Edited by: Ellen Roelfsema, Utrecht University, Netherlands
Reviewed by: Annamaria Grandis, University of Bologna, Italy; Domenico Caivano, University of Perugia, Italy
This article was submitted to Comparative and Clinical Medicine, a section of the journal Frontiers in Veterinary Science
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Laminitis is an extremely painful disease that compromises the integrity of the digital dermis and the normal biomechanics of the equine foot (
The pathophysiology of laminitis is still not completely understood. It has been defined as the failure of the attachment of the distal phalanx and the inner hoof wall (
These mechanisms lead to significant anatomical changes (
Digital venogram assessments have been shown to be very important for the assessment of vascular perfusion and integrity in the horse (
There is little information on the radiological anatomy of donkey feet (
Laminitis is currently an underestimated pathology in donkeys, despite being a common disease in this species, due to the lack of physiological data on the donkey digit (
Few studies have been conducted on evaluating the radiographic appearance of the donkey digit, either in healthy or laminitic animals (
The aim of this study was to assess the radiographic and venographic parameters of healthy Amiata donkey feet, to define the changes associated with mild and severe laminitis and to compare the results with other donkey breeds and horses.
A cohort of 8 Amiata donkeys belonging to the Regional Stud Farm of Tuscany and housed at the Veterinary Teaching Hospital, Department of Veterinary Sciences, University of Pisa were enrolled in this study. Approval to conduct this study was obtained from the ethical committee of the University of Pisa, according to the D. Lgs. 26/14 (Number 23/19).
All the animals enrolled were barren jennies used for reproduction purposes and were considered non-athlete. The animals were aged between 9 and 19 years (median age 13 years), the body weight (BW) ranged between 283 and 393 kg (median BW 342 kg), and the body condition score (BCS) ranged between 5 and 6.5/9 (median BCS 5.75/9). Jennies were housed in collective paddocks 24 h a day, fed with meadow hay
None of the jennies had a previous history of foot-related problems. An orthopedic evaluation was performed on all the animals to assess the following clinical signs related to laminitis: stance and gait irregularities, soundness according to the Obel score (
Hooves were inspected visually to assess the presence of the following signs of laminitis: presence of converging hoof growth rings, deformity of hoof capsule shape, slipper foot conformation, flattening of the sole, and widening of the white line. Since no previous studies are available in the literature, the presence of converging rings was assessed according to a grading scale specifically designed for this study. The wall deformity was thus scored from 0 to 3 (
Grading of the wall deformity (
Grade 0 | No visible changes |
Grade 1 | Converging hooves growth rings involving 1/3 of the hoof wall |
Grade 2 | Converging hooves growth rings involving 2/3 of the hoof wall |
Grade 3 | Wall changes involving the entire hoof wall |
For all the jennies enrolled in the present study, x-ray views were obtained for both forelimbs, for a total of 16 forefoot radiographs. Prior to radiography, the feet were thoroughly cleaned. All subjects were sedated with detomidine chloride (10 μg/Kg, IV) (Detogesic®, Zoetis Italia, Italy) and buthorphanol 0.025 mg/kg, IV (Nargesic®, ACME, Italy) (
All radiographs were obtained at a focal distance of 80 cm, with the beam focused midway between the dorsal and palmar aspect of the foot, and midway between the coronary band and the weight bearing border, in accordance with the literature (
All the forefoot radiographs obtained were assessed in terms of the radiological parameters relevant to laminitis. These radiometric parameters and associated definition are shown in
Direct and derived radiological parameters relevant in laminitis, for the forefoot and their definitions, in latero-medial and dorso-palmar radiographic views [modified from (
