| |

Received: 7 December 2018    Revised: 23 February 2019    Accepted: 11 April 2019

DOI: 10.1111/jpn.13118

ORIGINAL ARTICLE

Abnormal bone mineralization in a puppy fed an imbalanced

raw meat homemade diet diagnosed and monitored using dual‐
energy X‐ray absorptiometry

Sarah Dodd | Maureen Barry | Caitlin Grant | Adronie Verbrugghe

Department of Clinical Studies, Ontario

Veterinary College, University of Guelph,
Guelph, Ontario, Canada
Correspondence
Adronie Verbrugghe, Department of
Clinical Studies, Ontario Veterinary College,
University of Guelph, 50 Stone Rd. E,
Guelph, ON N1G 2W1, Canada.
Email: averbrug@uoguelph.ca
Abstract
A 4‐month‐old male Old English Sheepdog was presented for evaluation of a raw
meat‐based homemade diet after a 1‐month history of progressive lameness. Marked
dietary deficiencies were detected, which included calcium, phosphorus and vita‐
min D. Hypovitaminosis D and hypocalcaemia were diagnosed by serum analysis.
Evidence of severe diffuse osteopenia was noted on survey radiographs. Dual‐energy
X‐ray absorptiometry (DEXA) was used to quantify bone mineral content and den‐
sity and compare to published reference ranges. The puppy's initial bone mineraliza‐
tion was markedly subnormal, with bone mineral density 66% lower than expected,
and bone mineral content 40% lower than expected. Subsequent DEXA scans were
performed at intervals during the puppy's recovery to document the rate of bone
re‐mineralization and guide therapeutic recommendations. Marked improvement was
achieved within 4 months through exercise control and feeding of a diet appropriately
formulated for large breed puppy growth and development. This report reinforces the
necessity of thorough dietary history and highlights the potential for malnutrition in
pets fed homemade and raw meat‐based diets. Use of DEXA has rarely been reported
in clinical cases, yet can be a valuable tool for diagnosing and monitoring cases with
abnormal bone mineralization. Further studies using DEXA to track bone mineraliza‐
tion in healthy puppies are encouraged to develop a more robust reference range of
bone mineralization in growing dogs of varying sizes, weights and ages.

KEYWORDS
bone, calcium, DEXA, dog, homemade diet, hypovitaminosis, mineralization, vitamin D

1 |  I NTRO D U C TI O N which there is no suitable commercial therapeutic diet (Remillard,

Despite a myriad of readily available commercial diets formulated
to meet the nutritional requirements of growing puppies, many dog
owners elect to prepare their pet's food at home, a trend which ap‐
pears to be increasing (Dodd, Cave, Adolphe, & Verbrugghe, 2018;
Laflamme et al., 2008). Appropriately formulated homemade foods
may convey benefits to pet health and the pet–human relationship,
particularly for patients with nutritionally responsive diseases for
2008). However, there is significant risk of nutrient insufficiencies,
excesses and imbalances in homemade diets. Evidence from veter‐
inary literature suggests that the majority of homemade diets are
not nutritionally sufficient for the animal or life stage for which
they are fed, even those formulated by veterinarians (Larsen, Parks,
Heinze, & Fascetti, 2012; Lauten, Smith, Kirk, Bartges, & Adams,
2005; Stockman, Fascetti, Kass, & Larsen, 2013; Streiff et al.,
2002). Furthermore, there are many case reports of adverse health

