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Morphometric data on the accessory ligament of the deep digital flexor tendon in the equine hindlimb
The Veterinary Journal 184 (2010) 298–302
Contents lists available at ScienceDirect
The Veterinary Journal journal homepage: www.elsevier.com/locate/tvjl
Morphometric data on the accessory ligament of the deep digital flexor tendon in the equine hindlimb q Sofie Muylle a,*, Katrien Vanderperren b, Jimmy Saunders b, Paul Simoens a a b
Department of Morphology, Faculty of Veterinary Medicine, Ghent University, Salisburylaan 133, B-9820 Merelbeke, Belgium Department of Medical Imaging of Domestic Animals and Small Animal Orthopaedics, Ghent University, Salisburylaan 133, B-9820 Merelbeke, Belgium
a r t i c l e
i n f o
Article history: Accepted 29 May 2009
Keywords: Accessory ligament Deep digital flexor tendon Hindlimb Morphology Horse
a b s t r a c t Desmopathy of the accessory ligament of the deep digital flexor tendon (ALDDFT) in the hindlimb has recently been described as a cause of lameness in horses. However, there is limited morphometric data on this ligament. In the present study, the ALDDFT was carefully dissected in 165 hindlimbs that were collected from an abattoir. Length, width (lateral-to-medial) and thickness (plantar-to-dorsal) of the ligament were measured. It was found that the ALDDFT may be absent in a minority of horses, but when it was present the general morphology was variable. The ALDDFT can be a single rectilinear structure ranging from slender or poorly developed to quite large and can be divided, in part or in its entirety, into two or three bundles. Ó 2009 Elsevier Ltd. All rights reserved.
Introduction The accessory ligament of the deep digital flexor tendon (ALDDFT) in the horse is a reinforcing ligament that originates from the plantar (palmar) fibrous joint capsule of the tarsus (carpus), courses distally between the suspensory ligament (SL) and the deep digital flexor tendon (DDFT) and inserts on the dorsal surface of the DDFT in the mid-metatarsal (metacarpal) region. In the pelvic limb, the ALDDFT is poorly developed (Dyce et al., 1996), but in the forelimb it is of major importance as a part of the passive stay apparatus which enables the animal to maintain a standing posture with relatively little muscular exertion (Shively, 1983). During exercise, the ALDDFT of the forelimb shares tensile load with the DDFT and prevents overstretching of the latter by passively carrying the load during maximal extension of the distal interphalangeal and metacarpophalangeal joints, as seen in the second half of the support phase or when landing after a jump (Riemersma and De Bruyn, 1986; Swanstrom et al., 2004). Disorders of the ALDDFT in the front limb are a common cause of lameness in horses. Both the normal and the pathological ultrasonographic features of the ALDDFT have been extensively described (Pharr and Nyland, 1984; Genovese et al., 1986; Hauser, 1986; Dyson, 1991, 1992; McDiarmid, 1994; Reef, 1998a,b; Stashak, 2002a,b). In contrast, in the hindlimb desmopathy of the
q Parts of information in the text were presented at the European Veterinary Conference Voorjaarsdagen, Amsterdam, Netherlands, 2008 and at the European Veterinary Diagnostic Imaging Congress, Norway, 2008. * Corresponding author. Tel.: +32 9 264 77 11. E-mail address: sofi[email protected] (S. Muylle).
1090-0233/$ - see front matter Ó 2009 Elsevier Ltd. All rights reserved. doi:10.1016/j.tvjl.2009.05.026
ALDDFT is a less usual cause of lameness and data on its function, clinical importance and/or pathological changes were limited (Boswell and Schramme, 2000) until the recent descriptions by Eliashar et al. (2005) and Jorgensen et al. (2007). Descriptive and morphometric data on the normal anatomy of the tarsal ALDDFT are imprecise. Most anatomical textbooks simply indicate that the ALDDFT of the hindlimb is longer and more slender than its thoracic counterpart and that it maybe absent in some horses and in donkeys (Barone, 2000). However, specific information on length, width, thickness and macroscopic appearance of the ALDDFT in the pelvic limb is lacking. This study presents a macroscopic study of the size and development of the ALDDFT in the equine hindlimb. These data can be used to identify and recognise anatomical variations and pathological changes of this structure in clinical patients. Materials and methods One hundred and sixty-five isolated equine hindlimbs, amputated at the centrodistal joint, were obtained from an abattoir and were harvested from horses of unknown history of lameness. Limbs normal in appearance at inspection and palpation were selected. If any lesion was observed or if there was any suspicion of tendinous, ligamentous or bony abnormalities the limb was excluded. The breed, age and sex of the horses were not recorded, but all specimens were weighed and orientated (left/right) prior to dissection. Twelve hindlimbs of donkeys were also obtained from routine post mortem examinations at the department of Pathology at the Faculty of Veterinary Medicine, Ghent University. In all 177 specimens the flexor tendons were examined by palpation and subsequent dissection. A skin incision was made at the latero-plantar border of the superficial digital flexor tendon (SDFT), extending from the tarsal region to the fetlock joint. After the SDFT was detached and reflected, both the DDFT and the ALDDFT were carefully exposed and dissected. The proximo-distal length of the ALDDFT was measured from its origin at the plantar tarsometatarsal ligament to its fusion
S. Muylle et al. / The Veterinary Journal 184 (2010) 298–302 with the DDFT. The lateral-to-medial width of the ALDDFT was measured both at its origin at the plantar tarsometatarsal ligament at the base of the fourth metatarsal bone and more distally near the fusion with the DDFT. Measurements were carried out using a flexible measuring tape pressed against the plantar side of the ligament. In 65 specimens the plantar-to-dorsal thickness was measured near the origin of the ALDDFT at the base of the fourth metatarsal bone by means of Vernier callipers with a precision of 0.1 mm. All measurements were carried out by two people who independently evaluated the ALDDFT of every limb. Possible correlations between the weight of the limb and the length of the ALDDFT, its lateral-to-medial width (proximal and distal) and its thickness, and between the length of the ALDDFT, the lateral-to-medial width (proximal and distal) and the thickness were calculated.
