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Home , Accessory bone, Appendicular skeleton, Dactyly, Digit (anatomy), Dysostosis, Ectrodactyly

Article Four Unusual Cases of Congenital Malformations in Dogs

Simona Di Pietro 1 , Giuseppe Santi Rapisarda 2, Luca Cicero 3,* , Vito Angileri 4, Simona Morabito 5, Giovanni Cassata 3 and Francesco Macrì 1

1 Department of Veterinary Sciences, University of Messina, Viale Palatucci, 98168 Messina, Italy; [email protected] (S.D.P.); [email protected] (F.M.) 2 Department of Veterinary Prevention, Provincial Health Authority of Catania, 95030 Gravina di Catania, Italy; [email protected] 3 Institute Zooprofilattico Sperimentale of Sicily, Via G. Marinuzzi, 3, 90129 Palermo, Italy; [email protected] 4 Veterinary Practitioner, 91025 Marsala, Italy; [email protected] 5 Ospedale Veterinario I Portoni Rossi, Via Roma, 57/a, 40069 Zola Predosa (BO), Italy; [email protected] * Correspondence: [email protected]

Simple Summary: Congenital defects are sporadically encountered in dogs during normal clinical practice. Literature concerning their diagnosis and management in canine species is poor. Sometimes, the diagnosis and description of congenital limb abnormalities are complicated by the concurrent presence of different malformations in the same limb and the lack of widely accepted classification schemes. In order to improve the knowledge about congenital limb anomalies in  dogs, this report describes the clinical and radiographic findings in four dogs affected by unusual  congenital forelimb defects, underlying also the importance of reviewing current terminology. Citation: Di Pietro, S.; Rapisarda, G.S.; Cicero, L.; Angileri, V.; Morabito, Abstract: Four dogs were presented with thoracic limb deformity. After clinical and radiographic S.; Cassata, G.; Macrì, F. Four Unusual examinations, a diagnosis of congenital malformations was performed for each of them. In one Cases of Congenital Forelimb case, a deformity involving both the radial and ulnar side of the distal limb was observed. Based on Malformations in Dogs. Animals 2021, clinical and radiological evaluations, a diagnosis of postaxial terminal longitudinal ulnar 11, 813. https://doi.org/10.3390/ was performed. The term was used to refer different malformations characterized ani11030813 by skin and soft tissue separation of the distal forelimb observed in two dogs. Simple complete uncomplicated of the right forelimb, and complex incomplete uncomplicated syndactyly Academic Editor: Francesca Ciotola of the left forelimb were diagnosed in the fourth case. To the authors’ knowledge, ectrodactyly and

Received: 1 February 2021 simple complete uncomplicated syndactyly are very uncommon anomalies in companion animals Accepted: 11 March 2021 and have been rarely documented. Moreover, postaxial terminal longitudinal ulnar hemimelia has Published: 14 March 2021 still not been reported in dogs.

Publisher’s Note: MDPI stays neutral Keywords: congenital limb deformity; dog; ectrodactily; syndactyly; ulnar hemimelia with regard to jurisdictional claims in published maps and institutional affil- iations. 1. Introduction Appendicular skeletal dysostoses are a group of dysmorphologies arising from al- terations of the limb’s developmental process, resulting in a wide range of abnormalities Copyright: © 2021 by the authors. involving individual or portions of bones of the growing embryo body extremi- Licensee MDPI, Basel, Switzerland. ties [1]. This article is an open access article Hereditary (genetic aberrations) and environmental factors (drugs, maternal diseases, distributed under the terms and radiations and trauma) can cause an abnormal developmental process or an interference conditions of the Creative Commons with a normal developmental process, respectively [2,3]. Attribution (CC BY) license (https:// Limb formation is an intricate process, which takes place during the first weeks (from creativecommons.org/licenses/by/ D23 to D35) of gestation in dogs [3–5] Presumptive limb-forming fields are early established 4.0/).

Animals 2021, 11, 813. https://doi.org/10.3390/ani11030813 https://www.mdpi.com/journal/animals Animals 2021, 11, 813 2 of 12

during embryonic development because of the rounding up of the somatic mesoderm cells of the hypomere beneath the surface ectoderm [5,6]. Congenital defects and varying associations of stilopodium, zeugopodium and au- topodium dysmorphologies have been previously described in cats and dogs. [7–12]. The term stylopodium refers to a limb that terminates anywhere along the or ; zeugopodium is a limb that terminates along the and or and fibula, and autopodium when a limb terminates at the bones of the [13]. Recent reports of forelimb and malformations of carnivores include ectro- [14], preaxial longitudinal intercalary radial hemimelia [15], simple syndactyly and unilateral pelvic limb adactyly in puppies [16,17], absence of the humerus with preaxial terminal longitudinal hemimelia and hypoplasia of the in a dog [17] and partial paraxial radial hemimelia [18]. Despite the growing number of reports, in dogs the current knowledge about congeni- tal limb deformity is very poor. Moreover, compared to literature, in veterinary medicine a complete and unequivocal description of many congenital defects is still lacking. In order to improve the knowledge about congenital limb anomalies in dogs, the aim of this report is to describe the clinical and radiographic findings in four dogs affected by dysostoses of the distal extremities. The importance of this report lies in it helping the clinician to recognize more easily the features of rarely reported congenital limb deformities in canine species in order to perform a diagnosis.

2. Case Presentations 2.1. Ethical Statement No ethical approval was required in compliance with European Directive 2010/63/UE and Italian Regulation D.Lgs n. 26/2014 because all the data derived from routine veteri- nary clinical practices.

2.2. Clinical Examination Four client-owned, crossbreed young dogs were presented each with an obvious de- formity in the . All dogs had an unknown history and the anomalies of forelimbs were supposed to be congenital. The sites of deformation were assessed by physical and radiographic examination. Forelimb radiographs were obtained using an Analogic Radio- graphic/Fluoroscopic Table System (Dedalus Mb 90/20 IMX-2A, Imago Radiology S.r.l., 20081, Abbiategrasso (MI), Italy) with a digital system (Fujifilm Medical Sys- tems, Cernusco sul Naviglio (MI), Italy) in different projections: mediolateral, oblique and dorsopalmar views. The following X-ray exposure setting was used: 40–60 kV, 8–12.5 mAs, 100 cm film-focus distance, no grid. Below, the physical and radiographic findings of enrolled dogs are described.

