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DOI: 10.1002/vms3.

619

ORIGINAL ARTICLE

The cat as a small dog?—Comparison of trabecular and cortical


bone microarchitecture of radius and ulna in cats and small
dogs using microcomputed tomography

Franziska Planner Franziska Feichtner Andrea Meyer-Lindenberg

Clinic for Small Animal Surgery and


Reproduction, Ludwig-Maximilians-University, Abstract
Munich, Germany
The forearms of dogs and cats do not only differ anatomically from each other, but
Correspondence there are also differences in prevalence of radius and ulna fractures between the two
Franziska Planner, Clinic for Small Ani-
species. The prevalence of antebrachial fractures is 18.0% in dogs and 2.0–8.0% in cats.
mal Surgery and Reproduction, Ludwig-
Maximilians-University, Veterinärstr 13, Many studies focus solely on the trabecular and cortical bone structure of dogs and the
80539 Munich, Germany.
characteristics of the cat are often disregarded.
Email:
[email protected] The aim of this study was to evaluate the trabecular structure parameters [bone vol-
ume fraction per total volume (BV/TV), bone surface per total volume (BS/BV), trabecu-
lar number (Tb.N), trabecular thickness (Tb.Th), trabecular separation (Tb.Sp), connec-
tivity density (Conn. D), degree of anisotropy (DA)] and the diaphyseal cortical bone
density (Mean Density) of the antebrachium in cats and small dogs to visualise their
differences.
For this purpose, a total of 32 forearms of cats (n = 8) and small dogs (n = 8) were eval-
uated using microcomputed tomography and the findings were compared.
The results of the study showed that cats had higher values for BV/TV, Tb.Th, Tb.Sp,
DA and Mean Density and lower values for BS/BV, Tb.N and Conn.D at radius and ulna
compared to dogs.
According to the results of this study, the higher bone volume fraction (BV/TV), thicker
trabeculae (Tb.Th), increased anisotropy (DA) and significantly higher diaphyseal cor-
tical density (Mean Density) could contribute to the lower fracture risk of the ante-
brachium in cats compared to small dogs.

KEYWORDS
canine, distal radius fracture, feline, microcomputed tomography, morphometrical analysis

This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided
the original work is properly cited.
© 2021 The Authors. Veterinary Medicine and Science published by John Wiley & Sons Ltd.