J Anim Physiol Anim Nutr. 2021;105(Suppl. 2):29–36. © 2019 Blackwell Verlag GmbH |  29
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30       DODD et al.
conditions attributable to inadequate homemade diets, particularly
in relation to skeletal health (de Fornel‐Thibaud et al., 2007; Kienzle
& Dobenecker, 2012; Verbrugghe et al., 2011).
Little has been published regarding bone mineralization in grow‐
ing dogs, and conventional radiography has been suggested to have
poor sensitivity for detection of changes in bone mineralization
(Kumar et al., 2009; Lauten, Cox, Brawner, & Baker, 2001). The use
of dual‐energy X‐ray absorptiometry (DEXA) has been well estab‐
lished in human medicine and research, and its use for measuring
body composition and bone mineralization in dogs has been vali‐
dated by comparison with chemical analyses (Lauten et al., 2001;
Schneider et al., 2004). Yet, only one account has been published
in which DEXA has been used in an osteopenic case (Taylor, Geiger,
Saker, & Larson, 2009). The objective of this report is to describe a
case of hypovitaminosis D with concurrent calcium and phosphorus
deficiency and imbalance in a puppy fed an unbalanced homemade
diet which included raw meat and to introduce DEXA as an under‐
utilized modality for diagnosing and measuring progress of osteo‐
penic patients.
2 |  C A S E D E S C R I P TI O N
A 4‐month‐old, intact male Old English Sheepdog puppy was pre‐
sented to the Ontario Veterinary College Health Sciences Centre
(OVC HSC) Emergency Service. The puppy was first noted to have
left forelimb lameness 1 month prior to presentation to the OVC
HSC. He had a history of being “clumsy” such as slipping down stairs
and falling off furniture. Notably, he was reported to occasionally
roll onto his dorsum and vocalize during vigorous play. He was seen
by his family veterinarian, radiographs were taken and hip dysplasia
was initially suspected. When the puppy failed to respond to medical
therapy (tramadol and meloxicam, doses unreported) and his signs
progressed to hind limb paresis with occasional episodes of vomit‐
ing and muco‐haemorrhagic diarrhoea, he was presented first to the
client's local emergency veterinarian and then referred to the OVC
HSC emergency service.
On presentation, the puppy's body weight (BW) was 10.9 kg,
and he was bright, alert and responsive. He was reluctant to am‐
bulate; pelvic limb weakness and generalized muscle fascicula‐
tion were observed. His heart and respiratory rate were elevated,
and the remainder of his general physical examination was re‐
portedly unremarkable. A rapid enzyme immunoassay faecal test
for parvovirus antigen [Idexx SNAP ® Parvo] was performed due
to the puppy's history of recent diarrhoea, and the result was
negative. Quick assessment tests performed at the time of pre‐
sentation revealed hypocalcemia 1.36 mmol/L (reference range
2.50–3.00 [University of Guelph Animal Health Laboratory]) but
no other abnormalities. A commercial test for tick‐borne parasite
antibodies [Idexx SNAP ® 4DX®] was performed which yielded
negative results. Blood was collected for a complete blood count
(CBC) and serum biochemistry. Aside from the hypocalcemia
noted, the CBC and biochemistry were unremarkable when the
laboratory reference ranges were adjusted for his age (von Dehn,
2014), save for a mildly elevated creatine kinase (678 U/L, range
31‐255). Orthopedic and neurological examinations showed left
forelimb lameness, shifting bilateral pelvic limb lameness, mild
effusion in the left stifle, spinal pain particularly at the thoraco‐
lumbar and caudal thoracic regions, and pain on palpation of both
stifles. The carpi and tarsi felt irregular in shape, while the wings
of his scapulae had thickened, rounded, irregular margins. When
viewed from above, the puppy stood with a moderately kyphotic
stance. When viewed from the side, the puppy stood with mod‐
erate laxity of the tarsi, standing almost completely plantigrade.
No neurological abnormalities were detected. He was treated
with intravenous (IV) hydromorphone (0.025 mg/kg twice daily
(BID)) and oral meloxicam (0.1 mg/kg once daily (SID)) for pain
relief, as well as metronidazole (7.5 mg/kg slow IV) for anti‐diar‐
rhoea effects.
3 | I N ITI A L D I AG N OS TI C S
Polyarthritis was strongly suspected, and the puppy was transferred
to the OVC HSC Internal Medicine service for further diagnostics.
Sedation was achieved with dexmedetomidine (5 μg/kg IV) and hy‐
dromorphone (0.2 mg/kg IV), and synoviocentesis of both tarsal
joints was performed using aseptic technique. Mixed populations of
cells consistent with inadvertent aspiration of bone marrow, as well
as synovial fluid, were detected in the synovial aspirates. Though
limb radiographs had been performed by the referring veterinarian,
the unexpected joint aspirate results warranted further diagnostic
imaging. Lumbosacral radiographs were obtained, which revealed
marked diffuse osteopenia, irregularity of the caudal aspect of the
right femoral neck and kyphosis of the sacrum with suspected ver‐
tebral fracture. No obvious fractures could be detected, but could
not be ruled out due to the severity of osteopenia (Figure 1). A fen‐
tanyl patch (50 μg/hr) was placed, and oral gabapentin (10 mg/kg
BID) was prescribed for pain relief, in addition to continuation of the
hydromorphone and meloxicam previously described. At this time, a
diet history was collected from the owner. It was only then discov‐
ered that the puppy had been fed a homemade diet since acquisition
from the breeder at 9 weeks of age. The puppy was then referred
to the OVC HSC Clinical Nutrition service for diet evaluation and
nutritional recommendations.
F I G U R E 1   Lumbosacral radiographs revealing marked diffuse
osteopenia in a 4‐month‐old male Old English Sheepdog fed an
unbalanced homemade diet
DODD et al. |
      31