2.3. Case 1 A two-year-old male dog was referred for a nonfunctional right forelimb due to decreased range of motion of the right and moderate disuse muscle atrophy with no pain during palpation. On , coexistent clinical abnormalities were a reduced number of digits (hypodactlyly) with a complete rotation of the lateral , and an ectopic -like structure in the elbow region. Three complete footpads (metacarpal pad and two digital pads) were observed. A footpad was also present in the digit like structure (Figure1). Animals 2021, 11, 813 3 of 12 Animals 2021, 11, x 3 of 12 Animals 2021, 11, x 3 of 12

FigureFigure 1. Case 1. Medial Medial ( (AA)) and and lateral lateral ( (BB)) views views of of the the right right forelimb. forelimb. Figure 1. Case 1. Medial (A) and lateral (B) views of the right forelimb. The radiographic examination consisted consisted of of two two views, views, including including a amediolateral mediolateral view view ofof thetheThe forelimb radiographic section examinationand a dorsoplantar consisted view view of twoof of the the views, manus manus including (Figures (Figures a 22mediolateral andand 33).). view of the forelimb section and a dorsoplantar view of the manus (Figures 2 and 3).

FigureFigure 2. CaseCase 1. 1.Craniocaudal Craniocaudal radiograph radiograph (A) and (A) drawing and drawing scheme scheme (B) of the (B) right of the forelimb right forelimb mal- Figure 2. Case 1. Craniocaudal radiograph (A) and drawing scheme (B) of the right forelimb mal- malformation.formation. R: Radius; R: Radius; RC: radial RC: carpal radial ; carpal CB: bone; carpal CB: bone; carpal MC: bone; metacarpal MC:metacarpal bone; PP: proximal bone; PP: formation.phalange; MP: R: Radius; middle RC: phalange; radial carpal DP: distal bone; phalan CB: carpalge; DS: bone; dorsal MC: sesamoid; metacarpal PSB: bone; proximal PP: proximal sesa- proximal phalange; MP: middle phalange; DP: distal phalange; DS: dorsal sesamoid; PSB: proximal phalange;moid bone. MP: middle phalange; DP: distal phalange; DS: dorsal sesamoid; PSB: proximal sesa- sesamoidmoid bone. bone.

Figure 3. Case 1. Mediolateral radiograph (A) and drawing scheme (B) of the right forelimb mal- Figureformation. 3. Case CaseH: humerus; 1. 1.Mediolateral Mediolateral U: ulna; radiograph R: radiograph radius; ( RC:A) and (radialA) drawing and carpal drawing scheme bone; schemeCB: (B) second of the (B) right and of the thirdforelimb right distal forelimbmal- car- malformation.formation.pal bone; MC: H: humerus;metacarpal H: humerus; U: bone; ulna; U: PP:R: ulna; radius; proximal R: RC: radius; phalange; radial RC: carpal MP: radial bone; middle carpal CB: phal second bone;ange; CB:and DP: secondthird distal distal pha- and car- third pal bone; MC: metacarpal bone; PP: proximal phalange; MP: middle phalange; DP: distal pha- distallange; carpalDS: dorsal bone; sesamoid; MC: metacarpal PSB: proximal bone; PP:sesamo proximalid bone. phalange; The MP: middle and trochlear phalange; notch DP: were distal lange; DS: dorsal sesamoid; PSB: proximal . The olecranon and were phalange;hypoplastic. DS: dorsal sesamoid; PSB: proximal sesamoid bone. The olecranon and trochlear notch hypoplastic. were hypoplastic. Animals 2021, 11, x 4 of 12

In the mediolateral view of the forelimb section, a severe deformity was observed Animals 2021 11 , , 813 due to a collapse of the elbow joint, which was in acute flexion. The radial4 head of 12 and the humeral condyle were deformed, showing a rounded and irregular articular surface. The ulna showed only the olecranon, whereas the medial and distal ulnar portions were miss- ing.In the mediolateral view of the forelimb section, a severe deformity was observed due to a collapseThe olecranon of the elbow and joint, trochlear which was notch in acutewere flexion. hypoplastic. The radial This head may and suggest the humeral that the troch- condylelear notch were dislocated deformed, long showing before a roundedpresentation, and irregular explaining articular the stiffness surface. of The the ulna elbow joint. showed only the olecranon, whereas the medial and distal ulnar portions were missing. In the soft tissue near the caudal surface of the radial head a rudimentary digit con- The olecranon and trochlear notch were hypoplastic. This may suggest that the trochleartaining a notch hypoplastic dislocated metacarpal long before bone presentation, and proximal, explaining middle the and stiffness distal ofphalanx, the el- without bowevidence joint. of , was observed, suggestive of an ectopic digit-like structure. It was char- acterizedIn the softby the tissue outline near theof the caudal hypoplasic surface of fifth the radialmetacarpal head a bone rudimentary and the digitproximal, con- medial tainingand distal a hypoplastic phalanges metacarpal of the fifth bone digit. and proximal, The dorsopalmar middle and view distal of phalanx, the manus without showed no evidenceulnar carpal of joints, bone, was accessory observed, suggestivebone and ofdistal an ectopic line of digit-like carpal structure.bones. Th Ite wasradial charac- carpal bone, terizedtwo complete by the outline digits of and the hypoplasica hypoplasic fifth metacarpal metacarpal bonebone and without the proximal, its phalanges, medial and were noted. distalA 180° phalanges rotation of on the the fifth axial digit. plane The of dorsopalmar the lateral distal view of phalange the manus was showed observed. no ulnar The remain- carpal bone, and distal line of . The radial carpal bone, two ing digits and soft tissue were within the normal limits. Clinical and radiographic findings complete digits and a hypoplasic metacarpal bone without its phalanges, were noted. A 180showed◦ rotation a postaxial on the axial terminal plane of longitudinal the lateral distal ulnar phalange hemimelia was observed. with absence The remaining mid and distal digitsulna, and ulnar soft and tissue accessory were within carpal the bone, normal distal limits. carpal Clinical bone and IV radiographic and an ectopic findings fifth digital showedray. a postaxial terminal longitudinal ulnar hemimelia with absence mid and distal ulna, ulnarNo treatment and accessory was carpal performed bone, distalfor managing carpal bone the IV congenital and an ectopic deformity fifth digital because ray. the dog hadNo no treatment evidence was of discomfort. performed for managing the congenital deformity because the dog had no evidence of discomfort.