S | Dorsal hoof wall angle | Angle subtended between the dorsal aspect of the hoof wall and the ground line direct parameter |
Ts | Dorsal angle of the distal phalanx | Angle subtended between the dorsal aspect of the DP and the ground line Direct parameter |
U | Angle of proximal phalanx | Angle subtended between the long axis of the PP and the ground line Direct parameter |
C | Angle of middle phalanx | Angle subtended between the long axis of the MP and the ground line Direct parameter |
SA | Angle of solar aspect of the distal phalanx | Angle subtended between the solear aspect of the DP and the ground line Direct parameter |
PA (U-C) | Angle of pastern axis | Angular difference between long axis of the PP and MP Derived parameter. |
HPA (U-S) | Angle of hoof pastern axis | Angular difference between the dorsal hoof wall angle and the long axis of the PP |
H Ang (Ts-S) | Angular deviation between the dorsal aspect of the DP and dorsum of the hoof wall | Angular difference between dorsal aspect of the DP and the dorsal hoof wall angle Derived parameter |
F Ang (C-Ts) | DIP rotation Angle | Angular difference between dorsal aspect of the DP and the long axis of the MP Derived parameter |
R Ang (U-Ts) | Phalangeal rotation angle | Angular difference between dorsal aspect of the DP and the long axis of the PP Derived parameter |
D | Distal displacement of the distal phalanx | Perpendicular linear distance between the proximal limit of the hoof wall and the extensor process of the DP |
MPL | Middle phalanx length | Liner measurement of long axis of the middle phalanx |
IDA | Proximal integument depth of the dorsal aspect of the foot | Perpendicular linear distance between the dorsal aspect of the hoof wall and the dorsal surface of the DP, immediately distal to the distal limit of the extensor process |
IDB | Distal integument depth of the dorsal aspect of the foot | Perpendicular linear distance between the dorsal aspect of the hoof wall and the dorsal surface of the DP proximal to the apex of the DP |
IDM | Mid integument depth of the dorsal aspect of the foot | Perpendicular linear distance between the dorsal aspect of the hoof wall and the dorsal surface of the DP at the midpoint between the IDA and IDB measurement sites |
IDR | IDA/IDB ratio | |
SL | Lateral sole thickness | Perpendicular linear distance between the lateral solar aspect of the DP and the ground |
SM | Medial sole thickness | Perpendicular linear distance between the medial solar aspect of the DP and the ground |
LHW | Lateral hoof wall thickness | Perpendicular linear distance between the distal lateral aspect of the DP and the lateral hoof wall |
MHW | Medial hoof wall thickness | Perpendicular linear distance between the distal medial aspect of the DP and the medial hoof wall |
PPCA | Proximal palmar cortex angle | Angle subtended between the proximal palmar cortex of the DP and the ground line |
PPCL | Proximal palmar cortex length | Linear distance between the point of insertion of DDFT and the articular process of the navicular joint |
PCL | Palmar cortex length | Linear distance between the apex of the DP and the articular process of the navicular joint |
RA | Reflex angle of palmar cortex | Internal angle subtended between the proximal and distal palmar cortex of the DP |
AA | Apex angle | Internal angle subtended between the distal palmar cortex and the dorsal aspect of the DP |
Surface Convexity | Dorsal surface of the coffin bone convexity | Quality evaluation of the convexity of the parietal surface of the distal phalanx |
Erosion | Osteolysis of Distal margin of the coffin bone | Quality evaluation of resorption and remodeling of bone at the dorsal solear margin of the distal phalanx |
Distal Margin Lip | Remodeling of the distal margin of the coffin bone | Quality evaluation of new bone formation on the dorsal aspect of the toe of the distal phalanx |
Based on the results obtained from clinical examination and radiographic evaluation, the feet were retrospectively divided into three groups, as previously reported (
