An 8-month-old sexually intact female Shetland Sheep-dog was evaluated at the Veterinary Teaching Hospital of the Virginia-Maryland Regional College of Veterinary Medicine following a sudden onset of signs of neck pain, collapse, and inability to rise. Twenty-four hours earlier, the dog had yelped loudly while exercising outdoors, stumbled back into the home, and fallen to the floor; the dog was alert and extremely anxious and made unsuccessful attempts to rise. Shortly thereafter, the dog was examined by the family veterinarian, who noted signs of cervical pain and tetraparesis. A CBC and serum biochemical analyses were performed; abnormalities included hypocalcemia (6.9 mg/dL; reference range, 8.6 to 11.8 mg/dL), hypoalbuminemia (2.2 g/dL; reference range, 2.5 to 4.4 g/dL), and high serum alkaline phosphatase activity (232 U/L; reference range, 20 to 150 U/L). The biochemical reference ranges were adjusted to the age of the patient. Initial treatment performed by the referring veterinarian prior to transfer to the hospital was limited to administration of analgesics, which included butorphanol (0.4 mg/kg [0.18 mg/lb], SC, once), transdermal fentanyl patch (5.6 μg/kg/h [2.55 μg/lb/h], removed at the hospital 18 hours after placement), and carprofen (4.0 mg/kg [1.82 mg/lb], SC, once).
Historical information indicated that the dog had been routinely vaccinated 5 months prior to the initial evaluation at the hospital and was closely supervised in its home environment. Retrospectively, the owners commented that the dog's appetite and energy level had been decreased during the preceding 2 weeks and that it occasionally appeared lame when exercising, although these had not been notable concerns. Four months earlier, at 4 months of age, the dog's diet had been changed from a commercial growth food to a muesli-vegetable powder premixa (which the owners had seen advertised on the Internet) combined with raw ground beef. At the time, the manufacturer of the premix advertised that “when mixed with raw meat, the diet can be fed to both puppies and adult dogs of all dietary needs….”1 Detailed instructions for measuring and mixing of the diet components were provided on the package label. The puppy had been fed this diet during the 4-month period with no apparent ill effects.
At the initial evaluation at the hospital, physical examination findings were largely unremarkable. The dog's weight was 3.7 kg (8.1 lb); although this value was less than the lower limit of the reported breed standard2 for a dog of this age (4.5 to 6.8 kg [9.9 to 15.0 lb]), its BCS (4/9) was considered adequate. General conformation appeared unusual, in that the overall thoracic limb length appeared short bilaterally, compared with the lengths of the pelvic limbs. Littermates that had been fed puppy chow by different owners were comparably normal in stature.
Neurologic examination revealed nonambulatory spastic tetraparesis. Postural reactions were markedly depressed in the pelvic limbs and moderately depressed in the thoracic limbs. Extensor muscle tone was increased in all limbs, and all spinal reflexes were intact. Equivocal positional nystagmus was observed at the time of initial evaluation but could not be detected later. The remainder of the cranial nerve examination findings were apparently normal. With regard to mentation, the dog was anxious, alert, and responsive. No signs of pain were elicited on palpation of the vertebral column, although extensive manipulation was not attempted. These findings provided a neuroanatomic diagnosis of myelopathy between the first and fifth cervical spinal cord segments. Primary differential diagnoses included atlantoaxial instability, infarction, and disk herniation. Traumatic fracture, luxation, or contusion of the vertebral column, myelitis, and neoplasia were considered less likely.