2.4.2.4. Case Case 2 2 AnAn 11-month-old 11-month-old female female dog dog was referredwas referred for a nonfunctional for a nonfunctional right forelimb right forelimb without without painpain at at palpation. palpation. The The clinical clinical examination examination showed showed a lobster’s a lobster’s involving claw involving the paw, the paw, carpuscarpus and and antebrachium. antebrachium. The The skin skin and softand tissuessoft tissues of the distalof the limb distal were limb split were between split between radiusradius and and ulna ulna up up to to the the proximal proximal third third of of the the antebrachium. antebrachium. The The ulnar ulnar carpal carpal bone, bone, met- ◦ metacarpalacarpal bone bone and and phalanges showed showed a 180 a 180°rotation rotation on the on axial the plane. axial Theplane. ulnar The carpal ulnar carpal jointjoint was was in in acute acute cranial cranial flexion, flexion, with awith mediocaudal a mediocaudal rotation ofrotation the manus of the moving manus medial moving me- todial the to radio. the Theradio. radial The carpal radial joint carpal was joint also inwas acute also flexion in acute (Figure flexion4). (Figure 4).

FigureFigure 4. 4.Case Case 2. Medial2. Medial (A) ( andA) and lateral lateral (B) views (B) views of the of right the forelimb. right forelimb.

TheThe radiographic radiographic examination examination consisted consisted of mediolateral of mediolateral and dorsocaudal and dorsocaudal views of the views of rightthe right forelimb forelimb section section (Figures (Figures5 and6), where5 and a6), malformation where a malformation of the elbow of with the proximal elbow with prox- dorsalimal dorsal radial luxation radial luxation was observed. was observed. Animals 2021, 11, 813 5 of 12 Animals 2021, 11, x 5 of 12

Animals 2021, 11, x 5 of 12

Figure 5. Case 2. Craniocaudal radiograph (A) and drawing scheme (B) of the right forelimb mal- Figure 5. Case 2. Craniocaudal radiograph (A) and drawing scheme (B) of the right forelimb formation. R: Radius; U: Ulna; H: Humerus; RC: Radial Carpal Bone; UC: Ulnar Carpal Bone; AC: malformation.Figure 5. Case R:2. Radius;Craniocaudal U: Ulna; radiograph H: Humerus; (A) and RC: drawing Radial Carpalscheme Bone; (B) of UC: the Ulnarright forelimb Carpal Bone;mal- formation.Accessory Bone;R: Radius; MC: MetacarpalU: Ulna; H: Bone;Humerus; PP: Proxim RC: Radialal Phalange; Carpal Bone;DP: Distal UC: Ulnar Phalange; Carpal DS: Bone; Dorsal AC: AC: Accessory Bone; MC: Metacarpal Bone; PP: Proximal Phalange; DP: Distal Phalange; DS: Dorsal AccessorySesamoid. Bone;Note the MC: “stubby Metacarpal bone” Bone; (arrows) PP: Proximresultingal Phalange;by the fusion DP: of Distal the tw Phalange;o proximal DS: phalanges. Dorsal Sesamoid. Note the “stubby bone” (arrows) resulting by the fusion of the two proximal phalanges. Sesamoid. Note the “stubby bone” (arrows) resulting by the fusion of the two proximal phalanges.

Figure 6. Case 2. Mediolateral radiograph (A) and drawing scheme (B) of the right forelimb mal- formation. R: Radius; U: Ulna; H: Humerus; RC: Radial Carpal Bone; UC: Ulnar Carpal Bone; AC: FigureFigure 6. 6. CaseCase 2. 2. Mediolateral Mediolateral radiograph radiograph (A) ( Aand) and drawing drawing scheme scheme (B) of (B the) of right the forelimb right forelimb mal- formation.Accessory Bone;R: Radius; CB: Carpal U: Ulna; Bone; H: Humerus; MC: Metacarpal RC: Radial Bone; Carpal PP: Proximal Bone; UC: Phalange; Ulnar Carpal MP: Middle Bone; AC:Pha- malformation. R: Radius; U: Ulna; H: Humerus; RC: Radial Carpal Bone; UC: Ulnar Carpal Bone; Accessorylange; DP: Bone;Distal CB:Phalange; Carpal DS: Bone; Dorsal MC: Sesamoid.Metacarpal Arrows Bone; PP:indicate Proximal the “stubby Phalange; bone” MP: resulting Middle Pha- by AC: Accessory Bone; CB: Carpal Bone; MC: Metacarpal Bone; PP: Proximal Phalange; MP: Middle lange;the fusion DP: ofDistal the twoPhalange; proximal DS: phalanges. Dorsal Sesamoid. Arrows indicate the “stubby bone” resulting by Phalange;the fusion DP: of the Distal two Phalange; proximal DS: phalanges. Dorsal Sesamoid. Arrows indicate the “stubby bone” resulting by the fusionA severe of the hypoplasia two proximal of phalanges. the proximal of the radius was observed, the radial headA showed severe ahypoplasia severe deformation of the proximal with theepiphy flatteningsis of the of bothradius medial was observed, and lateral the epicon- radial A severe hypoplasia of the proximal epiphysis of the radius was observed, the ra- headdyles showedand an increased a severe deformationdimension of with the radial the flattening fossa was of noted. both medialThe olecranon and lateral was epicon-length- dial head showed a severe deformation with the flattening of both medial and lateral eneddyles andand flattened.an increased dimension of the was noted. The olecranon was length- epicondyles and an increased dimension of the radial fossa was noted. The olecranon was enedA and soft flattened. tissue separation between radius and ulna along the interosseous and lengthened and flattened. a severe increase of the intraosseus distance were observed. The ulna was shorter than AA soft soft tissue tissue separation separation between between radius radius and and ulna ulna along along the the interosseous interosseous ligament ligament and and radius. The radius-carpal joint was normal with a short bone compatible with the radial aa severe severe increase increase of of the the intraosseus intraosseus distance distance were were observed. observed. The The ulna ulna was was shorter shorter than than carpal bone, which in turn was articulated with a carpal bone of the second line. The carpal radius.radius. The The radius-carpal radius-carpal joint joint was was normal normal with with a a short short bone bone compatible compatible with with the the radial radial joint was in acute flexion. One metacarpal bone, dorsal and ventral sesamoids and two carpalcarpal bone, bone, which which in in turn turn was was articulated articulated with with a a carpal carpal bone bone of of the the second second line. line. The The carpal carpal phalanges of the first digits (proximal and distal phalanges) were noted. jointjoint was was in in acute acute flexion. flexion. One One metacarpal metacarpal bone, bone, dorsal dorsal and and ventral ventral sesamoids sesamoids and and two two phalangesphalangesThe distal of of the the epiphysis first first digits digits of (proximal (proximal the ulna andwas and distal articudistal phalanges)lated phalanges) with werethe were ulnar noted. noted. carpal bone and ac- cessoryThe bone. distal This epiphysis joint was of thein acute ulna cranialwas articu flexionlated showing with the a ulnar 180° rotationcarpal bone on the and axial ac- cessory bone. This joint was in acute cranial flexion showing a 180° rotation on the axial Animals 2021, 11, 813 6 of 12

