of studies in Great Danes have demonstrated that daily food intake of calcium rich diets lead to hyperplasia of calcitonin (CT) producing cells, reduced osteoclastic activity and disturbed endochondral ossification (Nunez et al., 1974; Hazewinkel et al., 1985). A decreased remodeling of the proximal femur (i.e., a delayed antetorsion) was observed in a group of Great Danes, a breed not particularly prone to HD, fed an ad libitum diet rich in calcium (Hedhammar et al., 1974).

Figure 3. Nutritional research in large-breed puppies concerning the optimum calcium content of food. (From Hedhammar et al., 1974; Lavelle et al., 1989; Hazewinkel et al., 1985 & 1991; Kealy et al., 1992; Schoenmakers et al., 2000; Weber et al., 2000). Different research groups have investigated the influence of nutrition on the manifestation of skeletal disease in large and giant breed puppies. These graphs (Royal Canin, 2004), account for the quantity of calcium and energy ingested by puppies at 2 and 5 months in the different studies. Several studies show that high calcium consumption can have deleterious effects on the skeleton, particularly in large breed dogs.

Others described delayed skeletal maturation in both Great Danes and in Poodles fed a diet with high calcium content (i.e., 3.3% calcium on a dry matter basis) when compared with controls fed a diet according to NRC (1974) guidelines (Voorhout & Hazewinkel, 1987a; Nap et al., 1993a).

Great Danes raised on diets with an increased calcium and phosphorus level (3.3 and 3.0% respectively [i.e., 1240 mg calcium per kg BW per day], in comparison with controls on 1.1% and 0.9% respectively [i.e., 400 mg calcium per kg BW per day]) starting at the age of weaning, developed disturbances in endochondral ossification in the growth plates of the distal radius or ulna. As a consequence, elbow incongruity developed either due to a severe disturbance of growth in length of the radius, or due to a severe radius curvus syndrome with disturbed growth in the length of the ulna (Hazewinkel et al., 1985; Schoenmakers et al., 2000). The latter may coincide with an ununited anconeal process or the painful distraction cubiti, and will all lead to OA of the elbow joint.

In another study, Great Danes fed diets differing only in calcium content, the higher calcium diet group showed progressively more severe disturbances of osteochondrosis in the proximal humerus as well as in growth plates of long bones and of non-weight bearing (i.e., ribs) areas (Hazewinkel et al., 1985).

Osteochondrosis of the proximal humerus.

1. Scapula
2. Humerus
3. Humeral head
4. Cartilage
5. Cartilage flap

Weber et al. (2002) found no abnormalities when starting a diet at 2 months of age in Great Dane dogs with a calcium content of 1.5 g per kg diet [i.e., 830 mg per kg BW per day].

Pathophysiology of Excess Calcium

In young dogs, calcium (Ca) is absorbed in the intestine by means of both uncontrolled passive diffusion and active, controlled absorption. Puppies less than 6 months of age are unable to protect themselves from an excess of calcium (Tryfonidou et al., 2002b); during weaning at least 50% of the calcium is absorbed whatever the quantity ingested (Hazewinkel et al., 1991) (Figure 4). Great Danes raised on a food according to the NRC (1974) recommended 11 g calcium per kg diet (DMB) [0.5 g per kg BW per day] absorbed 45 - 60% (260 - 300 mg/kg/d) of the ingested amount of Ca, whereas puppies with triple that amount of in their diet, absorbed 23 - 43% (115 - 215 mg/kg/d). Thus puppies fed the high calcium diet absorbed considerably higher amounts of calcium.

Figure 4. Fraction of calcium absorbed passively or actively according to the level of calcium consumed (in 3-month-old Puppies of Various Breeds). (From Tryfonidou et al., 2002).

Intake of food, and especially of Ca, causes the release of gastrointestinal hormones, some of which will cause calcitonin (CT) release from the thyroid glands. In the growing animal, chronic high calcium intake will cause chronic hypercalcitoninism (Hedhammar et al., 1974; Hazewinkel et al., 1985) which prevents calcium release from the skeleton by decreasing bone resorbing osteoclastic activity. Remodeling of the skeleton cannot occur. The calcium absorbed will be routed to the skeleton without influencing the concentration of calcium in the extracellular fluid at each meal.

Although it is not fully understood if calcium plays a direct role in disturbing chondrocyte maturation, or if it is mediated by CT and/or a relative deficiency of other minerals at a cellular level, there is little doubt on the deleterious effect of high calcium intake on endochondral ossification, with osteochondrosis as a consequence.

The recommended calcium allowance for a growing puppy according to NRC 2006 is 3.0 grams of calcium/ 1000 kcal Metabolizable Energy (ME) or 0.5 g of calcium/ kg of body weight/ day. The NRC 2006 minimum calcium requirement for growing puppies is 2 g/1000 kcal or 0.37 g of calcium / kg body weight / day. This should be appropriate for all breeds and sizes. Compilation of the previously mentioned studies suggests that there is a safety zone for calcium intake at which osteoarticular diseases do not develop. This safety zone would be 260 - 830 mg of calcium/ kg / day for puppies at 2 months of age. The range would narrow slightly at 5 months of age to 210 - 540 mg of calcium /kg/ day (Weber et al., 2000; Royal Canin, 2004) (Figure 5).

