Relationship of Nutrition to Developmental Skeletal Disease in Young  Dogs

Daniel C. Richardson

Phillip W. Toll

Developmental skeletal disease is common in large and giant-breed puppies. One manifestation, hip
dysplasia, affects millions of dogs. Genetics, environment, and nutrition all contribute to
developmental skeletal disease. Of the nutritional components, rate of growth, specific nutrients,
food amounts consumed, and feeding methods influence skeletal disease. Excess energy and calcium
are known risk factors; therefore, the level of these nutrients in the food should be near the
Association of American Feed Control Officials minimum requirement. Puppies should be fed a
growth-type food using a food-limiting technique. All puppies should be weighed and evaluated at
least every two weeks. Amounts fed should be increased or decreased based on weight and body
condition score.

Key Words: Developmental skeletal disease, calcium, energy, hip dysplasia, electrolyte balance,
osteochondrosis, body condition, feeding method.

Introduction

The musculoskeletal system changes constantly throughout life. These changes are most rapid during
the first few months of life and slow with skeletal maturity (about 12 months for most breeds). The
skeletal system is most susceptible to physical and metabolic insult during the first 12 months of life
because of the heightened metabolic activity. The physical manifestation of these results can be
lameness and/or altered growth. Both can affect locomotion and/or soundness of adult dogs.

Developmental skeletal disease is a multifactorial process that has genetic, environmental, and
nutritional components. These skeletal abnormalities primarily affect fast growing, large-breed dogs.
Lack of careful genetic monitoring can introduce and propagate disorders (e.g., hip dysplasia,
osteochondrosis) that are difficult to eliminate. Trauma, whether obvious (e.g., hit by a car) or subtle
(e.g., excessive weight) can adversely affect relatively weak growth centers and cause skeletal
disease (e.g., angular limb deformities). Nutrient excesses (e.g., excess calcium supplementation)
often exacerbate musculoskeletal disorders.1-4 This article reviews the role of nutrition in
developmental skeletal disease in young dogs.
 

Nutrition and Skeletal Disease

The role of nutrition in developmental skeletal disease is complex. Rate of growth, specific nutrients,
food consumption, and feeding methods have all been shown to influence skeletal disease. Large and
giant breeds are most susceptible to developmental skeletal disease, presumably because of their
accelerated growth rate.4,5 Dietary deficiencies are rare in young, growing dogs fed commercial
growth foods.6 Problems associated with dietary excess are far more likely, especially if a high
quality growth food is supplemented with minerals, vitamins, and energy.6 The following review
discusses some of the more critical nutrients in developmental skeletal disease.

Energy

The energy needed for any individual depends on breed, age, neuter status, and activity levels. In
general, growing puppies require twice as much dietary energy as adults for body maintenance,
activity, and growth. The need is greatest right after birth and decreases as the dog grows and
matures. Rapid growth in large and giant-breed dogs increases the risk of skeletal disease.4,5
Excessive dietary energy may support a growth rate that is too fast for proper skeletal development
and results in a higher frequency of skeletal abnormalities in large and giant-breed dogs.7 Because
fat has twice the caloric density of protein or carbohydrate, dietary fat is the primary contributor to
excess energy intake.

Excess energy leads to rapid growth. Dietary energy in excess of a puppy's needs will be stored as
body fat. Body condition scoring evaluates body fat stores and therefore correctness of energy
intake. Maintaining appropriate body condition during growth not only avoids excess body fat
storage, but also helps control excess growth rate. Limiting intake to maintain a lean body condition
will not impede a dog's ultimate genetic potential. It will only reduce food intake, fecal production,
obesity, and lessen the risk of skeletal disease.8 Energy or food-dose calculations can only be used
as general guidelines or starting points that must be modified based on frequent clinical evaluation of
each puppy because individual needs can vary widely. (Fig. 1). Physical evaluation or body
condition scoring should be done at least every two weeks (See Evaluation of Feeding Methods and
Scoring to follow).

Protein

Unlike other species, protein excess has not been demonstrated to negatively affect calcium
metabolism or skeletal development in dogs. Protein deficiency, however, has  more impact on the
developing skeleton. In Great Dane puppies, a protein level of 14.6% (dry matter basis) with 13%
of the dietary energy derived from protein can result in significant decreases in bodyweight and
plasma albumin and urea concentrations.9,10 The minimum adequate level of dietary protein
depends on digestibility, amino acids, and their availability from protein sources. A growth food
should contain > 22% protein (dry matter basis) of high biologic value (Table 1).11 The dietary
protein requirements of normal dogs decrease with age.