4 | C LI N I C A L N U TR ITI O N E VA LUATI O N

RER = 293 kJ ∗ (BWkg)0.75

After 3 days of hospitalization, the puppy was referred to the clini‐

cal nutrition service. A full nutrition assessment, including collec‐ The resting energy requirement was then multiplied by a daily

tion of a thorough diet history, was performed in accordance with energy requirement (DER) factor of 1.4 to provide additional energy

the World Small Animal Veterinary Association's Global Nutrition for growth and development:

Guidelines (Freeman et al., 2011). The puppy's diet had consisted DER = (293 kJ ∗ (BWkg)0.75 ) ∗ 1.4
mainly of raw and cooked meat with cow and goat dairy products,
as described in a pet food recipe book [Fresh Food and Ancient
For a puppy 4 months of age, the typical DER factor for growth
Wisdom, Dr. Ihor Basko DVM], summarized in Table 1. Upon physi‐
would be 2.0 (Debraekeleer, Gross, & Zicker, 2010), but protocol at
cal examination, the puppy was determined to be in suitable body
the OVC HSC accounts for reduced energy requirements of an an‐
condition scoring 4 out of 9 (WSAVA, 2013a), though he had poor
imal being strictly cage rested. The puppy's body weight was mea‐
muscle condition (WSAVA, 2013b). A nutrition plan was initiated
sured daily to ensure daily weight gain consistent with appropriate
to determine the puppy's energy and nutrient requirements. The
growth over time (Salt et al., 2017).
puppy was maintained on the commercial diet to which he had
At this time, blood was collected by jugular venipuncture and a vi‐
already been transitioned in hospital (Veterinary Diet Canine
tamin D profile was performed which showed mildly elevated ionized
DEVELOPMENT PUPPY LARGE DOG dry puppy food, Royal
calcium (iCa), high normal parathyroid hormone (PTH) and low 25‐hy‐
Canin®), as it was determined to be an appropriate diet for large
droxyvitamin D (25(OH)D) (Table 2). Considering that at the time of
breed puppy growth. Energy requirements while in hospital were
blood collection for the vitamin D profile, the puppy had already been
estimated to be 2,560 kJ/day. This energy requirement estimate
eating the commercial puppy diet in hospital for 36 hr, and these find‐
was determined by calculating resting energy requirements (RER)
ings were considered consistent with dietary calcium, phosphorus
based on metabolic BW:
and vitamin D deficiencies, leading to hyperparathyroidism (HPTH).
Though the puppy's PTH was within the normal reference range, this
does not rule out HPTH as an aetiology for the puppy's clinical signs,
TA B L E 1   Homemade diet fed to a 4‐month‐old male Old as PTH should not be in the high end of the normal reference range
English Sheepdog. This diet was fed from 9 weeks of age to time of
when serum ionized calcium is also high. This can be explained by the
presentation at 16 weeks of age
puppy being fed a calcium‐deficient diet long‐term, with provision of
Ingredient Quantity Frequency a diet replete in calcium for 36 hr prior to sampling. The puppy's PTH
Raw egg 1 Once daily [SID] was elevated to mobilize bone calcium stores in an attempt to main‐