Vet Med Sci. 2021;7:2113–2119. wileyonlinelibrary.com/journal/vms3 2113


2114 PLANNER ET AL.

1 INTRODUCTION The forearm bones used in this study were obtained from dogs
and cats that died or were euthanised for various reasons. Diseases
In some veterinary studies, the term carnivores is often used, with no of the musculoskeletal system that could possibly influence the study
distinction made between dogs and cats. Many anatomical and clinical were radiologically excluded. The carcasses were frozen at –21◦ C after
studies focus solely on dogs (Scott & McLaughlin, 2008). The character- euthanasia of the animals. For examination the animals were thawed at
istic features of the cats are disregarded and they are often treated as room temperature. Radius and ulna were disarticulated at the elbow
small dogs (Scott & McLaughlin, 2008). joint and the skin, surrounding muscles and ligaments were dissected
Anatomical peculiarities of cats compared to dogs can also be ver- down to the carpus. The antebrachial bones were preserved in 4.0%
ified on the antebrachial bones (Chandler & Beale, 2002). The feline formalin for a maximum of 1 week until further microcomputed tomo-
round Fovea capitis radii differs from the broader, dorsally retracted graphic measurements.
fovea of the dog. The Tuberositas radii can only be recognised as a rough
elevation in the dog. The radial shaft, Corpus radii, is almost smooth in 2.2 Microcomputed tomographic measurements
cats, but in dogs the contact surface to the ulna is rough (Nickel et al.,
1987). Proximal to the Facies articularis carpea is the Crista transversa, For the microcomputed tomographic scans, the forearm bones were
which unfolds as a prominent groin in cats and a transverse bulge in placed on a self-made polystyrene piece with the help of a specially
dogs (Nickel et al., 1987). The Ulna is distally more tapered in the dog manufactured plastic half-shell in the gantry of the device and fixed
than in the cat. The Tuber olecrani appears triangular in the dog and with adhesive tape, with the palmar side of the antebrachii facing
round in the cat. The Incisura trochlearis is divided by a sagittal crest into upwards.
a larger lateral and a smaller medial part only in dogs (König & Liebich, The samples were then scanned by microcomputed tomography
2001; Nickel et al., 1987; Vollmerhaus et al., 1994). (XtremeCT II: Scanco Medical, Zurich, Switzerland). The scan area
In addition, the two animal species differ in the movement of the included radius, ulna and the carpal bones. For this study, a tube volt-
radioulnar joint. Only the cat is able to actively perform considerable age of 68 kV, a voxel size of 30.3 µm, an integration time of 200 ms and
supination movements. In dogs, the rotation of the forearm can only be 1000 projections/180◦ were chosen.
passive (Roos et al., 1992).
Differences between the two species can also be established within
2.3 Microcomputed tomographic evaluation
radius and ulna fractures. In cats, these can be recorded with a preva-
lence of 2.0–8.0% (Harari, 2002). In dogs, antebrachial fractures are
The µCT Evaluation Program V6.6 (Scanco Medical, Zurich, Switzer-
the third most common limb fractures, with a prevalence of 18.0%
land) was used to evaluate the trabecular and cortical bone structure
(Boudrieau, 2003; Harasen, 2003).
of radius and ulna.
The main causes of forearm fractures in dogs and cats are falls from
Trabecular bone can be located in the proximal and distal epi- and
great heights and road traffic accidents (Harasen, 2003; Meyer, 1977;
metaphysis of the radius and ulna. At these four locations, proximal
Wetscher, 2012). Further causes in both species are other direct trau-
ulna, proximal radius, distal ulna, and distal radius, the mean 20.0%
matic events, such as bite wounds, getting stuck, kicks and entrapment
of the entire cancellous area was limited and defined as cylindrical
(Harasen, 2003; Meyer, 1977; Wetscher, 2012).
Regions of Interest (ROIs) (Figure 1). The beginning and the end of
While various studies have focused on trabecular structural analysis
the cancellous region were chosen so that at least 50.0% of trabecular
at different locations in dogs (Bagi et al., 2011; Fitzpatrick et al., 2016;
structures were visible in the cross-section of the bone. The diameter
Hu et al., 2002; Lau et al., 2013; Scherzer et al., 2009), studies on trabec-
of the cylindrical ROIs was adjusted, as shown in Figure 2, to include as
ular bone formation in feline bones are very limited (Boyd et al., 2005).
much cancellous bone as possible, but not the cortex.
Comparative studies of feline and canine structural bone architecture
In addition, the entire diaphysis was evaluated for cortical density.
are not found in the current literature.
The beginning and the end were defined in such a way that a maximum
Therefore, in the present study the trabecular structural parameters
of three trabecular connections were still visible in the cross-section of
and diaphyseal cortical bone density of the antebrachium of cats and
the bone in the medullary cavity. Finally, the diaphysis was divided into
small dogs are assessed by microcomputed tomography and the differ-
three parts: distal, middle and proximal third, where cylindrical ROIs
ences between these animal species are presented, with regard to the
were located (Figure 3).
different fracture prevalence.
Thresholds for cancellous bone and diaphyseal cortex were deter-
mined at each location for each group by two independent observers
2 MATERIALS AND METHOD
using a mean value. The thresholds were used to evaluate trabecu-
lar structural parameters [bone volume fraction BV/TV (%), bone sur-
2.1 Experimental model
face to volume ratio of bone BS/BV (mm–1 ), trabecular number Tb.N
(mm–1 ), trabecular thickness Tb.Th (mm), trabecular separation Tb.Sp
The experiment was approved by the Animal Ethics committee of
(mm), Connectivity-Density Conn. D (mm–3 ), Degree of Anisotropy DA]
the Faculty of Veterinary Medicine, Ludwig-Maximilians-University,
and the diaphyseal Mean Density (mg HA/ccm).
Munich, Germany.
PLANNER ET AL. 2115