Calcium

The absolute level of calcium in the diet, rather than an imbalance in the calcium/phosphorus ratio,
influences skeletal development.2 Young, giant-breed dogs fed a food containing excess calcium
(3.3% dry matter basis) with either normal phosphorus(0.9% dry matter basis) or high
phosphorus(3% dry matter basis, to maintain a normal calcium/phosphorus ratio) had significantly
increased incidence of developmental bone disease.2 These puppies apparently were unable to
protect themselves against the negative effects of chronic calcium excess.3 Further, chronic high
calcium intake increased the frequency and severity of osteochondrosis.7

Often puppies are switched from growth to maintenance-type foods to avoid calcium excess and
skeletal disease. However, because some maintenance foods have much lower energy density than
growth foods, the puppy must consume more dry matter volume to meet its energy requirement. If
the calcium levels are similar (dry matter basis) between the two foods, the puppy will actually
consume more calcium when fed the maintenance food. This point is exemplified in the case of
switching a 15-week-old, 15-kg male Rottweiler puppy from a growth food containing, on an as fed
b asis, 4.0 kcal/g metabolizable energy and 1.35% calcium (1.5% on a dry matter basis) to a
maintenance food containing the same amount of calcium but at a lower, 3.2 kcal/g energy density.
The puppy would require approximately 1,600 kcal/day. In order to meet this energy need the
puppy would consume approximately 400g of the growth food (containing 5.4g of calcium) vs. 500g
of the maintenance food (containing approximately 6.7g of calcium).

Feeding treats containing calcium and/or providing calcium supplements further increases daily
calcium intake. Two level teaspoons of a typical calcium supplement (calcium carbonate) added to
the growth food of the 15-week-old, 15-kg Rottweiler puppy would more than double its daily
calcium intake. This calcium intake is well beyond the levels shown to increase the risk for
developmental bone disease. A recent review article best sums up the need for calcium supplements:
"Because virtually all dog foods contain more calcium than is needed to meet the requirement, the
use of a calcium supplement certainly is unnecessary. Now that the deleterious effects of excess
dietary calcium have been delineated, we can say that the feeding of calcium supplements not only is
unnecessary, but, in fact, contraindicated!"8

Because these studies demonstrate the safety and adequacy of 1.1% calcium (dry matter basis) and
the Association of American Feed Control Officials (AAFCO) minimum recommendation is 1% (dry
matter basis, Table 1), we recommend that calcium levels for a growth food be within this range for
at risk puppies, with no supplementation.

Other Nutrients

L-ascorbic acid (Vitamin C) is necessary for hydroxylation of proline and lysine during biosynthesis
of collagen, a major component of ligaments and bones. Food devoid of Vitamin C fed to puppies
for 147 to 154 days neither affected growth nor caused skeletal lesions.12 There are no known
dietary requirements for Vitamin C in the dog.11 Vitamin C supplementation in pigs elevates plasma
levels of Vitamin C without changing articular concentrations of hydroxyproline.13 Similar studies in
dogs demonstrated transient elevation of plasma Vitamin C concentrations; however, long-term
supplementation did not increase concentrations much above normal.14 Even though Vitamin C has
been recommended, the relationship between Vitamin C and developmental skeletal disorders in
dogs such as osteochondrosis and hip dysplasia is unproven.15 Vitamin D metabolites regulate
calcium metabolism and therefore skeletal development in dogs. These metabolites aid in the
absorption of calcium and phosphorus from the gut, increase bone cell activity, and influence
endochondral ossification and calcium excretion.16 Unlike other omnivores, the dog seems
dependent on dietary Vitamin D sources from plants (Vitamin D2) or animals (Vitamin D3).
Commercial pet foods contain from two to 10 times the AAFCO recommended amounts of Vitamin
D.6 Diagnosis of Vitamin D deficiency can be made by measuring circulating levels of Vitamin D
metabolites and by measuring growth plate width. Clinical cases of Vitamin D deficiency (rickets) are
extremely rare in animals eating commercial foods.6 Increased growth plate width is not associated
with low calcium/high phosphorus foods but is a strong indicator of rickets.16 Excess Vitamin D can
cause hypercalcemia, hyperphosphatemia, anorexia, polydipsia, polyuria, vomiting, muscle
weakness, generalized soft tissue mineralization, and lameness. In growing dogs, supplementation
with Vitamin D can markedly disturb normal skeletal development due to increased calcium and
phosphorus absorption.16 The trace minerals copper and zinc are involved in normal skeletal
development. Supplementing a mare's dietary copper intake during the late stages of pregnancy, and
supplementing the foal's diet from 90 to 180 days of age has been shown to reduce the prevalence
and severity of developmental cartilage lesions.17 Copper deficiency in dogs has been associated
with hair depigmentation, hyperextension of the distal phalanges, and decreased copper levels in the
hair, liver, kidney, and heart muscle.18 However, bone copper concentration was not influenced by
dietary treatment and developmental skeletal abnormalities associated with a deficiency of dietary
copper were not described. Similarly, long-term studies of dietary zinc on canine growth and
reproduction showed no significant clinical influence on the skeletal development.19 The role of
these two nutrients in the development of skeletal disease in the dog remains unclear at this time.