The initial diagnostic plan included serum biochemical analyses and radiography of the cervical portion of the vertebral column, followed by advanced imaging procedures (computed tomography, myelography, and MRI) and CSF analysis. Notable serum biochemical abnormalities detected at the initial evaluation included low concentrations of phosphorous (2.2 mg/dL; reference range, 2.5 to 5.2 mg/dL), calcium (8.9 mg/dL; reference range, 9.3 to 10.6 mg/dL), and cholesterol (141 mg/dL; reference range, 160 to 345 mg/dL) and high activity of alkaline phosphatase (152 U/L; reference range, 13 to 110 U/L). Ionized calcium concentration (assessed in a sample of heparinized whole blood) was 1.21 mmol/L (reference range, 1.42 to 1.54 mmol/L).b A blood sample was submitted for lead assay via graphite furnace atomic absorption spectrometry (deuterium background correction method).c Results indicated that the blood lead concentration was not abnormal (30 ppb). Serum titers of antibodies against various causative agents of meningomyelitis were measured via either an indirect immunofluorescent antibody method (Rickettsia rickettsii, Ehrlichia canis, and Neospora caninum) or an enzyme-linked immunosorbent antibody method (Borrelia burgdorferi and Toxoplasma gondii).d Results of the assay for anti–T gondii antibodies suggested exposure without active infection (IgM antibody titer, 1:256; no IgG antibody detected). Results of all other serologic tests were negative.
Radiography of the cervical vertebral column revealed apparently normal vertebral conformation and no evidence of vertebral body fracture or luxation. However, generalized osteopenia was evident in the vertebral column, caudal aspect of the mandible, and scapulae. Survey radiography of the thorax, proximal portions of the thoracic limbs, and mandible were performed. Findings confirmed severe, diffuse osteopenia as well as gross deformity of weight-bearing bones and scapulae (Figure 1). Several so-called step incongruities were also detected on the caudal aspects of each scapula and spinal processes of select thoracic vertebrae, which were suggestive of pathologic fractures. The thoracic cavity appeared compressed dorsoventrally, and the hilar region was displaced dorsally on lateral radiographic views of the thorax. The lower dental arcade had signs of severe alveolar bone loss with only traces of lamina dura remaining. The radiographic findings, combined with confirmed mild hypocalcemia and hypophosphatemia, raised suspicion of metabolic bone diseases, including NSHPT and vitamin D–dependent rickets type I.
Left lateral and ventrodorsal radiographic views of an 8-month-old dog that had a sudden onset of signs of neck pain, collapse, and inability to rise obtained at the initial evaluation (A, C, D, and F) and at 30 weeks after treatment (B, E, and G). Views include the thorax (A and B), right scapula (lateral [C] and ventrodorsal [D and E] views), and mandible (F and G). In panels A, C, and D, notice the curvature of the scapula; in panel F, the lamina dura are not visible. Mineralization appears to improve after 30 weeks of dietary and medical treatment (B, E, and G), compared with the initial findings (A, D, E, and F); in panel E, the scapula appears to have straightened. Lamina dura are more visible in panel G. Some views have been magnified for visual enhancement; however, all views were taken at the same radiographic settings.
Citation: Journal of the American Veterinary Medical Association 234, 8; 10.2460/javma.234.8.1041
While awaiting results of serologic analyses, the dog received empirical treatment for the cervical myelopathy of unknown etiology, which included doxycycline (5.0 mg/kg [2.27 mg/lb], PO, q 12 h) and clindamycin (10.0 mg/kg [4.55 mg/lb], PO, q 8 h). When the test results were available, doxycycline was discontinued and treatment with clindamycin was continued for a 2-week period because of equivocal serologic findings regarding T gondii. Prothrombin and activated partial thromboplastin times, serum total thyroxine concentration, and blood pressure measurements were assessed for additional risk factors for cerebrovascular accidents; the results of these assessments were unremarkable.
On the second day of hospitalization, following an isolated episode of vomiting, the dog developed labored breathing, oxygen-dependent cyanosis, and pulmonary crackles attributed to presumed aspiration pneumonia. Treatment of clinical signs was instituted, including administration of supplemental oxygen via nasal cannula, enrofloxacin (10 mg/kg, IV, q 24 h), and ampicillin sodium–sulbactam sodium (20.0 mg/kg [9.09 mg/lb], IV, q 8 h). Respiration gradually returned to normal by the sixth day of hospitalization, and at that time, administration of amoxicillin-clavulanate potassium (15.0 mg/kg [6.82 mg/lb], PO, q 12 h) was substituted for IV administration of the other antimicrobials.