Goat's milk ½ cup SID tain serum calcium levels, and then, when the puppy was then fed the
calcium‐replete diet in hospital, his serum calcium levels would have
Raw ground beef, or ½ cup Three times daily [TID]
improved rapidly. PTH response is slightly slower, and while secretion
Chicken meat, or
was decreasing in response to the normalizing serum calcium, the
Turkey meat, or
levels were still high normal. In a healthy animal, PTH would not be
Lamb meat
expected to be at the high end of the reference range when calcium
Chicken liver ½ cup Every other day
was also high, due to negative feedback mechanisms.
Cottage cheese, or ½ cup Twice daily [BID] In order to determine dietary nutrient imbalances, the nutrient
Goat's milk yoghurt ¼ cup content of the homemade diet was estimated using computer soft‐
Cooked white rice, or ½ cup TID ware [BalanceIT®, Davis Veterinary Medical Consulting Inc], as has
Cooked sweet potato, or been previously reported (Stockman et al., 2013). Nutrient estima‐
Cooked oatmeal tions were made based on ingredient composition available in online
Carrot, or ¼–½ cup BID
Lettuce, or TA B L E 2   Vitamin D profile at presentation and after discharge
Alfalfa sprouts, or in a 4‐month‐old male Old English Sheepdog diagnosed with
nutritional secondary hyperparathyroidism
Broccoli
Dried alfalfa 2 tsp SID Parameter Initiala Day 42 Reference range
a
Cod liver oil 2 tsp SID Ionized Ca 1.47 1.42 1.25–1.45 mmol/L
a ®
Dr. Dobias GreenMin 1/8 tsp SID PTH 5.70 1.20 0.50–5.80 pmol/L
a
Dr. Dobias Soulfood® 1/4 tsp SID 25(OH)D 66 146 109–423 nmol/L
a a
The homemade diet was fed from acquisition at 9 weeks of age to pres‐ At the time of collection for the initial profile, the puppy had been fed
entation at 16 weeks of age, though supplements were added 6 days meals of an appropriate diet for 36 hr.
prior to presentation when the puppy was 15 weeks old. Ca, calcium; PTH, parathyroid hormone; 25(OH)D, 25‐hydroxyvitamin D.
 |
32       DODD et al.

TA B L E 3   Relevant nutrient concentrations calculated for a homemade diet fed to a 4‐month‐old male Old English Sheepdog diagnosed
with nutritional secondary hyperparathyroidism, and comparison to industry recommendations and a commercial diet fed in hospital

Homemade diet
a a
Nutrient/1000 kcal weeks 9–15 week 15 AAFCO NRC RA Commercial diet

Total protein (g) 91 85.8 ≥56.3 56.3 83.9

Ca (g) 0.23 0.33 3.0–4.5 3.0 3.3
P (g) 1.03 0.99 2.5–4.0 2.5 2.5
Ca:P 1:4 1:3 1:1–2:1 1.2:1 1.3:1
Vitamin D (IU) 17.1 1142 125–750 136–800 298
Magnesium (g) 0.13 0.16 ≥0.15 0.1 Unreported
Copper (mg) 0.72 0.72 ≥3.1 2.7 4.3
Iron (mg) 10.9 11.4 ≥22 22 59.8
Manganese (mg) 1.0 1.1 ≥1.8 1.4 20.0
Zinc (mg) 13 11 ≥25 25 56.5
α‐linolenic acid (g) 0.16 0.14 ≥0.2 0.2 0.6
Choline (mg) 321 302 ≥340 340 541
Vitamin E (IU) 2.7 9.4 ≥12.5 11.2 135

Industry recommendations and requirements reported from the Association of American Feed Control Officials (AAFCO, 2018) and the National
Research Council (NRC, 2006).
AAFCO, Association of American Feed Control Officials; Ca, Calcium; NRC, National Research Council; P, Phosphorus; RA, Recommended
Allowance.
a
The homemade diet was fed from acquisition at 9 weeks of age to presentation at 16 weeks of age, though supplements were added 6 days prior to
presentation when the puppy was 15 weeks old.