Results The mean weight of the disarticulated equine limbs (n = 165) was 3.3 ± 0.86 kg, with a minimum of 1 kg and a maximum of 6.6 kg (median 3.3 kg). In 155 of the hindlimbs, the ALDDFT was clearly developed, whereas in 10 specimens no ALDDFT could be identified despite careful dissection and precise inspection (weight of the limbs without ALDDFT ranged from 1.9 to 6.6 kg, median 3.6 kg). No correlation was found between the weight of the limb and the presence or absence of ALDDFT. The ALDDFT was absent in all 12 donkey limbs. In all 155 limbs with an ALDDFT, the ligament was situated with its axis of symmetry slightly lateral to the axis of the third metatarsal bone. The ALDDFT tapered distally towards the fusion with the DDFT. The total length of the ALDDFT varied from 7.9 to 18.5 cm (median 14.1 cm) with a mean of 14.0 ± 2.1 cm. The total length of the disarticulated limbs was not measured, but the ALDDFT consistently merged with the DDFT in the second quarter of the metatarsal region. Proximally, the mean width of the ALDDFT measured 1.9 ± 1.2 cm (range 0.2–3.2 cm and median 1.8 cm) and distally 1.2 ± 1.0 cm (range 0.2–2.6 cm and median 1.1 cm). The mean plantar-to-dorsal thickness measured in 65 specimens, was 1.3 ± 0.6 mm (range 0.1–3.3 mm and median 1.1 mm).
299
No significant correlation (r = 0.06) was found between the weight of the limb and the length of the ALDDFT, nor was there a significant correlation between the weight of the limb and the proximal (r = 0.02) and/or distal width (r = 0) of the ALDDFT. There was no significant correlation between the weight of the limb and the plantar-to-dorsal thickness of the ALDDFT (r = 0.08), between the length of the ALDDFT and its proximal (r = 0.16) and/or distal width (r = 0.10), nor between the length of the ALDDFT and its plantar-to-dorsal thickness (r = 0). In 143 limbs the ALDDFT was a single, rectilinear structure but in 12 specimens it was, in part or in its entirety, divided into two or three ligaments. The branching pattern showed anatomical variations (Fig. 1). In six limbs, the ALDDFT consisted of two entirely separate ligaments (Fig. 1A) situated besides each other (Fig. 2A) or one on top of the other (Fig. 2B). The two parts of the split ALDDFT were not entirely symmetrical, but each had a specific length, width and thickness (Table 1). In two limbs, the ALDDFT started proximally as a single structure, but ramified between its origin and insertion in two separate ligaments of different lengths (Figs. 1B and 3). In one specimen, the ALDDFT was a single structure both at its origin and at its insertion on the DDFT, but was bifurcated in the free mid-zone (Fig. 1C). In another specimen, the ALDDFT was single at its origin, but trifurcated distally (Fig. 1D). In one limb the ALDDFT bifurcated both proximally and distally, but was undivided in the mid-zone (Fig. 1E). In one specimen the most proximal part of the ALDDFT consisted of two separate ligaments which fused to form a single structure distally (Fig. 1F). The 165 limbs were selected at random at an abattoir. They were left/right orientated, but it was not possible to arrange the feet in pairs belonging to the same horse and was therefore not known whether the development, size and branching pattern of the ALDDFT was symmetrical in both hindlimbs of a same individual.
Fig. 1. A–F. Schematic drawings of various ramification patterns of the accessory ligament of the deep digital flexor tendon (ALDDFT). Tibia (a), calcaneal tuber (b), fourth metatarsal bone (c), second metatarsal bone (d) and third metatarsal bone (e). Long lateral collateral ligament (1), long medial collateral ligament (2), long plantar ligament (3) and suspensory ligament (4), ALDDFT (AL).
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S. Muylle et al. / The Veterinary Journal 184 (2010) 298–302
Fig. 2A. Medio-plantar view of specimen 123. The accessory ligament of the deep digital flexor tendon (ALDDFT) consists of two entirely separate ligaments (arrowheads) situated beside one another. Superficial digital flexor tendon (SDFT) (1), deep digital flexor tendon (DDFT) (2), tendon of medial digital flexor (3) joining DDFT and suspensory ligament (SL) (4).