The distal epiphysis of the ulna was articulated with the ulnar carpal bone and Animals 2021, 11, x accessory bone. This joint was in acute cranial flexion showing a 180◦ rotation on the 6 of 12

axial plane, with a mediocaudal rotation of the manus moving medial to the radio. One metacarpal bone and one dorsal sesamoid were noticed; we assumed a fusion of the two proximal phalanges resulting in one “stubby bone”. Two medial and distal phalanges wereplane, articulated with a withmediocaudal the stubby rotation bone. Clinical of the and manus radiographic moving findings medial were to consistentthe radio. One meta- withcarpal ectrodactyly. bone and one dorsal sesamoid were noticed; we assumed a fusion of the two prox- imalNo phalanges treatmentwas resulting considered in one at time “stubby for managing bone”. the Two congenital medial deformity. and distal phalanges were 2.5.articulated Case 3 with the stubby bone. Clinical and radiographic findings were consistent with ectrodactyly.A 10 months-old male dog was referred for an abnormal aspect of both front paws, not associatedNo withtreatment lameness. was Physical considered examination at time of fo ther managing involved limb the revealed congenital a deformity deformity. of the paw characterized by a cutaneous absence of normal separation between II–III digits and2.5. IV–V Case digits. 3 The right paw showed one metacarpal pad and three digital pads, whereas the leftA paw 10 showedmonths-old one metacarpal male dog pad was and referred two digital for pads an (Figureabnormal7). The aspect radiographic of both front paws, examination consisted of dorsopalmar view of the manus (Figure8). notIn associated the left manus, with a completelameness. bony Physical fusion betweenexamination proximal of the phalanges involved of the limb fourth revealed a de- andformity fifth digit of the was paw noted. characterized by a cutaneous absence of normal separation between II–IIIClinical digits and and radiographic IV–V digits. findings The wereright a paw simple sh completeowed one uncomplicated metacarpal syndactyly pad and three digital ofpads, the right whereas limb and the a complexleft paw incomplete showed one uncomplicated metacarpal syndactyly pad and of two the leftdigital limb. pads (Figure 7). TheThe radiographic dog had no evidenceexamination of discomfort, consisted so thatof dorsopalmar no treatment was view performed. of the manus (Figure 8).

FigureFigure 7. Case7. Case 3. Dorsal 3. Dorsal and Palmar and Palmar views of views both forelimbs. of both Rightforelimbs. manus Right (A,C) andmanus left manus (A,C) ( Band,D). left manus (B,D).

Figure 8. Case 3. Dorsopalmar radiograph (A) and drawing scheme (B) of the both forelimbs mal- formation. R: Radius; U: Ulna; RC: Radial Carpal Bone; UC: Ulnar Carpal Bone; CB: Carpal Bone; Animals 2021, 11, x 6 of 12

plane, with a mediocaudal rotation of the manus moving medial to the radio. One meta- carpal bone and one dorsal sesamoid were noticed; we assumed a fusion of the two prox- imal phalanges resulting in one “stubby bone”. Two medial and distal phalanges were articulated with the stubby bone. Clinical and radiographic findings were consistent with ectrodactyly. No treatment was considered at time for managing the congenital deformity.

2.5. Case 3 A 10 months-old male dog was referred for an abnormal aspect of both front paws, not associated with lameness. Physical examination of the involved limb revealed a de- formity of the paw characterized by a cutaneous absence of normal separation between II–III digits and IV–V digits. The right paw showed one metacarpal pad and three digital pads, whereas the left paw showed one metacarpal pad and two digital pads (Figure 7). The radiographic examination consisted of dorsopalmar view of the manus (Figure 8).

Animals 2021, 11, 813 7 of 12 Figure 7. Case 3. Dorsal and Palmar views of both forelimbs. Right manus (A,C) and left manus (B,D).

Animals 2021, 11, x 7 of 12

1–4: Distal Carpal Bones; MC: Metacarpal Bone; PP: Proximal Phalange; MP: Middle Phalange; DP: Distal Phalange; DS: Dorsal Sesamoid; S: Sesamoid Bone.

In the left manus, a complete bony fusion between proximal phalanges of the fourth and fifth digit was noted.