Noticeable improvement in neurologic function (motor strength and proprioception) occurred during the first 2 days of hospitalization. On the third day, the puppy was weakly ambulatory. Prior to discharge on the sixth day, the dog was able to ambulate strongly with mild proprioceptive ataxia and spastic tetraparesis. This rapid improvement reinforced the primary differentials of contusive or ischemic insult to the spinal cord. Once ambulation was restored, intermittent, mild, shifting-limb lameness was evident. This was attributed to pain resulting from normal weight-bearing forces on bones that were weakened and undergoing remodeling.
On the fifth day of hospitalization, an additional serum sample that was obtained after food had been withheld from the dog was submitted for analyses of PTH, 25(OH)D3, and ionized calcium concentrations; sample handling was performed as directed by the referral laboratory.e No abnormalities were detected with regard to serum concentrations of PTH (6.5 pmol/L; reference range, 3 to 17 pmol/L) and ionized calcium (1.45 mmol/L; reference range, 1.25 to 1.45 mmol/L), but serum 25(OH)D3 concentration was markedly low (32 mmol/L; reference range, 60 to 215 mmol/L). Derangement of these concentrations may have been underestimated because the dog had been fed a commercial prescription recovery diet for 5 days prior to sample collection.f Sample handling and processing both before and after shipment were performed as directed without known complications; however, temperature fluctuation during transit is a potential cause of artifactually decreased serum PTH concentrations as noted by the referral laboratory.e
For 4 months prior to evaluation at the hospital, the dog's daily diet consisted of 1.5 ounces of a packaged dog food premix,a 2 ounces of raw hamburger beef, 4.2 ounces of water, and 2 tablespoons of vegetable powder. On the basis of the strong clinical suspicion of metabolic bone disease and the dietary history, a sample of the complete mixture (prepared according to manufacturer's recommendations and as fed to the puppy) was sent to a commercial laboratory for analysis.g The nutrient composition of the dog's diet was reported on a dry matter basis (with the exception of energy, which was reported on an as-fed basis) and was compared with AAFCO published MAFGs3 for a canine growth diet. In the dog's diet, the most important deviation from the published allowances was the calcium-to-phosphorus ratio of 1:5.5 (MAFG, 1.0 to 2.0:1), which represented a relative calcium deficiency of 80% to 90%. In addition, there were deficiencies in the absolute concentrations of both calcium and phosphorous (0.08% and 0.44%, respectively [MAFGs, 1.0% to 2.5% and 0.8% to 1.6%, respectively]). The diet mix fed to the dog was excessive in energy density (3.95 kcal/g [MAFG, 3.5 kcal/g]) but was adequate in protein (23.9% [MAFG, 22.0%]) and fat (14.8% [MAFG, 8.0%]) contents. Potassium content of the dog's diet mix was 0.59% (MAFG, 0.60%). Amounts of magnesium and manganese were higher in the diet mix, compared with AAFCO allowances (0.13% [MAFG, 0.04%] and 31 ppm [MAFG, 5 ppm], respectively). Amounts of sodium, iron, zinc, and copper were low (0.105% [MAFG, 0.300%], 62 ppm [MAFG, 80 ppm], 48 ppm [MAFG, 120 ppm], and 5 ppm [MAFG, 7.3 ppm], respectively). The energy need for growth of the dog at 8 months of age was approximately 373 kcal of metabolizable energy/d. This value represented the dog's DER as calculated by use of the interspecies allometric equation as follows: (70 × [body weight in kilograms]0.75) × 1.4.4 The DER factor of 1.4 was chosen on the basis of the dog's age, size, BCS, and skeletal maturity.4 Although the energy density of the dog's diet mix was excessive, the amount fed to the dog, based on manufacturer guidelines, was 29% lower than calculated DER. The dog's diet mix was not analyzed for vitamin D2 or vitamin D3 content, nor was vitamin D added to the muesli-vegetable mixture by the manufacturer. After a review of the clinical and dietary findings, the differential diagnoses included vitamin D–dependent rickets type I, NSHPT, or both.