Figure 5. Synopsis of studies that have helped to determine the optimal calcium recommendation for a 2 month old puppy. (Hazewinkel et al., 1985-1991; Shoenmakers et al., 2000; Weber et al., 2000). There is no ideal calcium content relative to age, but there is a safety zone. To feed a 2 month-old large-breed puppy as safely as possible, it is advisable to give it between 260 and 830 mg of calcium/kg/day. At 5 months, the calcium safety zone should be lowered: between 210 and 540 mg of calcium/kg/day.

Calcium Metabolism and Skeletal Development in Young Dogs

1. In adult dogs and puppies calcium absorption takes place not only via an active mechanism, but also via a process of passive diffusion (Figure 6), dependent on the concentration gradient. In puppies, passive absorption is however more important than in the adult dog, where it is a minor phenomenon. As a consequence, there is higher calcium absorption from higher biologically available calcium diets, both in small and large breed dogs.
2. Even calcium excess at the time of partial weaning (i.e., from 3 - 6 weeks of age) causes hypertrophy of the calcitonin producing cells with consequences in later life. All large breed dogs with higher calcium intakes as weaning puppies developed enostosis at the age of 3 - 4 months.
3. Excess calcium as well as excess calcium and phosphorous, starting at the age of weaning (6 weeks of age) caused severe signs of osteochondrosis as well as radius curvus syndrome in large breed dogs.
4. Excess calcium starting at 3 weeks of age caused hypercalcemia, hypophosphatemia, and very low concentrations of parathyroid hormone. The skeleton revealed signs of hypophosphatemic rickets, i.e., widened growth plates and thin cortices.
5. Calcium deficiency occurs sooner in large than in small breed dogs: 0.55% Ca [i.e., 250 mg Ca per kg BW per day] DMB caused nutritional secondary hyperparathyroidism (NSHP) in 2 months-old Great Dane puppies but not in Miniature Poodles fed at 0.33% [i.e., 170 mg Ca per kg BW per day] Ca DMB. NSHP in Poodles was seen under 0.05% Ca [i.e., less than 25 mg Ca per kg BW per day] DMB.
6. In calcium deficiency, the proportion of inges-ted calcium which is actively absorbed versus passively diffused increases, although the total amount of calcium which is absorbed may still be less than required. In order to keep plasma calcium concentration constant, osteoclasts start to remove bone. Chronic calcium deficiency causes NSHP with severe calcium resorption of the skeleton and eventually pathological fractures (i.e., greenstick and compression fractures).
7. Vitamin D deficiency, even with adequate dietary content of calcium and phosphorus, leads to rickets.
8. Excessive vitamin D intake does not lead immediately to increased calcium absorption due to metabolic adaptations of vitamin D in the body, but it may cause osteochondrosis and radius curvus syndrome in young dogs of large breeds.

Figure 6a. Linear absorption of calcium. (From Tryfonidou & coll, 2002).

Influence of Two Levels of Calcium on Growth and Skeleton Development in Large-breed Puppies

Osteoarticular diseases are particularly common in large-breed and giant-breed puppies. Calcium excess (3.3%) and deficiency (0.55%) have in turn been incriminated as factors promoting skeletal developmental problems. The object of this study was to evaluate the influence of these two calcium levels, by remaining within the regular calcium-value range in puppy food.

Six Great Dane bitches (GD) and six giant Schnauzers (GS) were split into two groups (3GDs + 3 GSs) from the age of 9 weeks. These two groups were raised on two foods composed of the same ingredients (C08 and C15); the only difference was the calcium (0.8% vs 1.5%) and phosphorus (0.6% vs 1.23%) content in C08 and C15 respectively (identical metabolizable energy (ME) value: 3800 kcal/kg).

Between 10 and 40 - 46 weeks parameters including body weight, height to withers, length of ulna and tibia, serum calcium and phosphate concentrations, alkaline phosphate levels and IGF-1 were measured.

Figure 6b. Male great dane at different stages of growth. The bones grow primarily during the first few months. The second phase corresponds to muscular development, which continues until adult weight has been reached.

Skeletal radiographs and orthopedic examinations were also conducted regularly to evaluate the position of the legs and the conformation and to identify any lameness.

Energy ingested was identical for all the dogs. Energy intake increased gradually from 1400 kcal ME/day in week 10 to 3500 kcal ME/day in week 46 for the GDs versus 610 - 1800 kcal ME/day for the GSs. The calcium consumption was respectively 400 and 200 - 250 mg/kg/day in the puppies that receive the C15 and C08 diet.

No difference was observed in bodyweight or body condition between the two groups of puppies. Within the two breeds the differences in tibia and ulna length according to dietary group, were not significant. There was no significant difference between the groups with respect to the size of the GDs (from 40 cm in wk 10 to 77 cm in wk 46), or in the GSs (from 33 cm to 58 cm in wk 46).

The serum calcium, phosphate, alkaline phosphate, and IGF-1 values did not vary between the groups. In the GDs the median IGF-1 value during the study ranged between 254±61 and 406±40 ng/mL, while in the GSs these values ranged between 92±43 and 417±82 ng/mL.

No particular health problems were revealed. Orthopedic examinations did not provide any evidence of clinical difference between the dogs. No painful areas or biomechanical problems were detected. Mild osteochondrosis lesions were transiently shown in the two groups.

This study concluded that there were no skeletal developmental abnormalities detected in giant-breed puppies when they consumed a diet containing 0.8% or 1.5% calcium.

Weber M, Martin L, Dumon H et al. Calcium in large breed growing dogs: a safety range? 4th Conference of the European Society of Veterinary and Comparative Nutrition. April 2000; Amsterdam, The Netherlands.