Clinical and radiographic findings were a simple complete uncomplicated syndac- FiguretylyFigure of 8. 8. theCase Case right 3. 3. DorsopalmarDorsopalmar limb and radiographa radiograph complex (A ()incompleteA and) and drawing drawing uncomplicated scheme scheme (B) ( ofB) theof the both syndactyly both forelimbs forelimbs of themal- left limb. formation. R: Radius; U: Ulna; RC: Radial Carpal Bone; UC: Ulnar Carpal Bone; CB: Carpal Bone; malformation.The dog R: Radius; had no U: Ulna; evidence RC: Radial of Carpaldiscomfort, Bone; UC: so Ulnar that Carpal no treatment Bone; CB: Carpal was Bone; performed. 1–4: Distal Carpal Bones; MC: Metacarpal Bone; PP: Proximal Phalange; MP: Middle Phalange; DP: Distal Phalange; DS: Dorsal Sesamoid; S: Sesamoid Bone. 2.6. Case 4 2.6. Case 4 A one-year-old male dog was referred for right forelimb lameness. Physical exami- A one-year-old male dog was referred for right forelimb lameness. Physical examina- tionnation revealed revealed a deformity a deformity of the paw of characterized the paw charac by the presenceterized ofby only the two presence digits and of a only two digits “cleftand handa “cleft aspect”. Two aspect”. digital padsTwo in digital each paw pads and in one each carpal paw pad and in the one palmar carpal view pad in the palmar wereview observed were observed (Figure9). (Figure The radiographic 9). The radiogra examinationphic consisted examination of the dorsopalmar consisted of the dorsopal- viewmar of view the right of the manus. right (Figure manus. 10). (Figure 10).

FigureFigure 9. Case9. Case 4. Dorsal 4. Dorsal (A) and and palmar Palmar (B) viewsviews of of the the right right forelimb. forelimb. Note the deformity of the paw with only two digits and a “cleft hand aspect”.

Figure 10. Case 4. Dorsopalmar radiograph (A) and drawing scheme (B) of the right forelimbs malformation. R: Radius; U: Ulna; RC: Radial Carpal Bone; UCB: ulnar Carpal Bone; AC: Acces- sory Bone; SB: Sesamoid Bone; CB: Carpal Bone; MC: Metacarpal Bone; PP: Proximal Phalange; MP: Middle Phalange; DP: Distal Phalange; DS: Dorsal sesamoid; PSB: Proximal Sesamoid Bone.

On X-ray, normal radius and ulna bones, deformed radial and ulnar carpal bones, small and deformed carpal bones and the presence of only two complete digits articulated Animals 2021, 11, x 7 of 12

1–4: Distal Carpal Bones; MC: Metacarpal Bone; PP: Proximal Phalange; MP: Middle Phalange; DP: Distal Phalange; DS: Dorsal Sesamoid; S: Sesamoid Bone.

In the left manus, a complete bony fusion between proximal phalanges of the fourth and fifth digit was noted. Clinical and radiographic findings were a simple complete uncomplicated syndac- tyly of the right limb and a complex incomplete uncomplicated syndactyly of the left limb. The dog had no evidence of discomfort, so that no treatment was performed.

2.6. Case 4 A one-year-old male dog was referred for right forelimb lameness. Physical exami- nation revealed a deformity of the paw characterized by the presence of only two digits and a “cleft hand aspect”. Two digital pads in each paw and one carpal pad in the palmar view were observed (Figure 9). The radiographic examination consisted of the dorsopal- mar view of the right manus. (Figure 10).

Animals 2021, 11, 813 8 of 12

Figure 9. Case 4. Dorsal and Palmar views of the right forelimb.

FigureFigure 10. 10.Case Case 4. 4. Dorsopalmar Dorsopalmar radiograph radiograph (A )(A and) and drawing drawing scheme scheme (B) of(B the) of right the right forelimbs forelimbs malformation.malformation. R: Radius;R: Radius; U: Ulna; U: Ulna; RC: RadialRC: Radial Carpal Carpal Bone; UCB:Bone; ulnar UCB: Carpal ulnar Bone; Carpal AC: Bone; Accessory AC: Acces- Bone;sory SB:Bone; Sesamoid SB: Sesamoid Bone; CB: Bone; Carpal CB: Bone;Carpal MC: Bone; Metacarpal MC: Metacarpal Bone; PP: Bone; Proximal PP: Phalange;Proximal MP:Phalange; MiddleMP: Middle Phalange; Phalange; DP: Distal DP: Phalange; Distal Phalange; DS: Dorsal DS: sesamoid; Dorsal PSB: sesamoid; Proximal PSB: Sesamoid Proximal Bone. Sesamoid Bone.

OnOn X-ray, X-ray, normal normal radius radius and and ulna ulna bones, bones, deformed deformed radial andradial ulnar and carpal ulnar bones, carpal bones, smallsmall and and deformed deformed carpal carpal bones bones and theand presence the presence of only of two only complete two complete digits articulated digits articulated with carpal bones of the distal line, were noticed. A digit showed one supernumerary footpad, instead the other finger a hypoplasic footpad. Clinical and radiographic find- ings were consistent with ectrodactyly. No treatment was performed for managing the bone deformity.

3. Discussion In veterinary medicine, Nomina Embryologica Veterinaria (NEV) (2017) is the only classification system recognized that allows classifying many congenital limb malforma- tions. However, it needs to be expanded in order to improve and facilitate communication about the specific characteristics of congenital anomalies in animals [3,19–21]. It only lists malformations, without defining and describing them, and some deformities are listed more than once under different names. The NEV is not canine specific. This is one reason why manuscripts such as the current work are important. In this study we reported the clinical and radiological patterns of four appendicular skeletal in canine species. Clinical observation is only the first step in the diagnosis of bone malformations, so that radiographic evaluations are essential to evaluate the extent of deficits. In case 1, a malformation involving the antebrachium and carpal bones and paw of the right thoracic limb was reported. An additional feature was the presence of a floating digit-like structure without any bony attachment to the elbow joint. This congenital defect was identify as postaxial terminal longitudinal ulnar hemimelia. To the authors’ best knowledge, no similar deformities have been reported in dogs, other species or , although a variable degree of ulna and digit deficiency has been observed in the latter [22,23]. This can make description difficult. The dog showed unilateral ulnar defect associated with other congenital alterations involving the carpus, both medial and lateral digital rays and the elbow joint. It was consistent with previous reports of human ulnar longitudinal deficiency [21,24]. In case n.2 and 4, a diagnosis of ectrodactyly was performed, according to clinical cases of limb malformations previously described [9,25]. In both cases, radiography permitted detection of the absence or hypoplasia of phalangeal bones, , carpal bones Animals 2021, 11, 813 9 of 12