Initial treatment for the suspected nutritional deficit consisted of feeding a commercial prescription recovery dietf with intermittent feedings of a low-residue dieth in an attempt to encourage the dog to eat. Appetite was initially poor but gradually improved. Prior to discharge from the hospital, the commercial prescription recovery diet was gradually changed to a balanced commercial canine canned adult diet.i The rationale for feeding an adult diet was to promote controlled growth and homogeneous remineralization of the skeletal framework, thereby reducing the risk of development of new deformities or exacerbation of existing problems.4 A canned diet was recommended instead of kibble to reduce the strain of mastication on the osteopenic mandible. The owners were instructed to feed an amount of the adult canine canned diet that met the dog's DER (373 kcal of metabolizable energy/d) divided equally between 2 or 3 meals each day for 3 weeks. Home care consisted of gentle passive range of motion exercises in each limb, controlled leash walks, and cage confinement when the dog was unsupervised.
At 4 weeks after discharge from the hospital, the dog was returned for a recheck examination. The owners reported steady improvement in the dog's coordination, strength, and energy. It was more eager to both walk and prehend food and appeared to do so with less discomfort. The dog's weight and BCS remained unchanged at 3.7 kg and 4 (on a scale of 9), respectively. The dog was sedated and anesthetized for follow-up radiography and an initial DEXA scan.j Radiographically, no notable changes were observed relative to the initial findings. On the basis of DEXA scan data, the dog's body composition was 51% tissue fat and 49% lean tissue (fat and lean masses were 1,759 and 1,685 g, respectively); bone mineral content was 90.9 g, and bone mineral density was 0.259 g/cm2. Because little improvement was evident radiographically and the bone mineral density was markedly less than the mean value for young and mature dogs (1.0 g/cm2),5,k exercise restriction was continued. Because of the dog's maintenance of weight and BCS and its continued clinical improvement, the calculated DER and subsequent total daily calorie intake provided were judged to be appropriate and were not changed. At this point in the recovery process, it was recommended to incrementally increase the amount of dietary calcium provided to the dog by progressively changing its food from the canned adult diet to a canned canine growth diet.l Instructions were given to the owners to blend the adult diet with the growth diet so that the dog received 50% of the daily calories from each diet for a 4-week period.
At 8 weeks after discharge from the hospital, the dog was returned for another recheck examination. Although the BCS (4/9) had not changed, the dog's weight had increased by 5% to 3.9 kg (8.6 lb). The owners considered the dog clinically normal at this time, and no major deficits were detected via neurologic examination. The dog's gait appeared intermittently short-strided in all limbs but was dramatically improved, compared with previous findings. The dog was anesthetized for radiography and a second DEXA scan. Slight remineralization within the sternum, scapulae, and humeri was evident radiographically. The DEXA scan revealed that the fat and lean masses were 1,538 and 2,046 g, respectively, which represented a decrease in percentage tissue fat (to 43%) and an increase in percentage lean tissue (to 57%). Bone mineral content had increased to 100.4 g, and bone mineral density was 0.287 g/cm2. The owners were instructed to gradually change from feeding the adult diet–growth diet mixture to feeding only the canned canine growth diet over a 4-week period. Because of the increase in weight of the dog, the recalculated DER for growth was approximately 399 kcal of metabolizable energy/d, and the daily amount fed was increased accordingly.
At 16 weeks after discharge from the hospital, the dog was 1 year old and its BCS remained unchanged (4/9). It weighed 4.5 kg (9.9 lb). The owners were allowing the dog limited exercise at this time and reported that the dog had an increased energy level with no noticeable neurologic deficits. A repeat neurologic examination revealed equivocal postural reaction deficits on the left side with persistent mild shifting-limb lameness. Radiographically, bone density appeared increased by approximately 25%, compared with findings at the preceding recheck examination; remineralization was evident in all bone regions examined. A third DEXA scan was performed. The dog's fat and lean masses were 1,971 and 2,186 g, respectively; compared with data from the second scan, these values represented a slight increase in percentage tissue fat (to 47%) and a slight decrease in percentage lean tissue (to 53%). Over the 8-week period, bone mineral content had increased to 129.5 g and bone mineral density was 0.326 g/cm2. The bone mineral density was still less than published values5–8 for young adult dogs. Serum PTH, ionized calcium, and 25(OH)D3 concentrations were within reference ranges (11.5 pmol/L, 1.37 mmol/L, and 104 nmol/L, respectively). The owners were instructed to continue feeding the canned canine growth diet at the previously calculated DER and to increase exercise gradually.