F I G U R E 1 Presentation of the cylindrical Region of Interest (ROI)


for the measurement of trabecular bone structure, exemplarily shown
in the distal radius of a cat. First, the trabecular region was visually
limited so that at the beginning and end at least 50.0% of the
trabecular network was still visible in the bone cross-section
(trabecular area). Subsequently, the mean 20.0% was determined as
the length for the cylindrical ROI

F I G U R E 3 Presentation of the cylindrical Regions of Interest


(ROIs) for measurement in diaphyseal bone: proximal cortical ulna,
proximal cortical radius, middle cortical ulna, middle cortical radius,
distal cortical ulna and distal cortical radius. Each ROI corresponds to
F I G U R E 2 Presentation of the diameter of the cylindrical Regions one third of the diaphysis of the bones
of Interest (ROIs) in the distal trabecular bone of a cat. A circle at the
ulna or an oval at the radius was adapted, which included as much
cancellous bone as possible in diameter without including the cortex
3 RESULTS

2.4 Statistics For the aim of the present study, a total of 32 forearms of deceased or
euthanised cats and dogs were examined by microcomputed tomogra-
The statistical analysis and graphic presentation were performed using phy. The different animal species were divided into two groups. One
IBM SPSS Statistic 26.0 (IBM Corp., Armonk, NY, USA). group contained eight cats from 1.7 to 6.2 kg, including five European
First, a Shapiro–Wilk and Kolmogorov–Smirnov tests were per- Shorthair, one European Longhair, one British Shorthair and one Maine
formed to test for normal distribution. Coon. The second group contained three Poodles, two Terrier mon-
Subsequently, all values of the descriptive statistics were deter- grels, one Terrier-Dachshund mongrel, one Dachshund mongrel and
mined. The normally distributed data of the two groups were compared one Dachshund weighing 5.8–10.0 kg. In both groups, only adult ani-
for each structure parameter and each location using a t-test. For non- mals were included and the gender distribution was balanced in order
normally distributed data, a Mann–Whitney U-test was applied. to avoid differences due to age, sex or neutering.
Significant differences were assumed from a probability of error of When comparing the mean values from the descriptive statistics of
p < 0.05. the bone volume fraction (BV/TV) in the trabecular bone of dogs and
2116 PLANNER ET AL.

TA B L E 1 Mean values and standard deviation of bone parameters per localisation and group

Dogs Cats
BV/TV (%) Distal ulna 36.98 ± 9.62 45.79 ± 20.95
Distal radius 39.65 ± 8.53 42.86 ± 14.12
Proximal ulna 37.30 ± 6.42 40.85 ± 17.76
Proximal radius 43.54 ± 6.37 44.41 ± 3.52
BS/BV (mm ) –1
Distal ulna*
15.10 ± 3.28 9.79 ± 4.46
Distal radius 13.37 ± 2.30 9.76 ± 5.36
Proximal ulna* 12.21 ± 2.53 9.91 ± 5.10
Proximal radius *
11.58 ± 1.70 9.30 ± 3.95
Tb.N (mm–1 ) Distal ulna* 2.65 ± 0.17 1.85 ± 0.30
Distal radius *
2.33 ± 0.23 1.88 ± 0.63
Proximal ulna* 2.52 ± 0.26 1.90 ± 0.46
Proximal radius *
2.48 ± 0.22 1.81 ± 0.38
Tb.Th (mm) Distal ulna*
0.14 ± 0.03 0.25 ± 0.12
Distal radius 0.17 ± 0.04 0.31 ± 0.36
Proximal ulna* 0.15 ± 0.02 0.21 ± 0.07
Proximal radius 0.18 ± 0.02 0.26 ± 0.13
Tb.Sp (mm) Distal ulna 0.24 ± 0.05 0.31 ± 0.16
Distal radius 0.26 ± 0.05 0.39 ± 0.30
Proximal ulna 0.25 ± 0.05 0.36 ± 0.23
Proximal radius *
0.23 ± 0.04 0.31 ± 0.08
Conn.D (mm–3 ) Distal ulna* 20.73 ± 5.66 6.75 ± 4.06
Distal radius* 11.90 ± 3.39 8.14 ± 6.23
Proximal ulna *
17.19 ± 4.01 6.23 ± 3.53
Proximal radius* 15.37 ± 3.27 7.901± 5.90
DA Distal ulna*
1.61 ± 0.24 1.84 ± 0.23
Distal radius 1.83 ± 0.22 2.13 ± 0.57
Proximal ulna* 1.33 ± 0.09 1.98 ± 0.33
Proximal radius *
1.69 ± 0.07 2.16 ± 0.39
Mean density (mg HA/ccm) Distal cortical ulna* 1150.53 ± 38.16 1226.48 ± 74.71
Middle cortical ulna* 1182.69 ± 29.41 1249.11 ± 68.07
Proximal cortical ulna *
1190.40 ± 22.23 1259.34 ± 58.64
Distal cortical radius* 1211.12 ± 27.50 1250.19 ± 67.98
Middle cortical radius *
1208.79 ± 39.56 1269.69 ± 58.64
Proximal cortical radius* 1200.60 ± 28.75 1272.90 ± 59.90

