Received: 15 November 2020 Revised: 30 January 2021 Accepted: 9 February 2021

DOI: 10.1111/vru.12973

O R I G I N A L I N V E S T I G AT I O N

Vertebral heart score to evaluate cardiac size in thoracic

radiographs of 124 healthy rats (Rattus norvegicus)

Sara Dias1,3 Carlo Anselmi1 Yvonne Espada2 Jaume Martorell2

1
Hospital Clínic Veterinari – UAB, Bellaterra,
Barcelona, Spain Abstract
2
Departament de Medicina i Cirurgia Animals, Dilated cardiomyopathy is a relatively common disease in pet rats (Rattus norvegicus);
Universitat Autònoma de Barcelona,
however, there is a lack of radiographic references for the normal cardiac size in this
Bellaterra, Barcelona, Spain
3
Present address: Sara Dias, Pride Veterinary
species. The aim of this prospective, anatomical and reference interval study was to
Centre - Referral Hospital and Nottingham establish quantitative radiographic reference range measurements for the vertebral
University, UK
heart score (VHS) in rats. Right lateral (RL), ventrodorsal (VD), and dorsoventral (DV)
Correspondence radiographs of clinically healthy rats (n = 124) were evaluated. Measurements were
Sara Dias, Hospital Clínic Veterinari – UAB,
performed by 2 expert readers who were unaware of signalment data. The mean values
Bellaterra, Barcelona, Spain.
Email: saracorreiadias@gmail.com and references intervals of VHS were 7.7 and 7.0–8.5 for the RL, 7.5 and 6.6–8.6 for the
VD, and 7.9 and 6.9–9.0 for the DV, with VHS values greater in males than in females.
This article has been written accordingly to
STROBE-Vet guidelines. The measurements reported in this study can be used by the clinician as an objective
Previous presentations or publications dis- tool to evaluate cardiac size in rats, in order to improve the diagnosis and treatment of
closure: This study has not been previously
cardiac diseases.
presented or published.

KEYWORDS
cardiomyopathy, radiography, rats, thorax, VHS

1 INTRODUCTION
Rats (Rattus norvegicus) are popular companion animals due to their
small size, easy maintenance and husbandry, inquisitive nature, good
temperament, and intelligence. Cardiac disease is emergent among
several small exotic mammals such as ferrets,1 rabbits,2 African
hedgehogs,3 and rats.4,5
Cardiac disorders require prompt and accurate diagnosis and treat-
ment, and diagnostic imaging is one of the most important tools to aid
in the diagnosis.6 In small rodents, thoracic radiographs are easier to
perform than echocardiography due to small patient body size, high
heart rate, need for dedicated ultrasonographic probes and software,
and operator experience. Moreover, radiographs are more cost effec-
tive and available than cardiac ultrasonography.
The vertebral heart score (VHS) system was created to measure
the cardiac silhouette in a more objective way. The VHS was first
established for use in dogs,7 and this tool of assessment has been
extrapolated and validated in other companion animals, including
cats,8 ferrets,9,10 rabbits,11–13 chinchillas,14 African hedgehogs,3
prairie dogs,15 black-rumped agoutis,16 and in fruit bats.17 No studies
have been published to data establishing the normal reference range
of the VHS in rats, resulting in a clinician relying on experience and a
subjective assessment of cardiac structures. An objective measure-
ment of heart size may aid in an earlier and more accurate diagnosis
of cardiac disease, and more facilitate improved monitoring of disease
progression.
The aim of this study was to determine standard cardiac dimen-
sions in healthy rats using a standardized VHS measurement on right

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medium, provided the original work is properly cited, the use is non-commercial and no modifications or adaptations are made.
© 2021 The Authors. Veterinary Radiology & Ultrasound published by Wiley Periodicals LLC on behalf of American College of Veterinary Radiology

394 wileyonlinelibrary.com/journal/vru Vet Radiol Ultrasound. 2021;62:394–401.