The dog was returned to the hospital for another recheck examination 14 weeks later (at 30 weeks after discharge from the hospital). The owners reported that the dog had no visible abnormalities in stature or gait. Physical and neurologic examination findings were considered normal; the dog weighed 5.2 kg (11.5 lb), and its BCS was 5 (on a scale of 9). The dog was again anesthetized for radiography and a fourth DEXA scan. Radiography revealed marked remodeling of the scapulae, sternum, and ribs with only mild residual deformity (Figure 1). The bone density of previously osteopenic regions appeared nearly normal. The DEXA scan data indicated that the dog had 47% tissue fat and 53% lean tissue (fat and lean masses were 2,316 and 2,626 g, respectively). Bone mineral content had increased to 158.1 g (an increase of 28.6 g) over this 16-week period; bone mineral density was 0.386 g/cm,2 which represented an increase of 18.4% from the preceding recheck examination and an increase of 49% overall. Although these changes were positive, bone mineral density was still less than published reference values for adult dogs.6–8 Despite the success associated with feeding a canine commercial growth diet to the dog, the owners elected to change to a balanced homemade diet of cooked ingredients.
Discussion
In the dog of this report, vitamin D–dependent rickets type I or NSHPT was initially suspected on the basis of a cursory examination of the diet components, serum biochemical abnormalities, and radiographic findings. Rickets type I is an osteodystrophy that results from deficiency of vitamin D or, less commonly, phosphorous. Nutritional secondary hyperparathyroidism generally results from a calcium-deficient diet. Rickets type II was not suspected because it more typically develops as a result of vitamin D receptor abnormalities despite consumption of a balanced diet.9 In growing animals, vitamin D–dependent rickets type I, as well as NSHPT, is generally associated with bone pain, stiff gait, metaphyseal swelling, bowed limbs, pathologic fractures, and low serum vitamin D and calcium concentrations.10–13
The principal causes of osteodystrophies appear to be deficiencies or imbalances in dietary calcium, phosphorus, and vitamin D.12,14,15 Detection of the primary deficiency is problematic because absorption, activation, and use of calcium, phosphorus, and vitamin D are all interrelated to PTH.12,14–16 Absorption of calcium from the gastrointestinal tract is dependent on the presence of the active form of vitamin D, and that activation is dependent on PTH.16–19 Briefly, low blood calcium concentration is detected by calcium-sensing receptors in the chief cells of the parathyroid gland.15,16 Once secreted from chief cells, PTH stimulates osteoclastic activity in bones; it also stimulates hydroxylation of 25(OH)D3 (calcidiol) to the most active form, 1,25 dihydroxyvitamin D3 (calcitriol), in proximal tubules of the kidneys, a process that is catalyzed by 1-D hydroxylase.15,16 This active form of vitamin D activates calcium-binding proteins (calbindins) along with calcium channels and pumps, thereby enhancing enterocyte absorption of calcium and phosphorus from duodenal and colonic sites.12,14,17,19 As the circulating concentration of active vitamin D and, subsequently, blood concentration of calcium increase, PTH production is inhibited through a feedback mechanism that indirectly limits (or slows) dietary calcium absorption.18 An additional mechanism of dietary calcium absorption is directed via phosphorus homeostasis. Increased concentrations of phosphorus circulating in the blood can inhibit 1-D hydroxylase in the proximal tubules, thereby limiting production of the active form of vitamin D and thus limiting the amount of calcium and phosphorous absorbed from the diet.20 Specific bony lesions are associated with abnormalities in absolute or relative amounts of vitamin D, calcium, phosphorus, and PTH.10,12,15,21,22
In addition to deficiencies or excesses of any 1 constituent, a secondary pathologic change can develop because of feedback mechanisms, altered calcium-to-phosphorus ratio, or metabolic deficiencies.18 Over time, the bone mineral sources of calcium become depleted and the ability to maintain normal blood calcium and phosphorous concentrations becomes exhausted, and the patient becomes hypocalcemic.18 Clinical signs of hypocalcemia vary greatly but may include muscle fasciculations, tetany, seizures, cardiac conduction abnormalities, and death.23–25 In most cases of rickets type I and NSHPT, hypocalcemia is relatively mild; as a result, the most common clinical problems are related to chronic osteodystrophy (bone pain and pathologic fractures) rather than being direct sequelae of hypocalcemia.26