and the hard tissues fusion or separation [26–29]. Splitting of the skin and soft tissues between radius and ulna to the level of the proximal third of the antebrachium was the prominent feature in case 2. The absence of three digits associated with a deep, v-shaped, excessive interdigital space between the remainders was the main finding in case 4. In case 3, a diagnosis of syndactyly of the pectoral limbs was performed. To our knowledge, no report of simple complete uncomplicated syndactyly of the right forelimb and complex incomplete uncomplicated syndactyly of the left forelimb exists, as described in this report. Over time, the term “hemimelia” has been adopted for better specifying congenital deficits of limbs, where one or more bones were totally or partially missing [2,17]. In veterinary medicine, different patterns of this malformation were classified as hemimelia terminal, when all or parts of the middle and distal bones were absent and hemimelia intercalary when segments of the middle portion of the limb were lacking, while the located proximally and distally structures developed normally [30]. Each of these latter varieties, in turn, is also qualified as transverse or longitudinal, depending on whether bones are missing across the limb’s width or along the preaxial/postaxial side of the limb [31]. Canine defects of the medial and central rays of the limb bud have been previously described and named as radial hemimelia and ectrodactyly [14,17,26]. Moreover, both ulnar ray abnormalities confined to the paw and ulnar ray defects as partial symptoms of other malformations have been also reported in canine species [9,26,32]. In canine medicine, the term hemimelia has previously proved useful to identify which segments of the limb were misshapen or missing [17]. However, the term postaxial terminal longitudinal ulnar hemimelia is not sufficient to provide a complete description of the range of abnormalities occurred in the paw, and elbow in the present case. When describing the present dysmorphology, particular attention should be taken in reporting not only ulnar-side defects, but also the absence of metacarpal bone and phalanges of the first digit. In humans, some studies permitted detection and classification of complex forms of ulnar longitudinal deficiencies, such as those characterized by the presence of radial-side abnormalities of the manus [33]. Moreover, amongst the manus abnormalities, and first web deficiencies are noted frequently in congenital defects of bony and soft tissue elements of the forearm ulnar border. In these cases, thumb defects are recognized as a surgical priority because of the importance of restoring the opposition function [33]. In dogs, the first digit is not part of the weightbearing surface of the limb and does not exert the function of grasping items. Dogs bear weight on digits II to V, with main weight bearing occurring on digits III and IV, so that it may be possible to bear body weight without the fourth digit [34]. The term “ectrodactyly” means one or more digits are missing or not fully developed, even though in veterinary medicine this term was also used to indicate a median distal cleft of the limb [9,12,14,35]. This condition is very heterogeneous, due to the different mor- phological features. Clinical diversity occurs not only between animals, but also between legs of the same subject. The deformity is usually unilateral and may be associated with soft tissue , limited range of motion in the carpus and elbow luxation [26,36]; it is also associated with concurrent vertebral malformation [9]. Some authors reported that soft tissue separation involves the metacarpus, whilst distal cleft of the limb extended up the carpus joint occurs sporadically in dogs [36]. Few cases of complete parasagittal plane separation of the antebrachium between medial and lateral segments have been previously described [26,37]. Surgical therapy should be performed to relieve pain, guaranteeing aesthetic and functional recovery and preventing progressive limb deformities [14,26,38]. For this kind of malformation, the use of the generic term ectrodactyly does not aid in planning of treatment because it is used to identify different anomalies, such as and cleft of the , paw or limb [14]. Schistomelia is another term listed in Animals 2021, 11, 813 10 of 12

Nomina Embryologica Veterinaria [20] that refers to the split of the limb. However, this definition has never been mentioned in previous reports. Other terms such as and aphalangia have been used to describe malformations of the distal limb in veterinary medicine [3,10,17]. In case 3, the diagnosis of syndactyly of the pectoral limbs was based on the human nomenclature, already widely accepted in veterinary medicine. A simple syndactyly occurs when adjacent digits are merged only by skin and soft tissue. A complex syndactyly is characterized by the lack of separation of hard tissues, in addition to skin and soft tissue abnormalities. Syndactyly may further be qualified as complete, when digits are interconnected throughout their entire length, and uncomplete when total connection of adjacent digits does not occur. If other anomalies are associated with syndactyly, the term complicated syndactyly may be adopted, whereas the definition of uncomplicated syndactyly should be used otherwise [39–41]. Previous reports treated several patterns of this congenital defect in dog [3,17,35,39,42,43]. Although little is known about the basic mechanisms of congenital limb deformities, several aetiological factors have been identified [44]. Causes of very similar anomalies to those described in the present case reports include genetic defects, administration of chemotherapeutics, malnutrition (lack of riboflavin), intake of drugs such as thalidomide or corticosteroids (in chick embryos), transplacental virus infections and X-rays [45–47]. Other causes of distal limb absence in young animals include strangulation by restrictive bands, in utero accidents and postnatal trauma [48]. In our cases, there was no information concerning traumatic events, inbreeding and/or environmental or genetic factors, so that the aetiology of these abnormalities remains unknown.

4. Conclusions This report improves the literature about congenital limb deformities, describing the patterns of rarely reported lesions and discussing how difficult it is to know the correct identification and classification. A well-defined classification scheme of congenital dysmorphologies of the forelimb is advisable. Novel nomenclature should take into consideration both the genetic basis and the wide spectrum of morphological features of limb dysostosis. Extrapolation from the human literature has been considered of limited value [14] but in our opinion it may serve some important cues. Likely, the real prevalence of these conditions in companion animals is little known; therefore, further reports are required.