Two of the most common skeletal diseases of growing dogs are hip dysplasia and osteochondrosis.
The balance of this section will review the relationship between these diseases and critical nutrients.

Canine Hip Dysplasia (CHD)

Canine hip dysplasia (CHD) is the most frequently encountered orthopedic disease in
veterinarymedicine (Fig. 2). The actual number of cases is estimated to be in the millions.20 This
extremely common heritable disorder of large and giant-breed dogs can be influenced by nutrition
during growth. Early developmental findings of CHD, including joint laxity and coxofemoral
anatomical changes, have been documented within 2 weeks of birth. Rapid weight gain in German
Shepherd dogs during the first 60 days after birth has been associated with CHD at a later age. The
importance of this early influential time period was demonstrated in a study comparing
cesarean-section, hand reared puppies to vaginal birth, bitch-fed puppies. Cesarean section and
hand rearing markedly reduced growth and the incidence of CHD in these puppies. Vaginally born,
bitch-fed puppies that grew "optimally" or somewhat "suboptimally" had a higher incidence of
CHD.21 The period from 3 to 8 months of age is important in the development of CHD, with the
first 6 months generally regarded as the most critical. Frequency and severity of CHD was influenced
by weight gain in growing dogs that were offspring of parents with CHD or parents with a high
incidence of CHD in their offspring. Dogs with weight gain that exceeded breed standards had a
higher frequency and more severe CHD than dogs with weight gain below breed standards.22

In one colony of fast growing Labrador Retriever dogs, the triradiate growth plates of the acetabula
fused at 5 months as determined by conventional radiography. These growth plates normally close at
6 months in puppies growing at conventional rates. The investigators speculated that early fusion in
the acetabulum may result in bone/cartilage disparities in the future and predispose to dysplastic
changes.23 Limiting food intake in growing Labrador Retriever puppies has been associated with
less subluxation of the femoral head and fewer signs of hip dysplasia.24

Palpation of the hip is of little to no value in predicting development of hip joints. However, the
combination of physical and radiographic examination are important diagnostic methods for
evaluating the hips (Orthopedic Foundation for Animals, Columbus, MO; Penn HIP, Malvern, PA).
A recent review of nutritional influences on CHD contains more information and a more complete
reference list.25

Electrolyte Balance and CHD

Control of dietary electrolytes has been proposed as a preventative for CHD.26 Investigators have
associated the dietary anion gap (DAG) with the radiographic changes of subluxation in the
coxofemoral joints in several canine breeds. A food with a DAG (Na+ + K+ - Cl-) < 23 mEq/100g
of food was fed to large-breed puppies and resulted in less femoral head subluxation, on average, at
6 months of age. The slowed progression of subluxation was also observed in dogs fed a food with a
reduced DAG from 35 to 45 weeks of age.28 Hip joint laxity was determined using the Norberg hip
score computed from radiographs. Significant correlation between radiographic findings (e.g.,
Norberg hip scores)and progression of CHD, either radiographic or clinical was not proven. The
authors propose the balance of anions and cations in the food (specifically sodium, potassium, and
chloride) influence the electrolytes and osmolality in joint fluid. The joint fluid of dysplastic dogs has
higher osmolality and is increased in volume when compared to that of disease-free hips from dogs
of the same breed.29 The changes in osmolality and fluid volume could be a result rather than a
cause of CHD. Changes in synovial fluid osmolality and electrolyte concentrations were not
reported. These studies suggest an association between DAG and joint laxity without proving a
mechanism of action.