Discussion Whereas desmitis of the ALDDFT in the forelimb has been widely reported, injury of the ALDDFT in the hindlimb has been described as a rare or unusual finding (Reef, 1998b; Dyson, 2003). To the authors’ knowledge only a few cases have been described (Dyson, 1991; Boswell and Schramme, 2000; Eliashar et al., 2005; Jorgensen et al., 2007; Lamas et al., 2008). Several studies have
Fig. 2B. Latero-plantar view of specimen 113. The accessory ligament of the deep digital flexor tendon (ALDDFT) consists of two entirely separate ligaments of which the shorter and more slender ligament (arrowheads) is situated on the plantar side of the larger ligament (arrows). Superficial digital flexor tendon (SDFT) (1), deep digital flexor tendon (DDFT) (2), tendon of medial digital flexor (3) joining DDFT and suspensory ligament (SL) (4).
reported on the mechanical properties of the ALDDFT in the forelimb and concluded that the ALDDFT plays a primary role in supporting the thoracic limb. Passively, the ALDDFT contributes more to the limb support than do the muscles and it provides support during stance with minimal required muscle contraction (Swanstrom et al., 2004). The ALDDFT in the forelimb receives the second highest load of the palmar soft tissue structures (Jansen
Table 1 Morphometric data of the branched ALDDFT (n = 12). Specimen
Weight (kg)
Left/ right
Length (cm)
Proximal width (cm)
Distal width (cm)
29
3
R
116
3
R
123
3.7
L
152
3.9
R
159
3.8
L
163
2.1
R
27 63 24 68 18
2.9 3.7 2.9 3.8 2.8
L R R L L
11 17.1 12.5 13.5 16 15.5 10.5 11.4 12.7 13.6 9.6 11 16.3 11.2 18.2 14.8 11.2
0.8 1.13 0.9 0.4 0.3 0.2 1.2 1.5 0.9 0.9 0.5 1 1.9 2 2 2.5 1.6
0.3 0.8 0.7 0.2 0.2 0.2 0.9 1.1 0.4 0.5 0.2 0.6 0.7–0.5 0.4–0.3 1.7 0.8–1.2–0.5 0.3
155
2.4
L
15.4 14.2
1.6 0.4–1.2
1 1.2
Thickness (mm)
Branching of the ALDDFT Cleft over its entire length Cleft over its entire length
0.1 0.1 0.6 2 0.7 0.1 0.3 1
Cleft over its entire length Cleft over its entire length Cleft over its entire length Cleft over its entire length Bifurcated in the distal half Bifurcated in the distal half Bifurcated in the mid-part Trifurcated in the distal half Bifurcated proximally and distally, undivided in the midpart
1–0.3
AL cleft proximally
S. Muylle et al. / The Veterinary Journal 184 (2010) 298–302
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Fig. 3. Plantar view of specimen 27. ALDDFT ramifying between origin and insertion into two separate, well developed ligaments (arrowheads).
et al., 1993); it prevents hyperextension of the fetlock and facilitates carpal extension when the limb is loaded (Denoix, 1994; Mcllwraith, 2002). The ligament is under greatest loading during extension of the digit, either nearing the end of the stance phase or following landing over a fence (Meershoek et al., 2001). Studies on the mechanics of the ALDDFT in the hindlimb have not been performed. Eliashar et al. (2005) stated that the supporting function of the ALDDFT in the hindlimb is unclear but of minor importance. Back et al. (1995) and Eliashar et al. (2005) suggested that due to the reciprocal action of the tarsus, and compared to the antebrachium during stance, the ALDDFT in the hindlimb is probably under less tension in late stance. In a case report by Jorgensen et al. (2007) it was concluded that considering the slender structure of the ALDDFT in the hindlimb, together with its infrequent incidence of injury, it is probable that the forces imposed on the ligament are significantly lower than in the forelimb. In the thoracic limb, mean length of the ALDDFT (measured from the palmar carpal ligament to the fusion with the DDFT) was 13.7 ± 0.4 cm (Zarucco et al., 2004). Ultrasonographically, the lateral-to-medial width of this structure near its insertion level was 1.33 ± 0.4 cm in Arabian horses and 1.53 ± 0.5 cm in Thoroughbreds (Celimli et al., 2004), and varied from 1.8 ± 0.1 cm (Cuesta et al., 1995) to 1.97 ± 0.04 cm in Andalusian Anglo-Arabians (Reef, 1998b). The ultrasonographic palmar-to-dorsal thickness of the ALDDFT in the thoracic limb has been reported at 2.5 cm distal to the accessory bone and measured 0.83 ± 0.03 cm in Anglo–Arabian–Andalusian crossbred horses (Reef, 1998b). There is little information about the hindlimbs. Sisson and Grossman (1975) and Shively (1983) mention that the ALDDFT of the hind limb is longer, but more slender than its thoracic counterpart. According to Smith and Eliashar (2008), a normal ALDDFT in the hindlimb is usually <1 cm in width and approximately 2 mm in thickness but the authors do not say at what level the measurements were obtained. The results of the present study suggest that there was substantial morphometric variation in the dimensions of the ALDDFT. The length of the pelvic ALDDFT varied from 7.9 to 18.5 cm. Near its origin at the plantar tarsometatarsal ligament, the lateral-to-medial width of the ALDDFT varied from 0.2 to 3.2 cm and the plantar-to-dorsal thickness measured 0.1– 3.3 mm. Near the fusion with the DDFT, the lateral-to-medial width varied from 0.2 to 2.6 mm. The ALDDFT ranged from slender and poorly developed to large (Figs. 4 and 5). An awareness of the existence of variable ALDDFT dimensions may be useful
Fig. 4. Latero-plantar view of a right hindlimb with a slender accessory ligament of the deep digital flexor tendon (ALDDFT) (arrowheads). The lateral plantar neurovascular string is drawn back by tweezers. Superficial digital flexor tendon (SDFT) (1), deep digital flexor tendon (DDFT) (2) and suspensory ligament (SL) (4).