DIAS ET AL .
lateral (RL), ventrodorsal (VD) and dorsoventral (DV) radiographic
projections.
2 MATERIALS AND METHODS
2.1 Ethics statement
This research project was approved by the Ethical Committee of Ani-
mal and Human Experimentation of the Autonomous University of
Barcelona, Spain (authorization number: CEEAH 3520), being a part of
a larger study for a doctoral thesis. The study was conducted in accor-
dance with the guidelines of the Spanish Government (RD 1201/05)
and the European Union (Directive 86/609/EEC) on the protection of
animals used for scientific purposes.
2.2 Animals
One hundred twenty-four adult intact Sprague-Dawley rats (Rattus
norvegicus) were obtained from an authorized research animal breeder
(Charles River, Italy, Calco).
Rats were housed in the Exotic Animal Care Unit of the Hospital
Clínic Veterinari of the Universitat Autònoma de Barcelona (Spain), in
groups of four to six animals (of the same sex), at 50%–60% humid-
ity, 20◦ C–21◦ C temperature, and 12-h-light and 12-h-dark cycle. Rats
were fed a commercial diet (Oxbow Essentials adult rat food, Oxbow
Animal Health, Murdock, USA), with free access to vegetables, fruits,
and water. A physical examination was performed daily on each rat for
the duration of the study. All the husbandry and physical examination
were assessed by an ECZM – certified zoological medicine specialist in
small mammals (SD).
Based on a complete physical examination and the report from the
authorized research animal breeder, all rats were considered healthy.
The health status was confirmed at postmortem examination at the
end of the doctoral thesis research. Any cardiovascular abnormalities
detected on physical examination (like murmur and arrhythmias)
and on macroscopic postmortem exam lead to exclusion from the
study. The postmortem exam was performed by the first author
(SD) under the supervision of an experienced veterinary pathology
specialist.
2.3 Study design
This is a prospective, anatomical and reference interval study. Radio-
graphs were performed under general anesthesia in all cases. The ani-
mals were induced in an induction chamber using 5% isoflurane gas
(Isoflo 100%, Zoetis Spain S.L., Madrid, Spain) delivered in oxygen at
2 L/min. Anesthesia was maintained using 1%–3% isoflurane delivered
in oxygen at 1 L/min, by a small face mask and nonrebreathing cir-
cuit. Positive pressure breath hold was solely performed at the time of
radiographic exposure in order to obtain an image at inspiration peak,
395
otherwise spontaneous breathing was maintained by all the animals
throughout the entire procedure. Vital signs were monitored using a
stethoscope (Classic II Infant 28′’ Stethoscope, Littmann 3 M, USA)
and a pulse oximeter (PalmSAT 2500, Nonin, Tilburg, Netherlands).
Body temperature was monitored using a rectal probe (Electro-therm
TC100A, Cooper Instruments, Virginia, USA) and maintained between
37 and 39◦ C, using a small heat pad (Hotdog - Patient warming, Augus-
tine Surgical Inc, Minnesota, USA).
Right lateral, DV, and VD thoracic radiographs were obtained in each
animal (System: Premium Vet-variable focal distance, Sedecal, Madrid
Spain; X-ray tube: Rotanode E7239X, Toshiba, Tokyo-Japan. Parame-
ters: 45kVp; 400 mA; 0.025 s; 1-m film-focus distance) using a mammo-
graphic cassette (Regius CP1M200, Konika Minolta, Tokyo-Japan). The
thorax of the animal was positioned at the center of the mammographic
cassette with the thoracic and pelvic limbs extended cranially and cau-
dally, respectively. The beam was centered and collimated at the level
of the thorax between the scapulohumeral joint and the most caudal
rib (Figures 1–3). A computer radiography reader (Regius170, Konika
Minolta, Tokyo-Japan) was used, and images were stored in the PACS
system (Centricity PACS-IW, GE heathcare) of the Hospital Clínic Vet-
erinari – UAB.
Radiographs were anonymized, randomized, and evaluated sepa-
rately by two authors, an ECZM – certified zoological medicine spe-
cialist in SD, and an ECVDI – certified veterinary radiologist (Carlo
Anselmi). Readers were blinded to sex, age, and body weight of each rat.
Radiographs were evaluated using medical screens (RadiForce MX210,
EIZO, Japan), and reviewers were able to manipulate the images as
needed including changing the window width, window level, and mag-
nification. Radiographs were considered of diagnostic quality if there
was substantial symmetry/superposition of the ribs and scapulae as
well as widely accessible cardiothoracic structures with adequate con-
trast and pulmonary inflation. Each reviewer performed two measure-
ments of the VHS in each projection with a week interval between
reading sessions. A corresponding VHS mean was calculated for each
reader and individual projection, being that values used for statistical
purposes. Measurement technique is described below and illustrated in
Figures 1–3. Measurements were performed using adjustable calipers
and recorded. No compensation for magnification was made on any
radiograph.
The long and short axis of the cardiac silhouette was measured. On
the RL view, the long axis was defined as the longitudinal measurement
of the cardiac silhouette from the carina to the apex. The short axis
was defined as the measurement between the cranial and caudal
margins of the cardiac silhouette at its maximum width, perpendicular
to the long axis (Figure 1). On the DV and VD radiographic views, the
long axis was defined as the longitudinal measurement of the cardiac
silhouette between the cranio-lateral and the caudo-lateral apical mar-
gins. The short axis was defined as the widest measurement obtained
perpendicular to the long axis (Figures 2 and 3). Long axis and short
axis measures were added for each view, and this total axes measure
was compared to the number of thoracic vertebrae from the cranial
edge of the fourth thoracic vertebra and counting in a caudal direction
(Figures 1–3).
396 DIAS ET AL .