Osteochondrosis (OCD)

Osteochondrosis is a focal disruption in endochondral ossification. OCD is manifested clinically by
pain and lameness. Physical examination results can be confirmed radiographically. Figure 3  shows
a classic inoperative lesion on the proximal humerus. Acute inflammatory joint disease begins when
the subchondral bone is exposed to synovial fluid. Inflammatory mediators and cartilage fragments
are released into the joint and perpetuate the cycle of degenerative joint disease.27 OCD occurs in
the physis and/or epiphysis of growth cartilage, and is a generalized or systemic disease. When OCD
affects the physis, it may cause growth abnormalities in long bones. OCD is wide-spread among
young, rapidly growing, warm-blooded, domesticated species and humans. In all species, the
etiology is considered multifactorial. In dogs, risk factors for OCD are age, gender, breed, rapid
growth and nutrient excesses (primarily calcium).1,5,25,29

All large and giant-breed dogs are at increased risk for OCD. Great Dane, Labrador Retriever,
Newfoundland, and Rottweiler breeds are at highest risk.29 Males have an increased risk of OCD
in the proximal humerus but gender relationships are not found with OCD involving other joints.28

At least two schools of thought exist concerning the pathogenesis of OCD. In the first, cartilage
lesions develop secondary to excessive biomechanical stresses. This may be termed an "outside-in"
development. Over-nutrition, such as ad libitum feeding, stimulates skeletal growth, cancellous bone
remodeling, and weight gain in breeds already having inherent capacity for rapid growth.5 Rapid
growth combined with remodeling results in weakened subchondral regions to support the cartilage
surface. If osteopenic and biomechanically weak subchondral spongiosa develops, there is
inadequate bony support to the articular cartilage. The increasing body mass exerts excessive
biomechanical forces on the cartilage and secondarily disturbs chondrocyte nutrition, metabolism,
function, and viability. An outside-in development suggests OCD results when nutritional effects
initiate a biomechanical disease.

An "inside-out" pathogenesis has also been proposed. Here, abnormalities of the cartilage canal
vessels and chondrocyte necrosis are thought to precede degenerative changes in the articular
cartilage matrix.30 Focal lesions of dead and nectrotic chondrocytes develop, and subsequently,
biomechanical stresses disrupt the lesion. Osteochondrosis lesions are routinely found in pigs as
young as 25 days of age, when rapid growth and weight gain are much less of a factor. These
findings support a localized, primary effect on the chondrocyte rather than secondary effects of
biomechanical force.

Regardless of the pathogenesis of OCD, nutrition is still an underlying factor. In growing puppies,
overnutrition can result in a mismatch between body weight and skeletal growth, which can overload
skeletal structures.7 Nutrition of the mother may also play a role in the development of OCD in the
offspring.

Feeding techniques

The nutrient profile of the food and how it is fed control nutritional risk factors for developmental
skeletal disease. There are three basic methods of feeding growing dogs: free-choice (ad libitum),
time-limited, or food-limited.

Free-choice feeding

Free-choice feeding is relatively effortless and may reduce abnormal behavior such as barking at
feeding time. Frequent trips to the food bowl help reduce boredom, timid or unthrifty animals have
less competition when eating, coprophagy may be decreased, and frequent small meals may result in
a more constant blood level of nutrients and hormones.

Disadvantages of ad libitum feeding include food wastage, only dry forms of pet food can be fed,
and competition or boredom may stimulate overeating. The most serious disadvantage is increased
risk of developmental bone disease because of overconsumption in the large and giant breeds.1-4,
24 In general, free-choice feeding in contraindicated in "at risk" dogs until they have reached skeletal
maturity (about 12 months of age or at least 80 to 90% adult weight).

Time-limited feeding

Time-limited feeding can be used for most large and giant breeds. Making food available for a set
period of time, two to three times per day, may help control intake and help in discipline and
housetraining young puppies. The owner interacts with the puppy during this time and is able to
observe general condition and behavior. This may lead to earlier detection of health problems. A
routine of feeding a puppy then taking it outdoors can enforce housetrainng by taking advantage of
the gastrocolic reflex.

Some researchers have proposed that puppies fed on a time-limited basis consumed less food, had
slightly reduced growth rates, but achieved similar adult size and lean body mass when compared to
puppies eating free-choice.8 Other studies have shown that feeding 15 minutes twice a day did not
result in decreased food intake between ad libitum and time-restricted groups.31 Many variables
(e.g., breed, temperament, housing, etc.) influence these results and account for the varied findings. If
time-restricted feeding is used, 5 to 10 minute feeding periods (3x per day for the first month after
weaning, then 2x per day) may be required to decrease food intake in some puppies.