during an ultrasonographic examination of the metatarsal region in the horse, but the measurements of the present study do not provide accurate or definitive morphometric criteria as there was no information available about the age, breed or size of the horses. Unfortunately, there was no clinical history for these animals, and it was also not known whether some of the limbs may or may not have been paired. In the thoracic limb, the development of the ALDDFT is believed to be breed-dependent, with much better development in heavy draught horses compared to saddle animals (Nickel et al., 1986). According to van den Belt (1995), differences in ALDDFT dimensions in the forelimb are related to breed, age, bodyweight (BW) and height at the withers. Celimli et al. (2004) reported that breed-related body conformation and training appeared to have a greater influence on ligament and tendon dimensions than age, BW and height. In the present study breed, age, BW and trainingstatus of the horses were unknown. There was no significant correlation, however, between the weight of the disarticulated hindlimbs and the dimensions of the ALDDFT. The ALDDFT was absent in 6% of the examined hindlimbs, but no correlation could be found between the weight of the limb and the presence or absence of an ALDDFT. The ALDDFT was missing in some lighter weight hindlimbs (1.9 kg, 2.3 kg and 2.5 kg), but also in two of the heaviest specimens (6.2 kg and 6.6 kg). The results confirmed the assumption of Barone (2000) and Reef (1998b) that the ALDDFT of the hindlimb may be absent in some horses, but contradicted the statement of Smith and Eliashar (2008) who suggested that the ALDDFT in the hindlimb is present in every horse. The current study also confirmed the findings reported by Barone (2000), in a more limited study (n = 12) that the ALDDFT was absent in donkeys.
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S. Muylle et al. / The Veterinary Journal 184 (2010) 298–302
Fig. 5. Latero-plantar view of a left hindlimb with a well developed ALDDFT (arrowheads). The lateral plantar neurovascular string is drawn back by forceps. Superficial digital flexor tendon (SDFT) (1), deep digital flexor tendon (DDFT) (2), tendon of medial digital flexor (3) joining DDFT and suspensory ligament (SL) (4).
Conclusions The results of this limited study have demonstrated that the morphology of the ALDDFT in the hindlimb is variable. Irrespective of the limb’s weight, the ALDDFT may be absent or very slender and poorly developed, but it can also be prominent. The variations in length, width, thickness and general development of the ALDDFT in the hindlimb should be noted during a clinical and, in particular, during ultrasonographic examination of the lame horse. The existence of this variable morphology combined with the lack of literature data describing consequent malfunctions suggests that both the presence and the size of the ALDDFT are of minor importance as far as the supporting function in the hindlimb is concerned. Conflict of interest statement None of the authors of this paper has a financial or personal relationship with other people or organisations that could inappropriately influence or bias the content of this paper. Acknowledgements The authors wish to acknowledge Patrick Vervaet for his dedicated technical assistance. Ward De Spiegelaere is acknowledged for his professional advice. References Back, W., Schamhardt, H.C., Savelberg, H.H., van den Bogert, A.J., Bruin, G., Hartman, W., Barneveld, A., 1995. How the horse moves: 2. Significance of graphical
representations of equine hindlimb kinematics. Equine Veterinary Journal 27, 39–45. Barone, R., 2000. Arthrologie et myologie. In: Anatomie comparée des Mammifères Domestiques. Tome second, 4ième edn. Vigot, Paris, pp. 791–793. Boswell, J.C., Schramme, M.C., 2000. Desmitis of the accessory ligament of the deep digital flexor tendon in the hindlimb in a horse. Equine Veterinary Education 12, 129–132. Celimli, N., Seyrek-Intas, D., Kaya, M., 2004. Morphometric measurements of flexor tendons and ligaments in Arabian horses by ultrasonographic examination and comparison with other breeds. Equine Veterinary Education 16, 81–85. Cuesta, I., Riber, C., Pinedo, M., Gata, J.A., Castejon, F., 1995. Ultrasonographic measurement of palmar metacarpal tendon and ligament structures in the horse. Veterinary Radiology and Ultrasound 36, 131–136. Denoix, J.M., 1994. Functional anatomy of tendons and ligaments in the distal limbs (manus et pes).Veterinary Clinics of North America. Equine Practice 10, 273– 322. Dyce, K.M., Sack, W.O., Wensing, C.J.G., 