All the venographic exams were performed under sedation with detomidine chloride (10 μg/Kg, IV) (Detogesic®, Zoetis Italia, Italy) and buthorphanol 0.025 mg/kg, IV (Nargesic®, ACME, Italy) (
A total of 20 ml of contrast agent (Iopamiro 300®, Bracco Imaging, Italia) was used for an average-sized foot and two different syringes were used to avoid excessive injection pressure, and thus to prevent any perivascular extravasation or wall vein damage (
After all the contrast has been injected, the butterfly catheter was left in place and the tube line was taped proximally to the limb, until the radiographs were performed (
Six areas were evaluated on the venogram image (
Venographic parameters relevant in laminitis, for the forefoot and their definitions, in LM and DP radiographic views [modified from (
PDV | Palmar Digital Vein | Present—Altered—Absent |
TA | Terminal Arch | Present—Altered—Absent |
CV | Circumflex Vessels | Location of the Circumflex Vessels distal to the palmar rim of the distal phalanx |
LCJ | Lamellar-Circumflex Junction | Normal—Mild—Folded—Void of Contrast |
SLVB | Sublamellar Vascular Bed | Uniform Line—Rectangular Shape—Triangular Shape—Void of Contrast |
CP | Coronary Plexus | Normal—Abnormal—Void of Contrast |
PDV | Palmar Digital Vein | Present—Altered—Absent |
TA | Terminal Arch | Present—Altered—Absent |
CVM | Circumflex Vessels Medial | Location of the Medial Circumflex Vessels distal to the palmar rim of the distal phalanx |
CVL | Circumflex Vessels Lateral | Location of the Lateral Circumflex Vessels distal to the palmar rim of the distal phalanx |
LCJ | Lamellar-Circumflex Junction | Normal—Mild—Folded—Void of Contrast |
SLVB | Sublamellar Vascular Bed | Uniform Line—Rectangular Shape—Triangular Shape—Void of Contrast |
CPL | Coronary Plexus Lateral | Normal—Abnormal—Void of Contrast |
CPM | Coronary Plexus Medial | Normal—Abnormal—Void of Contrast |
These areas were examined both in LM and DP views for a quality evaluation of the contrast distribution (
Data were assessed for distribution. Since some parameters were normally distributed and others were not, we decided to express all the results as not Gaussian distributed. The results were reported as median and standard error, minimum and maximum values.
The Kruskal-Wallis-test for multiple comparisons was applied to verify differences between the three groups concerning the numerical data (angular and linear radiographic parameters, lameness and clinical parameters of hoof convergent rings), BW and BCS. The significance level was set at p <0.05. Statistical analysis was performed with GraphPad Prism v. 8.3.1 (GraphPad Software Inc., San Diego, CA, USA).
The results obtained from physical and external hoof examinations are reported in
Average values obtained from clinical evaluation, reported according to the subgroups.
Normal | 0 | No | 0 | No | Normal | Negative | 5 | 289 |
Mild | 0 | No | 0 | No | Normal | ± | 5.5 | 322 |
Severe | 0-3 | No | 1 | No | Warm | Positive | 6 | 316 |
Normal | No | 1.1 | Yes | No | ± | No | ||
Mild | No | 0.5 | Yes | ± | Yes | No | ||
Severe | Yes | 1.2 | Yes | Yes | Yes | No |
The results obtained for the angular, linear and morphometric radiological parameters relevant to the laminitis evaluation are shown in
Angular radiographic parameters from latero-medial view, expressed as degree, for the healthy, mild, and laminitic study groups.
Me | 60.1 | 59.3 | 61.9 | 62.5 | 66.4 | 71.3 | 61.2 | 60.2 | 63.8 | 64.7 | 58.6 | 67.9 | 7.7 | 11.3 | 15.7 | −0.8 | 0.0 | 3.5 | 2.2 | 0.1 | 8.2 | 2.5 | 7.6 | 11.1 | 2.2 | −7.8 | −5.0 | 0.6 | −5.9 | −7.2 |
m | 59.0 | 58.2 | 55.6 | 60.6 | 66.1 | 68.3 | 58.4 | 50.0 | 61.3 | 53.1 | 50.3 | 58.1 | 6.1 | 10.1 | 14.4 | −7.7 | −0.4 | −6.6 | −2.1 | −9.4 | −0.7 | 0.1 | 4.1 | 6.5 | −7.4 | −17.1 | −10.7 | −3.5 | −17.4 | −10. |
M | 61.1 | 62.0 | 63.4 | 64.1 | 67.3 | 78.6 | 69.1 | 62.5 | 73.0 | 72.1 | 61.3 | 76.6 | 9.2 | 13.7 | 22.4 | 5.3 | 4.6 | 5.7 | 8.0 | 3.2 | 9.7 | 3.1 | 8.0 | 16.7 | 9.2 | −4.7 | −2.0 | 5.0 | −4.1 | −1.2 |
Linear radiographic parameters from latero-medial view, expressed in cm, for the healthy, mild, and laminitic study groups.