Food-limited feeding

The method of choice for feeding puppies is limiting food intake to maintain growth rate and body
condition. Food-limited feeding requires feeding a measured amount of food based on calculated
energy requirement or as recommended by the manufacturer. Energy requirement is most easily
calculated by using resting energy requirement (RER) as a base on which to build. RER can be
calculated using either of the following two equations:

                         RER (kcal/day) - 70 (Wtkg)0.75

                                    or

                        RER (kcal/day) = 30 (Wtkg) + 70

As a starting point use 3x RER for the first 4 months of life and 2x RER from 4 months of age to
skeletal maturity (about 12 months for most breeds). Most large and giant-breed dogs will continue
to increase bodyweight and muscle mass after 12 months, but the growth rate is reduced and most if
not all growth plates are closed. At 12 months they can be fed as adults (1.6x RER).

Once daily caloric requirement has been calculated (kcal/day), divide this number by the energy
density of the food (kcal/cup or kcal/can) to determine the number of cups or cans to feed per day.
Remember, these calculations and manufacturers' recommendations are only starting points. Clinical
evaluation of the growing puppy and adjustment of food offered is crucial. Rapidly growing, large
and giant-breed dogs have a very steep growth curve and their intake requirements can change
dramatically over short time periods. These puppies should be weighed, evaluated, and their daily
feeding amount adjusted at least once every 2 weeks (Fig. 1). Most of the studies that have
demonstrated the beneficial effects of limiting food intake of puppies have fed the limited group 25 to
30% less food then their counterparts ate when fed free-choice. Unfortunately, this is not a practical
approach to feeding most puppies in a home environment.

Evaluation of feeding methods and body condition scoring

Regardless of a food's nutrient profile and how it is fed, the ultimate measurement of appropriate
intake is the physical condition of the puppy. The only way to reduce potentially harmful nutritional
risk factors that may affect skeletal development is to assess body condition and adjust the amount
fed to ensure lean, healthy growth. We recommend that at risk puppies be evaluated at least every 2
weeks. Figure 4 reviews body condition scoring and physical findings. A more in-depth discussion
follows.32

A body condition score of 1 is characterized as very thin. The ribs are easily palpable with no fat
cover. The tailbase has a prominent raised bony structure with no tissues between the skin and the
bone. The bony prominences are easily felt with no overlying fat. In  animals over 6 months, there is
a severe abdominal tuck when viewed from above.

An underweight condition is categorized as a 2 in the scoring system. The ribs are easily palpable
with minimal fat cover. The tailbase has a raised bony structure with little tissues between the skin
and the bone. The bony prominences are easily felt with minimal overlying fat. In animals over 6
months, there is an abdominal tuck when viewed from the side and a marked hourglass shape when
viewed from above.

The ideal body condition of a puppy is represented by a score of 3. The ribs are palpable with a thin
layer of fat between the skin and the bone. The bony prominences are easily felt with a significant
amount of overlying fat. In animals over 6 months, there is an abdominal tuck when viewed from the
side and a well proportional lumbar waist when viewed from above.  A score of 4 is defined as
overweight. The ribs are difficult to feel with moderate fat cover. The tailbase has some thickening
with moderate amounts of tissue between the skin and the bone. The bony structures can still be felt.
The bony prominences are covered by a moderate layer of fat. In animals over 6 month, there is little
or no abdominal tuck of the waist when viewed from the side. The back is slightly broadened when
viewed from above.

An obese condition is represented as a 5 on the scale. The ribs are very difficult to feel under a thick
fat cover. The tailbase appears thickened and is difficult to feel under a prominent layer of fat. The
bony prominences are covered by a moderate to thick layer of fat. In animals over 6 months, there is
a pendulous ventral bulge and no waist when viewed from the side. The back is markedly broadened
when viewed from above.

Conclusion

Large and giant-breed dogs are the most susceptible to developmental skeletal disease. Genetics,
environment, and nutrition play key roles. Nutritionally, rate of growth, food consumption, specific
nutrients, and feeding methods influence our ability to optimize skeletal development and minimize
skeletal disease. Maximizing the growth rate in young, growing puppies does not correlate to
maximal adult size. It does, however, increase the risk of skeletal disease. The growth phase of 3 to
8 months, and possibly the phases before weaning, are vital to ultimate skeletal integrity. The large
and giant breeds may be limited in their ability to cope with excesses of minerals such as calcium.