1996. The hindlimb of the horse. In: Textbook of Veterinary Anatomy, second ed. W.B. Saunders, Philadelphia, pp. 611–630. Dyson, S.J., 1991. Desmitis of the accessory ligament of the deep digital flexor tendon: 27 cases (1986–1990). Equine Veterinary Journal 23, 438–444. Dyson, S.J., 1992. Ultrasonographic examination of the metacarpal and metatarsal regions in the horse. Equine Veterinary Education 4, 139–144. Dyson, S.J., 2003. Desmitis of the accessory ligament of the deep digital flexor tendon. In: Roos, M.W., Dyson, S.J. (Eds.), Diagnosis and Management of Lameness in the Horse. W.B. Saunders, Philadelphia, pp. 650–653. Eliashar, E., Dyson, S.J., Archer, R.M., Singer, E.R., Smith, R.K.W., 2005. Two clinical manifestations of desmitis of the accessory ligament of the deep digital flexor tendon in the hindlimb of 23 horses. Equine Veterinary Journal 37, 495–500. Genovese, R.L., Rantanen, N.W., Hauser, M.L., Simpson, B.S., 1986. Diagnostic ultrasonography of equine limbs. Veterinary Clinics of North America: Equine Practice 2, 145–226. Hauser, M.L., 1986. Ultrasonographic appearance and correlative anatomy of the soft tissues of the distal extremities in the horse. Veterinary Clinics of North America: Equine Practice 2, 127–144. Jansen, M.O., van den Bogert, A.J., Riemersma, D.J., Schamhart, H.C., 1993. In vivo tendon forces in the forelimb of ponies at the walk, validated by ground reaction force measurements. Acta Anatomica 146, 162–167. Jorgensen, A.J.R., Seco Diaz, O., Reef, V., 2007. Ultrasonographic diagnosis – desmitis of the accessory ligament of the deep digital flexor tendon in a hindlimb in a horse. Veterinary Radiology and Ultrasound 49, 303–306. Lamas, L.P., Henson, F.M.D., Kidd, J.A., 2008. Desmectomy of a septic accessory ligament of the deep digital flexor tendon in the hindlimb of a horse under standing sedation. Equine Veterinary Education 20, 620–624. McDiarmid, A.M., 1994. Eighteen cases of desmitis of the accessory ligament of the deep digital flexor tendon. Equine Veterinary Education 6, 49–56. Mcllwraith, W.C., 2002. Diseases of joints, ligaments and tendon sheaths. In: Stashak, T.S., (Ed.), Adams’ Lameness in Horses, fifth ed. Lippincott Williams and Wilkins, Philadelphia, pp. 494–640.. Meershoek, L.S., Schamhardt, H.C., Roepstorff, L., Johnston, C., 2001. Forelimb tendon loading during jump landings and the influence of fence height. Equine Veterinary Journal, 6–10. Nickel, R., Schummer, A., Seiferle, E., Wilkens, H., Will, H., Frewein, J., 1986. The locomotor system of the domestic mammals. The Anatomy of the Domestic Animals, vol. 1. Verlag P. Parey, Berlin-Hamburg, p. 388. Pharr, J.W., Nyland, T.G., 1984. Sonography of equine palmar metacarpal soft tissues. Veterinary Radiology 25, 265–273. Reef, V.B., 1998a. Physics and instrumentation. In: Equine Diagnostic Ultrasound. W.B. Saunders, Philadelphia, pp. 1–2. Reef, V.B., 1998b. Musculoskeletal ultrasonography. In: Equine Diagnostic Ultrasound. W.B. Saunders, Philadelphia, pp. 48–49. pp. 56–59, pp. 95–99. Riemersma, D.J., De Bruyn, P., 1986. Variations in cross-sectional area and composition of equine tendons with regard to their mechanical function. Research in Veterinary Science 41, 7–13. Shively, M.J., 1983. Functional and clinical significance of the check ligaments. Equine Practice 5, 37–42. Sisson, S., Grossman, J.D., 1975. Equine myology, fifth ed. The Anatomy of the Domestic Animals, vol. 1 W.B. Saunders, Philadelphia, p. 451. Smith, R.K.W., Eliashar, E., 2008. Size isn’t everything: the importance of the hindlimb accessory ligament of the deep digital flexor tendon. Equine Veterinary Education 20, 625–626. Stashak, T.S., 2002a. Functional anatomy of equine locomotor organs. In: Adams’ Lameness in Horses, fifth ed. Lippincott Williams and Wilkins, Philadelphia, pp. 47–54. Stashak, T.S., 2002b. Equine diagnostic imaging. In: Adams’ Lameness in Horses, fifth ed. Lippincott Williams and Wilkins, Philadelphia, pp. 318–322. Swanstrom, M.D., Stover, S.M., Hubbard, M., Hawkins, D.A., 2004. Determination of passive mechanical properties of the superficial and deep digital flexor muscle– ligament–tendon complexes in the forelimbs of horses. American Journal of Veterinary Research 65, 188–197. Van den Belt, A.J.M., 1995. Ultrasonography of Equine Flexor Tendons and Ligaments. Thesis University Utrecht, Faculty of Veterinary Medicine, pp. 9–70. Zarucco, L., Taylor, K.T., Stover, S.M., 2004. Determination of muscle architecture and fiber characteristics of the superficial and deep flexor muscles in the forelimbs of adult horses. American Journal of Veterinary Research 65, 819–828.