*p < 0.05.

cats, it became apparent that the cats showed higher mean values than (p = 0.026), proximal ulna (p = 0.000) and proximal radius (p = 0.000),
the dogs at all four locations (Table 1). for Tb.Th at the distal (p = 0.001) and proximal ulna (p = 0.008) and for
An opposite pattern was observed when comparing the ratio of tra- Tb.Sp at the proximal radius (p = 0.001).
becular bone surface area (BS) to trabecular bone volume (BV). For The connectivity (Conn.D) of trabecular bone was lower in cats than
BS/BV lower mean values were observed at all locations for cats com- in dogs (Table 1). This was confirmed at all locations (distal ulna with
pared to small dogs, with p-values of 0.001 at the distal ulna, 0.003 at p = 0.000, distal radius with p = 0.042, proximal ulna with p = 0.000,
the proximal ulna and 0.042 at the proximal radius. The cats had fewer proximal radius with p = 0.001).
and thicker trabeculae (Tb.N, Tb.Th) with greater trabecular separation When comparing the anisotropy (DA) of the trabecu-
(Tb.Sp) than dogs at all locations (Table 1 and Figure 4a, b). These results lar bones, higher values were found in cats than in dogs
were obtained for Tb.N at the distal ulna (p = 0.000), distal radius at all locations (Table 1), with p = 0.013 at the distal ulna,
PLANNER ET AL. 2117

F I G U R E 4 Trabecular bone architecture at the distal radius of a representative dog (a) and a representative cat (b). The dog shows significantly
more and thinner trabeculae compared to the cat