In the dog of this report, the initial problem was attributed to focal myelopathy, an unusual solitary clinical manifestation of metabolic bone disease. The initial signs obscured the more traditional clinical signs of osteodystrophy, which were identified incidentally during the routine investigation. A careful neurologic examination is necessary to distinguish spastic tetraparesis and collapse associated with myelopathy from the tetanic spasms, paresis, and collapse associated with hypocalcemic tetany—2 disorders that have distinctly different potential etiologies and treatments. The classic signs of cranial cervical myelopathy in the dog of this report were accompanied by an apparent transient vestibular disturbance, which is a less common clinical sign occasionally associated with cranial cervical myelopathy.27
On the basis of the peracute onset of signs, the short duration of signs of neck pain, and the rapid resolution of collapse without specific treatment, the most likely cause of the myelopathy was contusive or ischemic insult. In contrast, disorders such as disk herniation and gross fracture or luxation generally cause persistent spinal cord compression and result in static or progressive clinical signs, often including signs of pain. Diseases such as myelitis, neoplasia, and primary degenerative myelopathies are generally progressive in nature and often multifocal or diffuse in distribution.28,29
Contusive injury to the spinal cord without persistent compression may be caused by vertebral body subluxation (as a result of trauma or malformation), traumatic herniation of nondegenerate disk material, or external concussive trauma.30,31 The clinical and diagnostic findings in animals with these disorders may be similar or identical to those of ischemic myelopathy, which complicates establishing a definitive antemortem diagnosis. The clinical course of contusive injury to the spinal cord is similar to that of ischemic injury, presuming that persistent or repetitive injury does not occur. Given the known skeletal weakness and plasticity in the dog of this report, it seems feasible that a contusive spinal injury could result from vigorous exercise or rough play that generated excessive vertebral body motion and subluxation.
Fibrocartilaginous embolism is the most well-recognized cause of focal spinal cord infarction.30 Little published information exists regarding confirmation of other causes of vascular accidents in the spinal cord of dogs. To our knowledge, there are no reported associations between the types of nutritional and metabolic problems that developed in the dog of this report and ischemic or vascular accidents in the CNS of dogs. In the absence of other supporting evidence, ischemic myelopathy remains a largely theoretical differential diagnosis that is based solely on the clinical course of neurologic disease.
Magnetic resonance imaging of the cervical portion of the spinal cord would have been the ideal imaging technique to attempt to distinguish between the possible causes of this dog's myelopathy. Magnetic resonance imaging not only provides accurate diagnosis of extradural and intradural pathologic processes but also has the added benefit over other imaging techniques of allowing detailed examination of the intramedullary compartment. Because spinal cord infarction or contusion results in pathologic changes that are largely confined to the parenchyma of the spinal cord, MRI is often the only method for definitive diagnosis of this type of injury.32 However, distinguishing between these 2 categories of disease is challenging with conventional MRI techniques on the basis of spinal cord appearance alone. Signal changes within the spinal cord parenchyma are similar or identical following ischemic or contusive insult. The presence of structural abnormalities in the vertebral column (eg, disk degeneration, disk space narrowing, or incongruity or stenosis of the vertebral canal) adjacent to a focal intramedullary signal abnormality may support contusion of the spinal cord. When no structural abnormalities are present, infarction is suspected. In any case, histologic examination of spinal cord specimens is required to positively identify the cause of an intramedullary signal change. Therefore, antemortem diagnosis of contusion or infarction is generally presumptive even with the use of MRI.30–32
For the dog of this report, the development of aspiration pneumonia dramatically increased the risk potential of MRI or other procedures requiring anesthesia. In addition, marked, rapid neurologic improvement reduced the need for urgent intervention in the unlikely event that the dog had compressive myelopathy. For these reasons, further imaging of the vertebral column was postponed and ultimately not pursued. The resolution of clinical signs mitigated the need for a more definitive diagnosis.