Contents lists available at ScienceDirect
The Veterinary Journal journal homepage: www.elsevier.com/locate/tvjl
Morphometric data on the accessory ligament of the deep digital flexor tendon in the equine hindlimb q Sofie Muylle a,*, Katrien Vanderperren b, Jimmy Saunders b, Paul Simoens a a b
Department of Morphology, Faculty of Veterinary Medicine, Ghent University, Salisburylaan 133, B-9820 Merelbeke, Belgium Department of Medical Imaging of Domestic Animals and Small Animal Orthopaedics, Ghent University, Salisburylaan 133, B-9820 Merelbeke, Belgium
a r t i c l e
i n f o
Article history: Accepted 29 May 2009
Keywords: Accessory ligament Deep digital flexor tendon Hindlimb Morphology Horse
a b s t r a c t Desmopathy of the accessory ligament of the deep digital flexor tendon (ALDDFT) in the hindlimb has recently been described as a cause of lameness in horses. However, there is limited morphometric data on this ligament. In the present study, the ALDDFT was carefully dissected in 165 hindlimbs that were collected from an abattoir. Length, width (lateral-to-medial) and thickness (plantar-to-dorsal) of the ligament were measured. It was found that the ALDDFT may be absent in a minority of horses, but when it was present the general morphology was variable. The ALDDFT can be a single rectilinear structure ranging from slender or poorly developed to quite large and can be divided, in part or in its entirety, into two or three bundles. Ó 2009 Elsevier Ltd. All rights reserved.
Introduction The accessory ligament of the deep digital flexor tendon (ALDDFT) in the horse is a reinforcing ligament that originates from the plantar (palmar) fibrous joint capsule of the tarsus (carpus), courses distally between the suspensory ligament (SL) and the deep digital flexor tendon (DDFT) and inserts on the dorsal surface of the DDFT in the mid-metatarsal (metacarpal) region. In the pelvic limb, the ALDDFT is poorly developed (Dyce et al., 1996), but in the forelimb it is of major importance as a part of the passive stay apparatus which enables the animal to maintain a standing posture with relatively little muscular exertion (Shively, 1983). During exercise, the ALDDFT of the forelimb shares tensile load with the DDFT and prevents overstretching of the latter by passively carrying the load during maximal extension of the distal interphalangeal and metacarpophalangeal joints, as seen in the second half of the support phase or when landing after a jump (Riemersma and De Bruyn, 1986; Swanstrom et al., 2004). Disorders of the ALDDFT in the front limb are a common cause of lameness in horses. Both the normal and the pathological ultrasonographic features of the ALDDFT have been extensively described (Pharr and Nyland, 1984; Genovese et al., 1986; Hauser, 1986; Dyson, 1991, 1992; McDiarmid, 1994; Reef, 1998a,b; Stashak, 2002a,b). In contrast, in the hindlimb desmopathy of the
q Parts of information in the text were presented at the European Veterinary Conference Voorjaarsdagen, Amsterdam, Netherlands, 2008 and at the European Veterinary Diagnostic Imaging Congress, Norway, 2008. * Corresponding author. Tel.: +32 9 264 77 11. E-mail address: sofi[email protected] (S. Muylle).
1090-0233/$ - see front matter Ó 2009 Elsevier Ltd. All rights reserved. doi:10.1016/j.tvjl.2009.05.026
ALDDFT is a less usual cause of lameness and data on its function, clinical importance and/or pathological changes were limited (Boswell and Schramme, 2000) until the recent descriptions by Eliashar et al. (2005) and Jorgensen et al. (2007). Descriptive and morphometric data on the normal anatomy of the tarsal ALDDFT are imprecise. Most anatomical textbooks simply indicate that the ALDDFT of the hindlimb is longer and more slender than its thoracic counterpart and that it maybe absent in some horses and in donkeys (Barone, 2000). However, specific information on length, width, thickness and macroscopic appearance of the ALDDFT in the pelvic limb is lacking. This study presents a macroscopic study of the size and development of the ALDDFT in the equine hindlimb. These data can be used to identify and recognise anatomical variations and pathological changes of this structure in clinical patients. Materials and methods One hundred and sixty-five isolated equine hindlimbs, amputated at the centrodistal joint, were obtained from an abattoir and were harvested from horses of unknown history of lameness. Limbs normal in appearance at inspection and palpation were selected. If any lesion was observed or if there was any suspicion of tendinous, ligamentous or bony abnormalities the limb was excluded. The breed, age and sex of the horses were not recorded, but all specimens were weighed and orientated (left/right) prior to dissection. Twelve hindlimbs of donkeys were also obtained from routine post mortem examinations at the department of Pathology at the Faculty of Veterinary Medicine, Ghent University. In all 177 specimens the flexor tendons were examined by palpation and subsequent dissection. A skin incision was made at the latero-plantar border of the superficial digital flexor tendon (SDFT), extending from the tarsal region to the fetlock joint. After the SDFT was detached and reflected, both the DDFT and the ALDDFT were carefully exposed and dissected. The proximo-distal length of the ALDDFT was measured from its origin at the plantar tarsometatarsal ligament to its fusion
S. Muylle et al. / The Veterinary Journal 184 (2010) 298–302 with the DDFT. The lateral-to-medial width of the ALDDFT was measured both at its origin at the plantar tarsometatarsal ligament at the base of the fourth metatarsal bone and more distally near the fusion with the DDFT. Measurements were carried out using a flexible measuring tape pressed against the plantar side of the ligament. In 65 specimens the plantar-to-dorsal thickness was measured near the origin of the ALDDFT at the base of the fourth metatarsal bone by means of Vernier callipers with a precision of 0.1 mm. All measurements were carried out by two people who independently evaluated the ALDDFT of every limb. Possible correlations between the weight of the limb and the length of the ALDDFT, its lateral-to-medial width (proximal and distal) and its thickness, and between the length of the ALDDFT, the lateral-to-medial width (proximal and distal) and the thickness were calculated.