Overnutrition from overconsumption and oversupplementation increases the frequency of
developmental bone disease in large and giant-breed dogs. Energy and calcium are the nutrients of
greatest concern. Often, owners feeding highly palatable, energy-dense growth foods switch to
maintenance type foods in an attempt to reduce developmental disorders. As shown earlier, this
practice may worsen total calcium intake. It is not only important to feed the appropriate food, but to
feed the food appropriately.

Table 1 lists the minimum requirement of some nutrients of concern for growing puppies. These
values represent the minimum and in some cases the maximum AAFCO recommendations for these
nutrients. Foods for large and giant-breed puppies should meet these recommendations. Because
energy (primarily from fat) and calcium are nutrients known to be risk factors for developmental
skeletal disease, the level of these nutrients should be near the minimum requirement. Meeting but not
exceeding the requirement for these nutrients ensures proper growth while minimizing risk factors for
skeletal disease.

Nutritional management alone will not completely control developmental bone diseases. Skeletal
diseases can be influenced during growth by feeding technique and nutrient profile. Dietary
deficiencies are minimal concern in this age of commercial foods specifically prepared for young,
growing dogs. The potential for harm is in overnutrition from excess consumption and
oversupplementation.

References

1. Hedhammer A, et al; Overnutrition and Skeletal Disease: An
Experimental Study in Growing Great Dane
Dogs, Cornell Vol 64 (suppl 5): 11-60, 1974

2. Hazewinkel HAW, et al; Calcium Metabolism in Great Dane Dogs Fed
Diets With Various Calcium and
Phosphorus Levels, J Nutr 121:599-S106, 1991.

3. Hazewinkel HAW, et al; Influences of Chronic Calcium Excess on the
Skeletal Development of Growing Great
Danes, JAAHA 21: 377-391, 1985

4. Meyer H, Zentek J; Energy Requirements of Growing Geat Danes, J Nitr
121: 335-838, 1991.

5. Daminnich K; Relationship Between Nutrition and Bone Growth in large
and Giant Dogs, J Nutr
121:8114-8121, 1991.

6. Kaltfalz FA, Ozanis DA; Overnutrition: An Epidemic Problem in Pet
Animal Practices, Vet Clinic North Am
Small Anim Pract 19(3): 433-446, 1989.

7. Nap RC, Hazewinkel HAW; Growth and Skeletal Development in the Dog in
Relation to Nutrition: A Review,
Vet Quarterly 1:50-59, 1994.

8. Alexander JE, WOOD LL; Growth Studies in Labrador Retrievers Fed a
Caloric-Dense Diet: Time-Restricted
Versus Free-Choice Feeding, Companion Animal 14 (2): 41-47, 1987.

9. Nap RC, et al; Growth and Skeletal Development in Great Dane Pups Fed
Different levels of Protein Intake, J
Nutr 121:8107-8113, 1991.

10. Nap RC, et al; The Influence of the Diet Protein Content on Growth
in Giant Breed Dogs, j Vet Comp
Orthop Trauma 6:1-8, 1993.

11. Ozanis DA; The AAFCO Dog and Cat Food Nutrient Profiles, In Current
Veterinary Therapy XII, Ed by JD
Bongura, Philadelphia, WS Saunders, 1995, pp 1418-1421.

12. National Research Council Nutrient Requirements of Dogs, Washington,
DC, National Academy Press,
1995.

13. Nakano T, Aheme FX, Thmopson JR; Effect of Dietary Supplementation
of Vitamin C on Pig Performance
and the Incidence of Osteochondrosis in Elbow and Stifle Joints in Young
Growing Swine, Can j Anim Sci
63:421-428, 1983

14. Teare JA, et al; Ascorbic Acid Deficiency and Hypertrophic
Osteodystrophy in the Dog: A Renuttal,
Cornell Vet 69:384-401, 1979.

15. Bennet D; Hip Dysplasia and Ascorbate Therapy: Fact or Fancy? Semin
Vet Med Surg (small Anim) 2 (2):
152-157, 1997.

16. Hazewinkel HAW; Nutrition in Orthopedics, In: Disease Mechanisms in
Small Animal Surgery, ed 2. Ed by
MJ Bojrab, Philadelphia, Lea & Febiger, 1993,