Me | 3.3 | 1.6 | 1.7 | 3.4 | 3.7 | 3.5 | 2.5 | 2.6 | 2.4 | 2.7 | 2.9 | 3.0 | 2.6 | 3.0 | 2.8 | 1.0 | 0.8 | 0.8 |
m | 1.2 | 0.8 | 1.3 | 3.3 | 3.4 | 3.4 | 1.7 | 2.0 | 2.1 | 2.1 | 2.4 | 2.5 | 2.0 | 2.2 | 2.4 | 0.8 | 0.8 | 0.8 |
M | 3.9 | 2.2 | 2.2 | 3.7 | 4.0 | 3.7 | 3.0 | 3.3 | 2.9 | 3.2 | 3.4 | 3.2 | 2.9 | 3.2 | 3.2 | 1.2 | 1.1 | 0.9 |
Morphometric radiographic parameters from latero-medial view, for the healthy, mild, and laminitic study groups.
Me | 49.0 | 53.5 | 59.3 | 2.5 | 2.7 | 2.5 | 4.4 | 4.7 | 4.4 | 140.6 | 137.4 | 137.4 | 52.4 | 57.2 | 53.4 |
m | 41.6 | 50.9 | 51.7 | 2.0 | 2.4 | 2.0 | 4.0 | 4.5 | 4.1 | 124.3 | 135.9 | 134.0 | 45.1 | 54.6 | 50.6 |
M | 61.5 | 55.0 | 61.5 | 2.9 | 3.5 | 2.9 | 5.2 | 5.2 | 5.0 | 147.4 | 144.6 | 145.3 | 56.8 | 64.6 | 60.3 |
Linear radiographic parameters from dorso-palmar view for the healthy, mild, and laminitic study groups.
Me | 2.5 | 2.0 | 2.1 | 2.4 | 2.3 | 1.9 | 2.0 | 2.2 | 2.0 | 1.8 | 1.7 | 1.8 |
m | 1.9 | 1.5 | 1.8 | 1.7 | 2.1 | 1.8 | 1.6 | 1.2 | 1.4 | 1.5 | 1.5 | 1.2 |
M | 2.9 | 2.8 | 2.7 | 3.1 | 2.7 | 2.9 | 2.4 | 2.7 | 2.8 | 2.0 | 1.8 | 2.0 |
Latero-medial plain radiographic images of healthy
The results obtained from the evaluation of the venographic parameters are given in
Values obtained from the evaluation of venographic parameters, shown according to subgroups. Minimum and maximum values are reported for each parameter.
PDV | Present | Present | Present |
TA | Present | Present | Present |
CV (mm) | 4.3 – 4.7 | 4.0 – 5.7 | 2.9 – 6.2 |
LCJ | Normal | Mild - Folded | Mild - Void of contrast |
SLVB | Uniform Line | Rectangular to Triangular shape | Triangular Shape -Void of contrast |
CP | Normal | Normal | Normal - Void of contrast |
PDV | Present | Present | Present |
TA | Present | Present | Present |
CVM (mm) | 2.2–3.8 | 3.0–6.4 | 2.3–5.7 |
CVL (mm) | 2.6–4.6 | 2.5–5.1 | 2.4–4.6 |
LCJ | Normal | Normal—Folded | Normal—Void of Contrast |
SLVB | Uniform Line | Uniform line—Rectangular shape | Rectangular shape—Void of contrast |
CPL | Normal | Normal | Normal—Abnormal |
CPM | Normal | Normal | Normal—Void of Contrast |
Latero-medial venograms of healthy
Dorso-palmar venograms of healthy
Finally, statistical differences were found for BCS (
The radiographic and venographic appearance of healthy and laminitic feet in donkeys were assessed in order to define the changes associated with mild and severe laminitis and to compare the results with other donkey breeds and horses.