Author Contributions: Conceptualization, F.M. and V.A.; methodology, F.M. and S.M.; software, G.C.; validation, F.M., S.D.P. and V.A.; formal analysis, L.C.; investigation, F.M. and S.D.P.; resources, G.C.; data curation, G.S.R., L.C. and G.C.; writing—original draft preparation, S.D.P., F.M.; writing— review and editing, S.D.P., F.M., S.M.; visualization, G.S.R.; supervision, V.A., F.M., S.D.P., S.M., L.C. and G.C. All authors have read and agreed to the published version of the manuscript. Funding: This research received no external funding. Institutional Review Board Statement: No ethical approval was required in compliance with Euro- pean Directive 2010/63/UE and Italian Regulation D.Lgs n. 26/2014 because all the data derived from routine veterinary clinical practices. Informed Consent Statement: Informed consent was obtained from all subjects involved in the study. Data Availability Statement: The data presented in this study are available on request from the corresponding author. Conflicts of Interest: The authors declare no conflict of interest. Animals 2021, 11, 813 11 of 12

References 1. Breur, G.J.; Lust, G.; Todhunter, R.J. Genetics of canine dysplasia and other orthopaedic traits. In The Genetics of the Dog; CABI Publishing: Wallingford, UK, 2009; pp. 267–298. 2. Towle, H.A.M.; Breur, G.J. Dysostoses of the canine and feline appendicular . J. Am. Vet. Med. Assoc. 2004, 225, 1685–1692. [CrossRef][PubMed] 3. Di Dona, F.; Della Valle, G.; Meomartino, L.; Lamagna, F.; Fatone, G. Congenital deformity of the distal extremities in three dogs. Open Vet. J. 2016, 6, 228–233. [CrossRef] 4. Ruvinsky, A. Developmental Genetics. In The Genetics of the Dog; Ruvinsky, A., Sampson, J., Eds.; CAB International: Wallingford, UK, 2001. 5. Gilbert, S.F. Development of the limb. In Developmental , 7th ed.; Sinauer Associates Inc.: Sunderland, MA, USA, 2003. 6. Noden, D.; De Lahunta, A. In The Embryology of Domestic Animals: Developmental Mechanisms and Malformations; Noden, D.M., De Lahunta, A., Eds.; Williams & Williams Co.: Baltimore, MD, USA, 1985; pp. 196–221. 7. Blevins, W.E.; Breur, G.J.; Kim, J. Morphological and functional evaluation of a dog with dimelia. Vet. Comp. Orthop. Traumatol. 2006, 19, 255–258. [CrossRef] 8. Montgomery, R.; McEwen, V.; Lockwood, A. Bilateral radial hemimelia, and cardiomegaly in two cats. Vet. Comp. Orthop. Traumatol. 2009, 22, 511–513. [CrossRef][PubMed] 9. Carvallo, F.R.; Domínguez, A.S.; Morales, P.C. Bilateral ectrodactyly and spinal deformation in a mixed-breed dog. Can. Vet. J. 2011, 52, 47–49. 10. Macrì, F.; Lanteri, G.; Rapisarda, G.; Marino, F. Unilateral forelimb partial aphalangia in a kitten. J. Feline Med. Surg. 2012, 14, 272–275. [CrossRef][PubMed] 11. Pisoni, L.; Cinti, F.; Del Magno, S.; Joechler, M. Bilateral radial hemimelia and multiple malformations in a kitten. J. Feline Med. Surg. 2012, 14, 598–602. [CrossRef] 12. Wrzosek, M.; Płonek, M.; Zeira, O.; Biezy´nski,J.;˙ Kinda, W.; Guzi´nski,M. Congenital bipartite atlas with hypodactyly in a dog: Clinical, radiographic and CT findings. J. Small Anim. Pr. 2014, 55, 375–378. [CrossRef] 13. Macrì, F.; De Majo, M.; Rapisarda, G.; Mazzullo, G. Two cases of feline : Autopodium ectromelia associated with humero-ulnar and zeugopodium ectromelia. J. Feline Med. Surg. 2009, 11, 731–734. [CrossRef] 14. Barrand, K.R. Ectrodactyly in a West Highland white terrier. J. Small Anim. Pract. 2004, 45, 315–318. [CrossRef] 15. Alam, M.R.; Heo, S.Y.; Lee, H.B.; Kim, J.H.; Park, Y.J.; Lee, K.C.; Choi, I.H.; Kim, N.S. Preaxial longitudinal intercalary radial hemimelia in a dog: A case report. Vet. Med. 2006, 51, 118–123. 16. Macrì, F.; Marino, F.; Rapisarda, G.; Lanteri, G.; Mazzullo, G. A Case of Unilateral Pelvic Limb Adactyly in a Puppy Dog. Anat. Histol. Embryol. 2010, 40, 104–106. [CrossRef] 17. Macrì, F.; Ciotola, F.; Rapisarda, G.; Lanteri, G.; Albarella, S.; Aiudi, G.; Liotta, L.; Marino, F. A rare case of simple syndactyly in a puppy. J. Small Anim. Pr. 2013, 55, 170–173. [CrossRef][PubMed] 18. Macrì, F.; Di Pietro, S.; Palumbo Piccionello, A.; Rapisarda, G.; Lanteri, G.; Angileri, V.; Marino, F. A rare case of partial paraxial radial hemimelia in a puppy: A case report. Vet. Med. 2017, 62, 681–684. [CrossRef] 19. Cornillie, P.; Van Lancker, S.; Simoens, P. Two Cases of Brachymelia in Cats. Anat. Histol. Embryol. 2004, 33, 115–118. [CrossRef] 20. World Association of Veterinary Anatomists. Nomina Embryologica Veterinaria (Second Edition). 2017. Available online: http://www.wavaamav.org/Downloads/nev_2017.pdf (accessed on 8 March 2021). 21. Ogino, T. Clinical features and teratogenic mechanisms of congenital absence of digits. Dev. Growth Differ. 2007, 49, 523–531. [CrossRef] 22. Kornak, U.; Mundlos, S. Genetic Disorders of the Skeleton: A Developmental Approach. Am. J. Hum. Genet. 2003, 73, 447–474. [CrossRef][PubMed] 23. Al-Qattan, M.; Al-Sahabi, A.; Al-Arfaj, N. Ulnar Ray Deficiency: A Review of the Classification Systems, the Clinical Features in 72 Cases, and Related Developmental Biology. J. Hand Surg. 2010, 35, 699–707. [CrossRef][PubMed] 24. Afzal, M.; Malik, S. Longitudinal deficiency of : Similar case presentation of two subjects with unilateral ulnar hemimelia, carpal and metacarpal deficiency, and severe oligodactyly. Asian Biomed. 2014, 8, 569–575. [CrossRef] 25. Lee, M.-I.; Kwak, H.-H.; Kim, J.-H.; Shin, H.-S.; Woo, H.-M.; Kang, B.-J. Surgical Ectrodactyly Repair Using Limb-lengthening and Bone Tissue Engineering Techniques in a Toy Dog Breed. In Vivo 2020, 34, 815–824. [CrossRef] 26. McKee, W.M.; Mitchell, R.A.S.; Innes, J.F.; Lascelles, B.D.X.; Johnson, K.A. Surgical reconstruction of ectrodactyly deformity in four dogs. Vet. Comp. Orthop. Traumatol. 2001, 14, 201–209. [CrossRef] 27. Ferreira, M.P.; Alievi, M.M.; Dal-Bó, I.D.S.; Nóbrega, F.S.; Gonzalez, P.C.S.; Beck, C.A.D.C. Surgical management of ectrodactyly in a dog. Semina Ciências Agrárias 2016, 37, 891. [CrossRef] 28. Tchaprazov, T.; Kostov, D.; Vladova, D. A case of ectrodactyly in a chow chow dog. Trakia. J. Sci. 2007, 5, 69–72. 29. Harasen, G. Surgical management of ectrodactyly in a Siberian husky. Can. Vet. J. La Rev. Vet. Can. 2010, 51, 421–424. 30. Frantz, C.H.; O’Rahilly, R. Ulnar hemimelia. Artif. Limbs 1971, 15, 25–35. [PubMed] 31. Towle, H.A.; Breur, G.J. Miscellaneous orthopedic conditions. In Veterinary : Small Animal; Tobias, K.M., Johnston, S.A., Eds.; Elsevier Saunders: St. Louis, MI, USA, 2012; Volume 1, pp. 1112–1126. Animals 2021, 11, 813 12 of 12