nutrient databases [Canadian Nutrient File, Government of Canada;
USDA Food Composition Databases, United States Department of
Agriculture] and from the manufacturer of the supplements used [Dr.
Dobias Natural Healing, Dr. Peter Dobias DVM]. Compared to indus‐
try recommendations (AAFCO, 2018; NRC, 2006), the diet was lack‐
ing in many nutrients, the most relevant to his clinical condition being
calcium (Ca), phosphorus (P) and vitamin D (Table 3). It was thus de‐
termined that the dietary deficiencies of Ca and P, an inverse ratio of
Ca to P, and a deficiency of vitamin D were all contributing factors to
nutritional secondary HPTH and the puppy's clinical osteopenic con‐
dition. The puppy was hospitalized for 1 week of strict rest to prevent
pathological fractures and manage pain as previously described.
5 |  D UA L‐ E N E RG Y X‐ R AY
A B S O R P TI O M E TRY
One week after presentation, the puppy was sedated (dexmedetomi‐
dine 5 μg/kg IV and hydromorphone 0.2 mg/kg IV) and underwent
DEXA to quantify bone mineral density (BMD), bone mineral con‐
tent (BMC), both as mass (BMCg) and as percentage of body weight
(BMC%), and total body composition (Figure 2). The results of the
DEXA revealed total body BMC and BMD markedly below normal
reported values. The puppy weighed 11.6 kg, and total body composi‐
tion was measured as 22% fat mass (2.6 kg), 73% lean soft tissue mass
(8.5 kg) and 2.18% BMC (253 g). Total body BMD was measured to
2
be 0.29 g/cm . Comparatively, total body BMC% and BMD in healthy
male puppies have been reported to be 2.40% and approximately 0.4–
0.5 g/cm2 respectively (Booles, Poore, Legrand‐Deferetin, & Burger,
1994; Lorinson, Loebcke, Skalicky, Grampp, & Lorinson, 2008). In
young adult male dogs, healthy BMC% reportedly ranges from 3.55%–
4.01%, while BMD ranges from 0.86–1.08 g/cm2, with larger breed
dogs having higher BMC and BMD than smaller breed dogs (Lauten
et al., 2001). Thus, this puppy's bone mineralization values were below
those reported for healthy dogs of any age or size. Bone mineral con‐
tent and BMD were also measured for particular bones and regions,
and compared to published data (Lorinson et al., 2008; Schneider et al.,
2004). In every region measured, the puppy's BMC and BMD were
markedly lower than the reported healthy mean (Table 4). The puppy
was hospitalized for another week following the results of the DEXA
scan in order to maintain strict cage rest and reduce risk of fractures.
Due to improvement in clinical signs, fentanyl was discontinued 3 days
after the DEXA scan, and hydromorphone discontinued another 24 hr
later. The puppy was discharged 2 weeks after initial presentation
with oral gabapentin (10 mg/kg BID), trazodone (2.27 mg/kg BID) and
meloxicam (0.1 mg/kg SID), and instructions to be strictly confined
until bone density was improved. At discharge, a repeat DEXA scan
was scheduled to be performed in a month's time.
6 | C A S E PRO G R E S S I O N
Four weeks later, 6 weeks after initial presentation, the puppy was
re‐admitted to the OVC HSC for a recheck and repeat DEXA scan.
DODD et al. |
      33

irregular in shape and size. When viewed from above, the puppy
stood with a mild lateral curvature of his spine, and the dorsal cur‐
vature previously seen was no longer evident. When viewed from
the side, the puppy still stood with mild laxity of the tarsi, though
his stance had improved since his last examination 6 weeks prior.
The remainder of his general physical examination was unremark‐
able, and he was sedated (dexmedetomidine 5ug/kg IV and butor‐
phanol 0.1 mg/kg IV) for the DEXA scan. At this time, blood was
also collected by cephalic venipuncture for a vitamin D profile, which
was found to have normalized (Table 2). The DEXA results revealed
a marked improvement from the initial scan. The puppy's total body
composition was 17% fat mass [2.5 kg], 78% lean soft tissue mass
[11.5 kg] and 2.76% BMC [405 g]. Total body BMD was measured
to be 0.50 g/cm2. While there were marked improvements in BMC,