F I G U R E 1 Eight and a half weeks old male (242 g) rat. (A) Position of the rat in right lateral (RL) recumbency for thoracic radiographs. (B)
Corresponding macroscopic in situ appearance of the cardiothoracic organs. (C) Example of VHS measurement on right lateral view. (D)
Radiographic study of the thorax in right lateral recumbency (parameters: 45kVp; 400 mA; 0.025 s; 1-m film-focus distance)Abbreviations: LA, long
axis of the cardiac silhouette; SA, short axis of the cardiac silhouette; T4, 4th thoracic vertebra [Color figure can be viewed at
wileyonlinelibrary.com]

2.4 Statistical analysis
The reference intervals for standardized VHS measurement on RL,
VD, and DV radiographic projections were determined following the
recommendations by the International Federation of Clinical Chem-
istry and the Clinical and Laboratory Standards Institute by an
experienced medical research statistician. The software Reference
Value Advisor (http://www.biostat.envt.fr/reference-value-advisor/)
was used.18 The remaining statistical analyses were carried out using
R software.19 The reference intervals were calculated based on the
measurements obtained by an ECVDI – certified veterinary radiolo-
gist (Carlo Anselmi), taking into consideration his greater experience in
radiology and specifically in the measurements of VHS in other species.
In the current study, differences in the values of VHS by gender were
also evaluated. In order to do that, we first evaluated the normality of
the data in the different groups using the Shapiro-Wilk test. If the test
evidenced the normality of data, means were compared using a t-test,
while if the test evidenced the lack of normality of data, means were
compared using the non-parametric, Mann-Whitney test.
Furthermore, we tested whether there was an association between
the values of VHS and the body weight. In order to do that, we first eval-
uated the normality of VHS values and the body weight data using the
Shapiro-Wilk test. If the test evidenced the normality of data, the cor-
relation was evaluated using Pearson correlation test, while if the test
evidenced the lack of normality of data, the correlation was evaluated
using the Spearman correlation test.
We also aimed to evaluate the interrater reliability index between
the two readers (i.e., an estimation of measurement error between
readers).20 This is done by measuring the intraclass correlation coef-
ficient (ICC). There are different versions of ICC, which applied to the
same data can give different results, so it is important to select the
appropriate ICC for each specific situation.21 In the case of this study,
we chose a two-way random-effects model, as we intended to gener-
alize the results to any other rater, a single rater, as there was single
measure per rater was used, and absolute agreement was measured, as
different raters assign the same score to the same subject.
3 RESULTS
3.1 Radiographs
A total of 124 rats were included in the study (62 males and 62 females,
with a mean age of 9.1 weeks (8.5–10.5), and a mean body weight of
260 g (females: 150–310 g with a mean of 251 g; males: 222–323 g with
a mean of 268 g).
DIAS ET AL . 397