p = 0.000 at the proximal ulna and p = 0.000 at the proximal could favour an increased antebrachial fracture risk of dogs over cats.
radius. In the literature, it has been reported that BV/TV can partially predict
The two groups showed distinctions in the Mean Density of the the mechanical properties of a bone (Pothuaud et al., 2002). The lower
diaphysis (Table 1). In the cats, a denser cortex was visible in all six the bone volume fraction, the higher the risk of fracture, because this
investigated locations compared to the dogs (distal cortical ulna with bone parameter has a high correlation with the mechanical failure load
p = 0.001, middle cortical ulna with p = 0.024, proximal cortical ulna of a bone (Arlot et al., 2008; Ding et al., 2002). Other canine micro-
with p = 0.000, distal cortical radius with p = 0.000, middle cortical computed tomographic studies investigated trabecular bone parame-
radius with p = 0.001 and proximal cortical radius with p = 0.000). ters in the Processus coronoideus medialis ulnae (Fitzpatrick et al., 2016;
Lau et al., 2013) to visualise changes in subchondral bone in MCD
(medial coronoid disease)-positive dogs or in the Caput ossis femoris
4 DISCUSSION (Scherzer et al., 2009) to identify changes in dogs with Legg Calve
Perthes disease. Lau et al. (2013) found almost similar BV/TV values
In the present study, cortical bone density and trabecular microarchi- in the proximal ulna in both healthy and MCD dogs as in the present
tecture of the radius and ulna in dogs and cats were examined compar- study. Scherzer et al. (2009) presented higher values of BV/TV at the
atively. femoral head of dogs compared to BV/TV of dogs in this study at the
It was possible to show the cortical and trabecular differences forearm. This deviation could be explained by the different location
between the canine and feline antebrachium, as well as possible rea- of the femoral head versus forearm bones and their different loads.
sons for the clearly lower prevalence of radius and ulna fractures in With regard to cats, only one comparative study (Boyd et al., 2005)
cats (Boudrieau, 2003; Harari, 2002; Harasen, 2003; Nolte et al., 2005). was found in the literature, which examined the changes in the feline
The risk of fracture is determined by bone density (Eckstein et al., 2004; proximal tibia after cranial cruciate ligament rupture using microcom-
Lochmüller et al., 2002; Lochmüller et al., 2008) and its trabecular net- puted tomography. Boyd et al. (2005) detected lower values for BV/TV
work (Arlot et al., 2008; Baum et al., 2013; Ding et al., 2002; Drews compared to the results of the cats in the present study. The difference
et al., 2008; Legrand et al., 2000; Müller et al., 2004; Pothuaud et al., between the two studies within the cats could also be explained by the
2002). different measurement localisations of tibia versus forearm bones, as
It should be noted that the purpose of the study was to advance these bones are also exposed to different loads.
scientific knowledge, not to develop the clinical management of ante- For the ratio of the trabecular surface area to the volume of tra-
brachial fractures. becular bone (BS/BV) contradictory results compared to BV/TV were
When comparing the trabecular structure parameter BV/TV of the obtained. According to this, the values of dogs for BS/BV at all locations
two animal species in the present study, it was found that the bone vol- were mostly significantly higher than those of cats. This behaviour
ume fraction of the dogs was lower compared to the cats. This result for trabecular surface density values can be explained by the other
2118 PLANNER ET AL.