Results The mean weight of the disarticulated equine limbs (n = 165) was 3.3 ± 0.86 kg, with a minimum of 1 kg and a maximum of 6.6 kg (median 3.3 kg). In 155 of the hindlimbs, the ALDDFT was clearly developed, whereas in 10 specimens no ALDDFT could be identified despite careful dissection and precise inspection (weight of the limbs without ALDDFT ranged from 1.9 to 6.6 kg, median 3.6 kg). No correlation was found between the weight of the limb and the presence or absence of ALDDFT. The ALDDFT was absent in all 12 donkey limbs. In all 155 limbs with an ALDDFT, the ligament was situated with its axis of symmetry slightly lateral to the axis of the third metatarsal bone. The ALDDFT tapered distally towards the fusion with the DDFT. The total length of the ALDDFT varied from 7.9 to 18.5 cm (median 14.1 cm) with a mean of 14.0 ± 2.1 cm. The total length of the disarticulated limbs was not measured, but the ALDDFT consistently merged with the DDFT in the second quarter of the metatarsal region. Proximally, the mean width of the ALDDFT measured 1.9 ± 1.2 cm (range 0.2–3.2 cm and median 1.8 cm) and distally 1.2 ± 1.0 cm (range 0.2–2.6 cm and median 1.1 cm). The mean plantar-to-dorsal thickness measured in 65 specimens, was 1.3 ± 0.6 mm (range 0.1–3.3 mm and median 1.1 mm).
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No significant correlation (r = 0.06) was found between the weight of the limb and the length of the ALDDFT, nor was there a significant correlation between the weight of the limb and the proximal (r = 0.02) and/or distal width (r = 0) of the ALDDFT. There was no significant correlation between the weight of the limb and the plantar-to-dorsal thickness of the ALDDFT (r = 0.08), between the length of the ALDDFT and its proximal (r = 0.16) and/or distal width (r = 0.10), nor between the length of the ALDDFT and its plantar-to-dorsal thickness (r = 0). In 143 limbs the ALDDFT was a single, rectilinear structure but in 12 specimens it was, in part or in its entirety, divided into two or three ligaments. The branching pattern showed anatomical variations (Fig. 1). In six limbs, the ALDDFT consisted of two entirely separate ligaments (Fig. 1A) situated besides each other (Fig. 2A) or one on top of the other (Fig. 2B). The two parts of the split ALDDFT were not entirely symmetrical, but each had a specific length, width and thickness (Table 1). In two limbs, the ALDDFT started proximally as a single structure, but ramified between its origin and insertion in two separate ligaments of different lengths (Figs. 1B and 3). In one specimen, the ALDDFT was a single structure both at its origin and at its insertion on the DDFT, but was bifurcated in the free mid-zone (Fig. 1C). In another specimen, the ALDDFT was single at its origin, but trifurcated distally (Fig. 1D). In one limb the ALDDFT bifurcated both proximally and distally, but was undivided in the mid-zone (Fig. 1E). In one specimen the most proximal part of the ALDDFT consisted of two separate ligaments which fused to form a single structure distally (Fig. 1F). The 165 limbs were selected at random at an abattoir. They were left/right orientated, but it was not possible to arrange the feet in pairs belonging to the same horse and was therefore not known whether the development, size and branching pattern of the ALDDFT was symmetrical in both hindlimbs of a same individual.
Fig. 1. A–F. Schematic drawings of various ramification patterns of the accessory ligament of the deep digital flexor tendon (ALDDFT). Tibia (a), calcaneal tuber (b), fourth metatarsal bone (c), second metatarsal bone (d) and third metatarsal bone (e). Long lateral collateral ligament (1), long medial collateral ligament (2), long plantar ligament (3) and suspensory ligament (4), ALDDFT (AL).