F I G U R E 2 Nine-week-old male (275 g) rat. (A)

Position of the rat in dorsal recumbency for thoracic
radiographs. (B) Corresponding macroscopic in situ
appearance of the cardiothoracic organs. (C) Example of
VHS measurement on ventrodorsal (VD) view. (D)
Radiographic study of the thorax in dorsal recumbency
(parameters: 45kVp; 400 mA; 0.025 s; 1-m film-focus
distance)Abbreviations: LA, long axis of the cardiac
silhouette; SA, short axis of the cardiac silhouette; T4, 4th
thoracic vertebra [Color figure can be viewed at
wileyonlinelibrary.com]

TA B L E 1 Mean and standard deviation values of vertebral heart The mean values and references intervals of VHS were 7.7 and 7.0–
score recorded by two readers for each radiographic projection (RL, 8.5 for the RL, 7.5 and 6.6–8.6 for the VD, and 7.9 and 6.9–9.0 for the
VD, and DV)
DV.
Reader Projection Mean ± SD* The comparison of the values of VHS by sex was carried out for the
Reader 1 RL 7.71 ± 0.36 three projections and for both readers (Table 2). The results indicate

VD 7.57 ± 0.57 that the difference was statistically significant (p < 0.05) for all combi-
nations of projections and readers, with VHS values greater in males
DV 7.92 ± 0.54
than in females (p < 0.01) (Figures 4 and 5). Our results also showed no
Reader 2 RL 7.69 ± 0.34
correlation between VHS and body weight for any of the projections
VD 7.50 ± 0.55
(p > 0.05).
DV 7.86 ± 0.52 The evaluation of the ICC (i.e., agreement between readers) showed
*
SD, standard deviation. an agreement of 0.88 (95% confidence interval [CI]: 0.83–0.91) for the
RL projection, of 0.93 (95% CI: 0.89–0.96) for the VD projection, and
0.89 (98% CI: 0.85–0.93) for the DV projection. Therefore, agreement
The three available projections (RL, DV, and VD) for each rat were between readers can be considered as good (i.e., ICC between 0.75 and
considered diagnostic by both readers, and no animal was excluded due 0.9) for the RL and DV projections, and excellent (i.e., ICC above 0.9) for
to poor radiographic quality. Results from both readers are compiled in the VD projection.
Table 1.
The assessment of the normality of the data carried out according to 3.2 Postmortem examination
Anderson-Darling test and evidenced the normality of the distributions
for the three projections (p > 0.05). Presence of outliers was evaluated On postmortem examination, the thoracic and abdominal organs of all
using the Tukey test, but outliers were not detected in any of the pro- included rats appeared macroscopically unremarkable. In particular no
jections. macroscopic cardiac abnormalities were detected.
398 DIAS ET AL .

F I G U R E 3 Eight and a half weeks old male (269 g) rat. (A) Position of the rat in ventral recumbency for thoracic radiographs. (B) Example of
VHS measurement on dorsoventral (DV) view. (C) Radiographic study of the thorax in ventral recumbency (parameters: 45kVp; 400 mA; 0.025 s;
1-m film-focus distance)Abbreviations: LA, long axis of the cardiac silhouette; SA, short axis of the cardiac silhouette; T4, 4th thoracic vertebra
[Color figure can be viewed at wileyonlinelibrary.com]

TA B L E 2 Comparison of vertebral heart score measurements recorded by two readers for male versus female rats

Reader Projection Males (n = 62)Mean ± SD* Females (n = 62)Mean ± SD* p-value

Reader 1 RL 7.85 ± 0.32 7.57 ± 0.34 <0.001
VD 7.80 ± 0.47 7.35 ± 0.57 <0.001
DV 8.15 ± 0.44 7.68 ± 0.52 <0.001
Reader 2 RL 7.84 ± 0.30 7.55 ± 0.32 <0.001
VD 7.74 ± 0.42 7.26 ± 0.55 <0.001
DV 8.09 ± 0.43 7.64 ± 0.50 <0.001

*SD, standard deviation.

p-value ≤ 0.05 is statistically significant.