Typically, grossly abnormal physeal widening at the metaphyses is evident in dogs with vitamin D–dependent rickets type I; such changes were not detected in the dog of this report. However, radiography revealed severe curvature of the scapulae, which is a common vitamin D deficiency–induced deformity in dogs and sheep.10–12 Although the diet mixture fed to the dog of this report was not analyzed for vitamin D content, the specific diet components (muesli-vegetable premix and ground beef) are not adequate sources of 1,25-hydroxyvitamin D3,4 nor was the muesli-vegetable premix supplemented with vitamin D by the manufacturer. The dog's low serum 25(OH)D3 concentration, along with the suspected dietary vitamin D deficiency, supported the diagnosis of osteopenic deformities caused by hypovitaminosis D. This osteodystrophy, in combination with detected serum abnormalities (hypocalcemia, hypophosphatemia, and hypovitaminosis D) and results of diet analysis (low calcium and phosphorus contents and altered calcium-to-phosphorus ratio), was also consistent with the suspicion of NSHPT. Diets that are typically high in phosphorous content relative to calcium content include meat diets that do not contain supplemental calcium and cereal- or seed-based diets; 1 such diet was fed to the dog of this report during 4 months of its growth phase. It is likely that both vitamin D deficiency and NSHPT were responsible for the clinical disease. The definitive diagnostic test for NSHPT is a serum PTH assay; in the dog of this report, results of that assay were within reference limits. However, logistic limitations as well as a delay in establishing an initial diagnosis prevented submission of a serum sample before treatment was initiated; the sample submitted was collected after the dog had been fed intermittently with calcium-fortified diets for 4 days. Thus, the extremely short half-life of PTH in circulation may account for a false-negative result in this case.33 The half-life of PTH in circulation has been reported to be < 30 minutes in humans.34
Young animals require calcium to mineralize newly formed cartilage and osteoid. In dogs, approximately 225 to 900 mg of calcium/kg/d (102 to 409 mg/lb/d) is deposited in the skeleton, and 100 to 225 mg of calcium/kg/d (45 to 102 mg/lb/d) is absorbed from the diet.21,33 The dietary calcium content in the diet mixture fed to the dog of this report supplied < 20 mg of calcium/kg/d (9.1 mg/lb/d), which resulted in poor mineralization of bone and increased bone resorption that caused pronounced skeletal abnormalities. When normal physiologic processes are restored after a period of inhibited growth because of malnutrition or illness of short duration, an animal will grow at a rate greater than that typically expected for its age (socalled catch-up growth).35 To avoid rapid calcium deposition in bone from excessive amounts of dietary calcium, a slow, gradual increase in calcium content of the dog's food intake was instituted. The adult canned maintenance dieti provided 184 mg of calcium/100 kcal, whereas the canine growth diete provided 322 mg of calcium/100 kcal. The calculated calcium-to-phosphorus ratio of the canned growth diet (1.37:1) was slightly higher than that of the maintenance canned diet (1.12:1). Thus, the nutritional management goal of an incremental increase in amount of dietary calcium was achieved by initiating feeding of a balanced canine maintenance life-stage diet followed by gradual transition to a balanced growth formula.
In a recently published case report,10 adequate recovery from skeletal malformations and bone demineralization in a puppy was achieved over a 3-month feeding period without the use of a transitional feeding protocol. Although the diagnosis was similar, specific aspects of that case and findings in the dog of this report differed, prompting dissimilar dietary treatment approaches. In the previous report,10 the puppy's bone mineral density prior to initiating a diet change was only moderately decreased (80% of the value expected in clinically normal puppies of the same age). In contrast, the initial bone mineral density in the dog of this report was < 50% of the expected value for a healthy 8-month-old dog. A phosphorus-restricted, vitamin D–adequate renal diet was fed to the puppy, which resulted in pathologic changes to the skeletal frame.10 The diet that precipitated skeletal changes in the dog of this report was deficient in calcium, phosphorus, and vitamin D (although some calcium carbonate has since been added to the premix36). Thus, because of the degree of bone mineral deficit, complexity of skeletal malformations, and duration of dietary mineral deficiency, remineralization of the bones in a stepwise, conservative manner was considered prudent for this patient.