F I G U R E 2   Body composition images from DEXA scan
confirming initial severe osteopenia and showing progressive
mineralization after dietary intervention in a 4‐month‐old male
Old English Sheepdog. From left to right: 1 week post‐treatment,
6 weeks post‐treatment and 14 weeks post‐treatment. The
positioning in the initial scan (left) was conservative to avoid risk
of iatrogenic fractures from tensioning forelimbs into the more
conventional position (middle and right). Lateral deviation of
the spine can be visualized in the last (right) image, which also
demonstrates the challenge of acquiring straight images of patients
with skeletal deformities
At this time, the owner reported marked improvement in the puppy's
demeanour and appetite, though he had experienced an episode of
diarrhoea 1 week previously resulting in early discontinuation of
all medications. The owner reported continued improvement even
in the absence of analgesics, with no lameness detectable. At re‐
presentation, the puppy weighed 14.9 kg and was bright, alert and
responsive. He was energetic, and his general appearance and be‐
haviour were comparable to a normal, healthy puppy of the same
age. On physical examination, the puppy was determined to have
maintained a BCS of 4 out of 9 (WSAVA, 2013a) and had some minor
improvement in muscle condition. No pain or effusion was detected
in any joint, though his carpi, tarsi and scapulae were palpably
BMD and clinical appearance, when compared with published val‐
ues, the BMC and BMD were still moderately decreased (Table 4) so
the owner was advised to begin to cautiously transition the puppy
from strict cage rest to light controlled exercise and was referred to
the OVC HSC Fitness and Rehabilitation service for physiotherapy. A
repeat DEXA scan was scheduled for 6 to 8 weeks later.
The puppy returned to the hospital 8 weeks later, 14 weeks after
initial presentation, for a third DEXA scan. The owner reported
good progress with no discernible pain or lameness, though a gait
abnormality was noted. The owner noted what she believed to be
“spasms” occasionally in one of the puppy's pelvic limbs, mentioning
that the puppy would hold the affected limb up occasionally when
running. No physiotherapy or rehabilitation had been undertaken,
and some behavioural concerns were reported by the owner. The
owner also had some concerns that the puppy was developing a dis‐
taste for the kibble diet he had been discharged with (Veterinary
Diet Canine DEVELOPMENT PUPPY LARGE DOG dry puppy food,
Royal Canin®), reporting that he did not eat all of the food offered
and preferred training treats (dehydrated turkey “jerky,” brand un‐
known). Calculation revealed that the puppy was being offered 100 g
(358 kcal) more kibble than recommended to meet his energy re‐
quirements, as well as the extra treats, despite feeding instructions
given to the owner during their previous visit. At this presentation,
the puppy weighed 21.5 kg and was bright, alert and responsive. On

TA B L E 4   Dual‐energy X‐ray absorptiometry results in a 4‐month‐old male Old English Sheepdog diagnosed with nutritional secondary
hyperparathyroidism, compared to reported data for healthy dogs

BMD (g/cm2) BMC (g) BMC (%)

Age (months) Measured Expected Measured Expected Measured Expected

b a
4 0.29 ± 0.01 0.86 ± 0.04 253 ± 4 405 ± 83 2.19 ± 0.04 3.62 ± 0.18a
5 0.50 ± 0.01 0.71 ± 0.16b 405 ± 7 603 ± 10a,b 2.76 ± 0.04 3.75 ± 0.06a,b
b a,b,c
7 0.68 ± 0.01 0.85 ± 0.09 622 ± 8 628± 180 2.89 ± 0.04 3.66 ± 0.93a,b,c