4 DISCUSSION
The aim of this study was to determine reference intervals for normal
VHS in anesthetized rats.
The VHS values for healthy rats are proposed in this study with
larger values observed in males compared with females. The interob-
server variability between the readers and variability between the pro-
jections were good to excellent. Agreement between the reviewers was
best for the VD projection. Based on our review of the literature, this
is the first report measuring VHS in rats using three different radio-
graphic projections (RL, VD, and DV).
Thoracic radiographs are commonly performed in order to detect
pathological processes allowing the clinician to provide differential
diagnosis based on the study and the clinical history of the patient.22
Clinicians can rely on cardiac measurements on radiographs as a fast
and feasible tool. Recording the VHS encourages objectivity and is a
more accurate way to monitor heart size changes in order to evaluate
progression of the disease.
In accordance with previously published data, in this study the car-
diac measurements were also easy to perform.3,7–15,23–25 Subjectively,
the identification of the cardiac silhouette was hindered due to the
superimposition of cranial mediastinal tissues silhouetting with the
cranial cardiac border, as previously described in other species.12,15
This problem was partially corrected by increasing the pulmonary
expansion through manual ventilation of the pulmonary parenchyma
using a tight face mask and performing positive pressure breath hold
during the radiographic exposure. In order to facilitate restraint and
minimize motion artifacts during cardiac evaluation, gas anesthesia
was used in all rats.
Comparing data published in other species, the mean VHS for rats
in the current study (7.7, 7.5, and 7.9 for RL, VD, and DV, respectively)
were larger than values reported for rabbits (RL: 7.60,12 RL:7.5511 ),
ferrets (RL: 5.27; VD: 6.11),9 black-tailed prairie dogs (RL: 7.12; DV:
4.46),15 and cats (RL: 7.5),8 respectively. Conversely, mean VHS for
chinchillas (RL: 8.9),14 African hedgehogs (Atelerix albiventris) (RL:
8.16),3 three species of flying foxes (P. rodricensis RL: 9.8; P. hypome-
lanus RL: 9.3; P. vanpirus RL: 9.2),23 ring-tailed lemur (Lemur catta) (RL:
8.92; DV: 9.42),24 red panda (Ailurus fulgens) (RL: 8.34; DV: 8.78),25
cats (VD: 8.2; DV: 8.1),8 and dogs (RL: 9.7)7 were larger than the VHS
in this report respectively. This great range of VHS intervals among
DIAS ET AL .
F I G U R E 4 VHS values by sex – reader 1 (plot graphic)
[Color figure can be viewed at wileyonlinelibrary.com]
F I G U R E 5 VHS values by sex – reader 2 (plot graphic)
[Color figure can be viewed at wileyonlinelibrary.com]
species leads to the imperative need of species-specific reference
values.
In the current study, statistical differences of VHS were detected
comparing RL and VD/DV projections. This is in accordance with pre-
vious researches in cats,8 dogs,7 and red panda.25
In dogs and cats, DV radiographs are preferred over VD radiographs
for the evaluation of the heart size, because cardiac contours are more
consistent in DV projections and because there is magnification in VD
radiographs as a result of the increased distance between the heart and
the cassette.7,26,27 In the present study this magnification factor was
not evident, as the VHS values were higher in DV projections than VD
projections in both readers. A definitive explanation for this difference
was not identified and is beyond the aim of this study.
It is paramount to realize that a VHS within normal limits does
not preclude an actual cardiac disease, mainly in cases where heart
enlargement is not part of the process. Careful inspection of the cardiac
borders should also be routinely performed, as animals can develop
concentric cardiac hypertrophy without dilation.
399
In dogs some limitations regarding VHS range were described in lit-
erature, mainly due to the large variations in size and thoracic con-
formation of the canine breeds. Those differences cause less accu-
racy with wide ranges of values, leading to the need of canine breed-
specific studies.28–30 Nevertheless, due to the relatively standard tho-
racic conformation and size of rats, it is authors’ opinion that the values
herein described can be a useful tool in cardiac cases. A similar conclu-
sion was obtained in feline patients due to their uniform shape of the
thorax.31
In this study, there was a good to excellent interobserver variability.
Variations can be justified by operator dependent and human factors,