32. Alonso, R.A.; Hernandez, A.; Diaz, P.; Cantú, J.M. An autosomal recessive form of hemimelia in dogs. Vet. Rec. 1982, 110, 128–129. [CrossRef][PubMed] 33. Cole, R.J.; Manske, P.R. Classification of ulnar deficiency according to the thumb and first web. J. Hand Surg. 1997, 22, 479–488. [CrossRef] 34. Riegger-Krugh, C.; Millis, D.L.; Weigel, J.P. Canine Anatomy. In Canine Rehabilitation and Physical Therapy, 2nd ed.; WB Saunders Co.: St. Louis, MO, USA, 2014; pp. 41–78. 35. Pratschke, K. A case of ectrodactyly in a dog. Irish. Vet. J. 1996, 49, 412–413. 36. Carrig, C.; Wortman, J.; Morris, E.; Blevins, W.; Root, C.; Hanlon, G.; Suter, P. Ectrodactyly (split-) in the dog. Vet. Radiol. 1981, 22, 123–144. [CrossRef] 37. Mehrjerdi, H.K.; Hayati, F.; Sardari, K.; Mirshahi, A.; Gachpaz, S. Ectrodactyly in a mix breed dog. Iran. J. Vet. Surg. 2008, 3, 87–91. 38. Pisoni, L.; Del Magno, S.; Cinti, F.; Dalpozzo, B.; Bellei, E.; Cloriti, E.; Joechler, M. Surgical induction of metacarpal synostosis for treatment of ectrodactyly in a dog. Vet. Comp. Orthop. Traumatol. 2014, 27, 166–171. [CrossRef][PubMed] 39. Towle, H.; Friedlander, K.; Ko, R.; Aper, R.; Breur, G. Surgical treatment of simple syndactylism with secondary deep digital flexor tendon in a Basset Hound. Vet. Comp. Orthop. Traumatol. 2007, 20, 219–223. [CrossRef] 40. Kozin, H.S. Syndactyly. J. Hand Surg. 2001, 1, 1–13. [CrossRef] 41. Dao, K.D.; Shin, A.Y.; Billings, A.; Oberg, K.C.; Wood, V.E. Surgical Treatment of Congenital Syndactyly of the Hand. J. Am. Acad. Orthop. Surg. 2004, 12, 39–48. [CrossRef][PubMed] 42. Richardson, E.F.; Wey, P.D.; Hoffman, L. Surgical management of syndactyly in a dog. J. Am. Vet. Med. Assoc. 1994, 205, 1149–1151. 43. Schultz, V.; Watson, A.G. Lumbosacral transitional and thoracic limb malformations in a Chihuahua puppy. J. Am. Anim. Hosp. Assoc. 1995, 31, 101–106. [CrossRef] 44. Gilbert, S.F. Development Biology, 6th ed.; Sinauer Assoc. Inc.: Sunder land, MA, USA, 2000. 45. Johnson, E.M. Nutritional factors in mammalian . In Teratology, Principles and Techniques; Wilson, J.G., Warkany, J., Eds.; The University of Chicago Press: Chicago, IL, USA, 1965; pp. 113–130. 46. Karnofsky, D.A. Mechanism of action of certain grow—thinhibiting drugs. In Teratology, Principles and Techniques; Wilson, J.G., Warkany, J., Eds.; The University of Chicago Press: Chicago, IL, USA, 1965; pp. 185–214. 47. Warkany, J. Development of experimental mammalian teratology. In Teratology, Principles and Techniques; Wilson, J.G., Warkany, J., Eds.; The University of Chicago Press: Chicago, IL, USA, 1965; pp. 1–20. 48. Johnson, K.A.; Watson, A.D.J.; Page, R.L. Skeletal diseases. In Textbook of Veterinary Internal Medicine, 4th ed.; Ettinger, S.J., Feldman, E.C., Eds.; W.B. Saunders: Philadelphia, PA, USA, 1995; pp. 2077–2102.