Overall, we found statistical differences between healthy vs. severe laminitic donkeys for Ts, SA, H, and R ang, but not between mild vs. severe laminitic or healthy feet. No differences were found for other radiographic parameters. Thus, our results support the idea that the bone alignment and its relationship with the hoof capsule is relevant in the evaluation of laminitis in donkeys, in line with literature (
In our study, Ts and SA values differed significantly between severe laminitic and healthy group. In particular, Ts and SA values were higher in the severe laminitic group compared to the healthy group, in agreement with Collins et al. (
The statistically differences obtained in the H Ang values between healthy and severe laminitic groups were in line with the previous study by Collins et al. (
In this work, the R Ang values statistically differ between healthy and severe laminitic groups, as also reported by Collins et al. (
The lack of differences between mild vs. severe laminitic feet or healthy feet for Ts, SA, H, and R ang might be related to the small number of animals included in the study and/or by the wide variability in digit values registered in donkey breeds (
We found 1/8 donkey presenting one healthy forefoot and the other one showing mild laminitic changes, in line with literature. In fact, laminitis may affect only one foot, if the causes are repeated trauma on the foot, abnormal distribution of the loading force and any other alteration of the normal gait (
The PDV and TA values obtained from venographic studies in healthy donkeys were clearly evident, in agreement to literature (
In our study, the CV values, obtained both in the LM and DP views, showed wide ranges both in the mild and severe laminitic groups compared with the healthy one. To the best of authors' knowledge, the CV range has not been reported in healthy donkey feet yet. The results obtained for CV parameter in healthy donkeys in this study is comparable to what reported in a previous study (
On the other hand, our results for the LCJ and SLVB revealed strongly altered values in both the mild and severe laminitic groups compared with the healthy group, both in DP and LM views. Donkeys show a well-developed anastomosis in foot circulation compared to horses (
Lastly, in our study CP parameters showed comparable results between the healthy and mild laminitic groups. On the other hand, the CP ranged from normal to void of contrast in the severe laminitic group. These findings may be explained considering that occasionally an inadequate volume of contrast creates a technical artifact, reducing the filling of CP, as reported in horses (
As reported in literature, the presence of dermal pathology may be overlooked without venograms and the appropriate treatment may be delayed (
This study has some limitations. The venogram appearance was evaluated in a small number of healthy feet, thus this might have led to a bias in the interpretation of results. Therefore, more studies needed to correctly establish the normal venogram appearance of healthy donkey feet in order to properly evaluate a pathological foot and to verify the reproducibility of the study.
The raw data supporting the conclusions of this article will be made available by the authors, without undue reservation.
The animal study was reviewed and approved by the Ethical Committee of the University of Pisa, according to the D. Lgs. 26/14 (Number 23/19). Written informed consent was obtained from the owners for the participation of their animals in this study.
MS and SC conceived, designed, and supervised the project. IN, BA, and LB executed the experiment. IN, BA, and LG-C analyzed the data. MS executed the formal analysis. IN and MS had full access to all the data in the study and take responsibility for the integrity of the data, and the accuracy of the data analysis. All the authors interpreted the data, wrote and critically revised the manuscript for intellectual content, and approved the final version. All authors contributed to the article and approved the submitted version.
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
We are grateful to the Regional stud farm Ente Terre Regionali Toscane (Tuscany, Italy) for allowing us to use the animals for this study. The authors thank Giuseppe Conte for statistical support.