such as difference in caliper position during measurements. Another
component to consider is the different experience and specialty area
between the two readers (ECVDI vs. non-ECVDI). The VD projection
had the best ICC (i.e., agreement between readers), with an excellent
score of 0.93 (95% CI: 0.89–0.96), and this can at least in part be related
to the differences between DV/VD projections as described in dogs
and cats. In small animals, on DV radiographs the heart assumes an
400
upright position, making it appear more round. In DV view, the acces-
sory lung lobe is less aereated because of cranial displacement of the
diaphragm, leading to left-cranial shift of the cardiac silhouette and less
assessment to the cranial mediastinum. The rounder appearance and
displacement to the left that occur normally in the DV radiographs are
commonly misinterpreted as cardiomegaly. The VD view allows a more
complete assessment of the caudal mediastinum than the DV view, as
the accessory lung lobe is more aereated, and the heart is therefore dis-
placed from the diaphragm slightly, increasing the space available for
the caudal mediastinum. Moreover, in VD projection the cardiac
silhouette is more elongated.22 These factors could possibly
play similar roles in rats, influencing the ICC observed in this
study.
In this study, as in humans32 and in ferrets,9 a difference between
male and female heart size was observed, with females having smaller
hearts than males. In dogs, some authors described larger VHS in males
than in females, but without definitive consensus.28,29,33 In kittens and
rabbits, no sex-related VHS significant differences were observed.34,35
Adult male rats have an average weight of 267–500 g, while the
average weight of adult female rats is 225–325 g. Both male and female
rats are considered sexually mature at 4.5 weeks of age.36 Taking into
consideration that in the present study the mean age is 9.1 weeks, and
the mean weight for males is 268 g and for female 251 g, the values
obtained in this study are considered representative of adult animals.
A population of young adults was elected instead of older adults in
order to reduce the risk of the development of cardio-respiratory dis-
ease with age; however, further studies are needed to evaluate if age
would influence VHS in rats.
This study has several limitations. Due to the small size of pet rats,
obtaining an optimal radiographic position can be challenging, leading
to some degree of rotation. Additionally, motion artefact secondary
to respiratory movements and cardiac cycle may have affected the
results. Moreover, the high respiratory rate in pet rats can prevent
obtaining thoracic radiographic in inspiratory phase, mostly if an
endotracheal tube is not in place. Unfortunately, endotracheal tube
placement can be challenging in small rodents and is not routinely
performed.
The radiographs generated in this study were considered diagnos-
tic, allowing an accurate VHS measurement in all the animals and
projections.
5 CONCLUSION
Reference values of VHS in orthogonal radiographic projections of
healthy rats are detailed in this study.
The measurements reported in this study can be used by clinicians
as an objective tool to evaluate cardiac size in pet rats, as well as in
research settings.
Future studies would be necessary in order to determine if radio-
graphic VHS would detect cardiomegaly in rats. The reference ranges
established in this study can be useful as a reference baseline for the
diagnose and progression of cardiac disease in rats.
DIAS ET AL .
ACKNOWLEDGMENTS
The authors would like to thank Rosa Novellas for the assistance with
the radiographic interpretations, Sebastian Napp for the statistical
analysis, and Nicky Cassel for the grammar review.
LIST OF AUTHOR CONTRIBUTIONS
Category 1
(a) Conception and Design: Dias, Martorell
(b) Acquisition of Data: Dias
(c) Analysis and Interpretation of Data: Dias, Anselmi, Espada,
Martorell
Category 2
(a) Drafting the Article: Dias
(b) Revising Article for Intellectual Content: Dias, Anselmi, Espada,
Martorell
Category 3
(a) Final Approval of the Completed Article: Dias, Anselmi, Espada,
Martorell
CONFLICT OF INTEREST
The authors declare no conflict of interest.
ORCID
Sara Dias https://orcid.org/0000-0002-2656-8345
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How to cite this article: Dias S, Anselmi C, Espada Y, Martorell
J. Vertebral heart score to evaluate cardiac size in thoracic
radiographs of 124 healthy rats (Rattus norvegicus). Vet Radiol
Ultrasound. 2021;62:394–401.
https://doi.org/10.1111/vru.12973