structural parameters. The high number of trabeculae in dogs resulted within the cat studies, Boyd et al. (2005) found clearly higher values
in a high value for BS/BV at low BV/TV (Scherzer et al., 2009). for anisotropy at the feline tibia than in the present study at the feline
In the present study, cats showed fewer trabeculae (Tb.N), mostly antebrachium. Again, the reason could be the different locations of the
with a greater separation (Tb.Sp) than dogs; however, they were sig- measurements, stress on the bones or osseous pathology.
nificantly thicker (Tb.Th). This could lead to the conclusion that cats In addition to trabecular bone parameters, diaphyseal cortical den-
have more stable forearm bones at the evaluated localisations than sity (Mean Density) was also analysed in the present study, which was
dogs with regard to trabecular thickness. According to the study by significantly higher in cats than in dogs. Thus, it can be assumed that
Ding et al. (2002), trabecular thickness also has a high correlation with the cortical diaphysis of the investigated antebrachial bones of the cats
the mechanical failure load and to existing osseous microdamage (Arlot showed a higher stability.
et al., 2008). When comparing the values for Tb.Th at the radius and In the literature, the prevalence of radius and ulna fractures in cats
ulna of the dogs in the present study with the studies of Lau et al. (2013) is described as 2.0–8.0% (Harari, 2002; Nolte et al., 2005), which is
and Fitzpatrick et al. (2016) at the Processus coronoideus medialis ulnae clearly lower than the prevalence in dogs at 18.0% (Boudrieau, 2003).
and Scherzer et al. (2009) at the Caput ossis femoris, they settled in com- The lower risk of fracture in cats could therefore be due to higher bone
parable areas. For the structural parameter Tb.Sp in the present study, volume fraction (BV/TV), thicker trabeculae (Tb.Th), higher anisotropy
similar mean values were recorded for the dogs as in the elbow studies (DA) and significantly higher diaphyseal cortical density (Mean Den-
of Lau et al. (2013) and Fitzpatrick et al. (2016). Scherzer et al. (2009) sity).
determined lower values for Tb.Sp in the canine femur. This deviation In general, the differences in trabecular and cortical structure of the
could be explained by the different locations of the microcomputed antebrachium between dogs and cats should not be ignored. Based on
tomographic evaluations and the different stress on the bones. A fur- these results the cat should not be seen as a small dog.
ther reason for differing values could be the remodelling processes of
the bones while aging. In the present study, mainly old dogs were anal- ACKNOWLEDGEMENTS
ysed, whereas in the other studies young dogs between 15 weeks and 3 The authors would like to thank the research team at the Faculty of Vet-
years were examined (Fitzpatrick et al., 2016; Lau et al., 2013; Scherzer erinary Medicine, Ludwig-Maximilians-University, Munich, who sup-
et al., 2009). Body weight could also have an influence on the struc- ported and guided the author on how to operate with the µCT. Pascal
tural parameters, whereby in the present study only dogs below 10.0 kg Bawidamann is acknowledged for his advice during data analysis.
were measured, while the other studies primarily included heavier Open Access funding enabled and organized by Projekt DEAL.
dogs between 18 and 23 kg (Fitzpatrick et al., 2016; Lau et al., 2013;
Scherzer et al., 2009). When comparing the feline results of radius and CONFLICT OF INTEREST
ulna of the present study with those from the feline tibia, Boyd et al. The authors declare that they have no conflict of interest.
(2005) detected higher values for Tb.N and Tb.Sp and lower values for
Tb.Th. Again, this could be explained by the different locations of the COMPLIANCE WITH ETHICAL STANDARDS
measurements and the load on the bones. In the study by Boyd et al. The experiment was approved by the Animal Ethics Committee of
(2005) cats suffered from a cruciate ligament rupture with consequent the Faculty of Veterinary Medicine, Ludwig-Maximilians-University,
bone pathology. Munich, Germany.
In the present study, higher connectivity was observed in the exam-
ined bones of dogs than those of cats. This could be due to the fact DATA AVAILABILITY STATEMENT
that dogs had more trabeculae, which were therefore better connected The data that support the findings of this study are available from the
than the few thick trabeculae of cats. corresponding author upon reasonable request.
Scherzer et al. (2009) reported similar results for Conn.D in their
measurements in the canine femoral head compared to the results of PEER REVIEW
the dogs in the radius and ulna in the present study. The connectivity The peer review history for this article is available at https://publons.
of the feline tibia in the study by Boyd et al. (2005) was clearly higher com/publon/10.1002/vms3.619
than the results of the present study at the feline forearm, which again
could be explained by the different locations of the tibia versus radius AUTHOR CONTRIBUTION
and ulna, the different load on the bones or the comparison of healthy Franziska Planner: Conceptualisation, data curation, formal analysis,
cats versus cats with torn cruciate ligaments. investigation, methodology, validation, visualisation, writing – original
In the studies by Legrand et al. (2000), Ding et al. (2002) and Drews draft, writing – review & editing.
et al. (2008), the degree of anisotropy showed a negative correlation Franziska Feichtner: Conceptualisation, data curation, formal anal-
with trabecular bone fragility. In the present study, this value was sig- ysis, project administration, supervision, methodology, validation, visu-
nificantly higher in cats than in dogs. This could therefore indicate for alisation, writing – original draft, writing – review & editing.
more stable forearm bones in cats. In the study by Hu et al. (2002), the Andrea Meyer-Lindenberg: Conceptualisation, project administra-
anisotropy of dogs at lumbar vertebrae was comparable to the values tion, resources, supervision, methodology, validation, visualisation,
of dogs at the radius and ulna in the present study. In the comparison writing – original draft, writing – review & editing.
PLANNER ET AL. 2119

ORCID Legrand, E., Chappard, D., Pascaretti, C., Duquenne, M., Krebs, S., Rohmer,
Franziska Planner https://orcid.org/0000-0003-0922-3262 V., Basle, M. F., & Audran, M. (2000). Trabecular bone microarchitecture,
bone mineral density, and vertebral fractures in male osteoporosis. Jour-
nal of Bone and Mineral Research, 15(1), 13–19.
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