To our knowledge, the effects of feeding a growth-type diet (high calcium content) and feeding a maintenance-type diet (maintenance calcium content) to young dogs during recovery from skeletal malformations associated with deficient dietary calcium and vitamin D intake have not been specifically compared. The approach taken for the dog of this report eliminated a rapid or catch-up growth phase. This was evidenced by the gradual increase in bone density measured via DEXA and the minimization of bone and joint abnormalities during the recovery period. The bone mineral density steadily increased over time as the calcium content in the dog's diet increased. Likewise, the increase in the dog's weight over time paralleled an increase in skeletal strength. This was most apparent in the scapular remodeling. Grossly, externally visible deformities (limb length and stance) were noticeably improved at the final visit.
At the initial evaluation, radiography provided valuable visual confirmation of diffuse, pathologic osteopenia, as well as revealing additional pertinent pathologic findings such as severe curvature of the scapulae. However, throughout the recovery process, radiography failed to accurately reflect progress in remineralization, whereas DEXA scan data provided a quantitative measure of increasing bone mineral density that was helpful in determining appropriate adjustments of the calcium content in the dog's diet.
Juvenile rickets type I and NSHPT have been reported rarely in veterinary medicine. This is likely because of the availability of commercially formulated pet diets and the nutritional adequacy of those diets (based on AAFCO guidelines). As highlighted by the dog of this report, clinical problems may develop as a result of feeding an unbalanced, home-prepared diet to pets. The potential risks of providing a nutritionally incomplete and unbalanced diet, especially during a high-stress period such as growth, cannot be overemphasized. Numerous concerns have been raised regarding the safety of commercial pet foods, particularly in light of recent product recalls, which may have led to an increased number of owners who are feeding home-prepared diets to cats and dogs. To ensure these diets are complete and balanced for the recipient animal, we strongly recommend that owners submit a representative sample to a reputable laboratory for a complete nutrient profile. Review of the diet analysis, ingredient source list, and diet preparation protocol, along with a thorough physical assessment of the pet, by a veterinarian may highlight potential nutritional concerns and prevent avoidable illness.
Abbreviations
| AAFCO | Association of American Feed Control Officials |
| BCS | Body condition score |
| DER | Daily energy requirement |
| DEXA | Dual-energy x-ray absorptiometry |
| MAFG | Minimum allowance for growth |
| MRI | Magnetic resonance imaging |
| NSHPT | Nutritional secondary hyperparathyroidism |
| PTH | Parathyroid hormone |
| 25(OH)D3 | 25-hydroxyvitamin D3 |
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Sojos European Style Dog and Cat Food Mix, Sojourner Farms, Minneapolis, Minn.
Rapidlab 348 blood gas analyzer, Siemens Healthcare Diagnostics, Tarrytown, NY.
SpectrAA 220 fast sequential atomic absorption spectrometer, Varian Inc, Palo Alto, Calif.
Athens Veterinary Diagnostic Laboratory, College of Veterinary Medicine, University of Georgia, Athens, Ga.
Diagnostic Center for Population Animal Health, Michigan State University, Lansing, Mich.
Hill's Science Diet Prescription a/d, Hill's Pet Nutrition, Topeka, Kan.
Dairy One, Ithaca, NY.
Eukanuba Maximum Calorie, Canned, Iams Co, Dayton, Ohio.
Hill's Science Diet, Canine Maintenance, Canned, Hill's Pet Nutrition, Topeka, Kan.
Lunar Prodigy Advance Model 8743, General Electric Health Care, Diegem, Belgium.
Waltham Centre for Pet Nutrition, Leicestershire, England.
Hill's Science Diet, Puppy, Canned, Hill's Pet Nutrition, Topeka, Kan.