Bone mineral density (BMD), bone mineral content (BMC) and per cent bone mineral content (%BMC) measured in the puppy as compared with
values extrapolated from literature, ±standard deviation. Age measured in months.
a
Based on adult dogs with similar lean soft tissue mass (±10%) (Lauten et al., 2001; Santarossa, unpublished data).
b
Based on adult dogs with similar body weight (±10%) (Bjørnvad, Nielsen, Hansen, & Nielsen, 2017; Lauten et al., 2001; Santarossa, unpublished
data).
c
Based on Labrador retriever puppies of similar lean soft tissue mass (±10%) (Booles et al., 1994).
 |
34       DODD et al.
physical examination, the puppy was determined to have attained
a BCS of five out of nine (WSAVA, 2013a) but had no further im‐
provements in muscle condition (WSAVA, 2013b). No pain or effu‐
sion was detected in any joint, though his carpi, tarsi and scapulae
retained their irregular shape and size. Palpation and manipulation
of the pelvic limbs was unremarkable, other than the abnormalities
previously noted, and no abnormal muscle or neurological activity
could be elicited. When viewed from above, the puppy still stood
with a mild lateral curvature of his spine. When viewed from the
side, the puppy's tarsal laxity had resolved. The remainder of his
general physical examination was unremarkable, and he was sedated
(dexmedetomidine 5 μg/kg IV and butorphanol 0.1 mg/kg IV) for
the DEXA scan. At this time, further manipulations of the hind limb
joints were performed, though no abnormalities were detected. The
DEXA results revealed further improvement in bone mineralization.
The puppy's total body composition was 22% fat mass [2.5 kg], 73%
lean soft tissue mass [15.0 kg] and 2.90% BMC [620 g]. Total body
2
BMD was measured to be 0.680 g/cm . The total body values at this
time were much closer to the range reported for healthy puppies and
adults, and this was also true of individual regions. The owner was
advised that the puppy could exercise as appropriate for a healthy
puppy of that age, and physiotherapy was again recommended in
order to improve his muscle condition. When the puppy's growth
was compared to standard growth curves (Salt et al., 2017), it was
determined that he had been gaining body weight quicker than de‐
sired since the last measurement. The owner was advised to feed
only the recommended amount of food and to decrease the number
of treats given so as not to exceed his daily caloric requirements. A
repeat examination and DEXA was recommended at 1 year of age;
however, the owner declined any further investigation at that time.
7 |  D I S CU S S I O N
This report describes a case of nutritional secondary HPTH due to
hypovitaminosis D and calcium deficiency, a condition which has
been uncommon since the introduction of complete and balanced
commercial diets to the commercial market (de Fornel‐Thibaud et al.,
2007; Tal, MacKenzi, Parr, & Verbrugghe, 2018; Taylor et al., 2009;
Verbrugghe et al., 2011). Calcium homoeostasis is tightly regulated
by PTH and 1,25‐dihydroxyvitamin D (1,25(OH)2D), among others,
thus the relationship between these hormones must be born in mind
when considering abnormalities in dietary intake and/or skeletal
mineralization (Hazewinkel & Tryfonidou, 2002). Circulating levels
of Ca are kept within a narrow biological range, with the skeleton
acting as a store of Ca which can be drawn upon when plasma Ca
cannot be maintained by dietary intake (Hazewinkel & Tryfonidou,
2002). In response to decreased circulating Ca, PTH upregulates me‐
tabolism of vitamin D to the active metabolite 1,25(OH)2D, stimu‐
lating increased intestinal absorption of Ca and P, decreased renal
excretion of Ca and P, and increased osteoclast activity to release Ca
and P from mineralized bone (Hazewinkel & Tryfonidou, 2002). The
blood sample from which the iCa, PTH and 25(OH)D were measured
was collected after the puppy had already been fed a diet replete in
vitamin D, Ca and P. Given the short half‐lives and rapid response of
PTH and 1,25(OH)2D to changes in circulating Ca, these hormones
would already have begun to normalize and re‐instate appropriate
Ca homoeostasis prior to sample collection. Thus, the mild elevation
in plasma iCa in the presence of high normal PTH and low 25(OH)
D was suggestive of nutritional secondary HPTH due to hypovita‐
minosis D, despite the PTH value lying within the reference range,
as high iCa with concurrent high PTH is inappropriate. The diagno‐
sis was further supported by plasma 25(OH)D which was still mark‐
edly below reference range, even in the face of adequate dietary
provision for approximately 36 hours prior to sample collection.
Furthermore, at the time of presentation, initial laboratory analyses
which revealed hypocalcemia (1.36 mmol/L, reference range 2.50–
3.00 [University of Guelph Animal Health Laboratory]) and clinical
signs consistent with hypocalcemia, such as muscle fasciculation,
weakness and tachycardia (McKelvey & Post, 1983).
In this puppy, the suspected HPTH, supported by the marked
dietary deficiencies of essential nutrients including Ca, P and vi‐
tamin D, was confirmed when the puppy responded appropriately
with feeding of a complete and balanced puppy diet. While knowl‐
edge of the effects of HPTH on the developing skeleton are well
documented, there has been little research performed which has
quantified bone mineralization at diagnosis and during recovery.
Additionally, while normal values have been published for adult dogs
of varying sex, age and body weight (Lauten et al., 2001; Lorinson
et al., 2008; Schneider et al., 2004), only one study has documented
BMC in growing puppies (Booles et al., 1994). Radiographic evalua‐
tion of osteopenia is subjective and has poor sensitivity, so DEXA
was employed in order to quantifiably measure bone mineralization.
This case thus presented the opportunity to measure bone mineral‐
ization in an osteopenic puppy and quantifiably track progress.
In studies which have examined the effects of signalment on
BMC and BMD, it has been found that size, both in terms of body
weight and bone length, sex and lean soft tissue mass were the
strongest determinants of BMC, while size, sex and age were sig‐
nificantly correlated with BMD (Lorinson et al., 2008). Therefore, in
order to compare the puppy's BMC and BMD to appropriate animals,
values for males of the same size and lean soft tissue mass were used
for BMC evaluation and males of the same size and age were used
for BMD evaluation.
As BMCg is proportional to the size of the bone being measured,
a secondary measure is the percentage of total body weight from
bone mineral, BMC%, which may be more comparable between
animals. The puppy's initial results revealed BMCg 38% below ex‐
pected, BMC% 40% below expected and BMD 55%–66% below
expected, when compared with male dogs of comparable age, size
and/or lean soft tissue mass. Bone mineral content, measured as
mass, appeared to normalize most rapidly, with BMCg achieving
99% of expected within 12 weeks eating a diet replete in Ca, P and
vitamin D. In that same time, BMD more than doubled, attaining
80% of expected, while BMC% reached 78% of expected (Table 4).
These BMD and BMC% still appear to be quite low when compared
DODD et al.
to previous research which has reported normal BMC% between
3%–4% regardless of breed or body size (Lauten et al., 2001).
Others, however, have reported BMD of dogs less than 1 year
between 0.5–0.8 g/cm2 (Lorinson et al., 2008; McMillan, Griffon,
Marks, & Mauldin, 2006). Furthermore, considering the very large
range of reported values, it is likely that within 12 weeks of eating
an appropriate diet this puppy achieved bone mineralization close
to or within normal limits. Similar recovery timelines have been pre‐
viously reported (McMillan et al., 2006; Taylor et al., 2009).
8 | CO N C LU S I O N
With the increase in unconventional feeding practices, including
homemade and raw meat‐based diets, practitioners must be pre‐
pared to diagnose and treat nutritionally associated diseases more
frequently. Thorough dietary histories should be collected as part
of a nutritional evaluation of every patient at every consultation. In
patients with suspected osteopenia, DEXA is a rapid, non‐invasive
method of quantifying bone mineralization which can be used for di‐
agnosis as well as monitoring response to therapy. Further research
to better define normal reference ranges for BMC and BMD in grow‐
ing dogs is strongly encouraged.
AC K N OW L E D G E M E N T S
The authors would like to thank Amanda Santarossa MSc, for provid‐
ing data in which normal bone mineralization in healthy dogs was
measured—Table 4.
C O N FL I C T O F I N T E R E S T
S. Dodd: is engaged in research at the Ontario Veterinary College
funded in part by industry sponsors, has engaged in consultancy
with pet food companies and has received research grants and in‐
ternships in association with pet food companies. C. Grant: This au‐
thor discloses no conflict of interest. M. Barry: This author discloses
no conflict of interest. A. Verbrugghe: is the Royal Canin Veterinary
Diets endowed Chair in Canine and Feline Clinical Nutrition at the
Ontario Veterinary College, serves on industry‐related scientific ad‐
visory boards and has received research grants and speaker fees in
association with pet food companies.
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A. Abnormal bone mineralization in a puppy fed an imbalanced
raw meat homemade diet diagnosed and monitored using
dual‐energy X‐ray absorptiometry. J Anim Physiol Anim Nutr.
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