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Fig. 2A. Medio-plantar view of specimen 123. The accessory ligament of the deep digital flexor tendon (ALDDFT) consists of two entirely separate ligaments (arrowheads) situated beside one another. Superficial digital flexor tendon (SDFT) (1), deep digital flexor tendon (DDFT) (2), tendon of medial digital flexor (3) joining DDFT and suspensory ligament (SL) (4).
Discussion Whereas desmitis of the ALDDFT in the forelimb has been widely reported, injury of the ALDDFT in the hindlimb has been described as a rare or unusual finding (Reef, 1998b; Dyson, 2003). To the authors’ knowledge only a few cases have been described (Dyson, 1991; Boswell and Schramme, 2000; Eliashar et al., 2005; Jorgensen et al., 2007; Lamas et al., 2008). Several studies have
Fig. 2B. Latero-plantar view of specimen 113. The accessory ligament of the deep digital flexor tendon (ALDDFT) consists of two entirely separate ligaments of which the shorter and more slender ligament (arrowheads) is situated on the plantar side of the larger ligament (arrows). Superficial digital flexor tendon (SDFT) (1), deep digital flexor tendon (DDFT) (2), tendon of medial digital flexor (3) joining DDFT and suspensory ligament (SL) (4).
reported on the mechanical properties of the ALDDFT in the forelimb and concluded that the ALDDFT plays a primary role in supporting the thoracic limb. Passively, the ALDDFT contributes more to the limb support than do the muscles and it provides support during stance with minimal required muscle contraction (Swanstrom et al., 2004). The ALDDFT in the forelimb receives the second highest load of the palmar soft tissue structures (Jansen
Table 1 Morphometric data of the branched ALDDFT (n = 12). Specimen
Weight (kg)
Left/ right
Length (cm)
Proximal width (cm)
Distal width (cm)
29
3
R
116
3
R
123
3.7
L
152
3.9
R
159
3.8
L
163
2.1
R
27 63 24 68 18
2.9 3.7 2.9 3.8 2.8
L R R L L
11 17.1 12.5 13.5 16 15.5 10.5 11.4 12.7 13.6 9.6 11 16.3 11.2 18.2 14.8 11.2
0.8 1.13 0.9 0.4 0.3 0.2 1.2 1.5 0.9 0.9 0.5 1 1.9 2 2 2.5 1.6
0.3 0.8 0.7 0.2 0.2 0.2 0.9 1.1 0.4 0.5 0.2 0.6 0.7–0.5 0.4–0.3 1.7 0.8–1.2–0.5 0.3
155
2.4
L
15.4 14.2
1.6 0.4–1.2
1 1.2
Thickness (mm)
Branching of the ALDDFT Cleft over its entire length Cleft over its entire length
0.1 0.1 0.6 2 0.7 0.1 0.3 1
Cleft over its entire length Cleft over its entire length Cleft over its entire length Cleft over its entire length Bifurcated in the distal half Bifurcated in the distal half Bifurcated in the mid-part Trifurcated in the distal half Bifurcated proximally and distally, undivided in the midpart
1–0.3
AL cleft proximally
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Fig. 3. Plantar view of specimen 27. ALDDFT ramifying between origin and insertion into two separate, well developed ligaments (arrowheads).
et al., 1993); it prevents hyperextension of the fetlock and facilitates carpal extension when the limb is loaded (Denoix, 1994; Mcllwraith, 2002). The ligament is under greatest loading during extension of the digit, either nearing the end of the stance phase or following landing over a fence (Meershoek et al., 2001). Studies on the mechanics of the ALDDFT in the hindlimb have not been performed. Eliashar et al. (2005) stated that the supporting function of the ALDDFT in the hindlimb is unclear but of minor importance. Back et al. (1995) and Eliashar et al. (2005) suggested that due to the reciprocal action of the tarsus, and compared to the antebrachium during stance, the ALDDFT in the hindlimb is probably under less tension in late stance. In a case report by Jorgensen et al. (2007) it was concluded that considering the slender structure of the ALDDFT in the hindlimb, together with its infrequent incidence of injury, it is probable that the forces imposed on the ligament are significantly lower than in the forelimb. In the thoracic limb, mean length of the ALDDFT (measured from the palmar carpal ligament to the fusion with the DDFT) was 13.7 ± 0.4 cm (Zarucco et al., 2004). Ultrasonographically, the lateral-to-medial width of this structure near its insertion level was 1.33 ± 0.4 cm in Arabian horses and 1.53 ± 0.5 cm in Thoroughbreds (Celimli et al., 2004), and varied from 1.8 ± 0.1 cm (Cuesta et al., 1995) to 1.97 ± 0.04 cm in Andalusian Anglo-Arabians (Reef, 1998b). The ultrasonographic palmar-to-dorsal thickness of the ALDDFT in the thoracic limb has been reported at 2.5 cm distal to the accessory bone and measured 0.83 ± 0.03 cm in Anglo–Arabian–Andalusian crossbred horses (Reef, 1998b). There is little information about the hindlimbs. Sisson and Grossman (1975) and Shively (1983) mention that the ALDDFT of the hind limb is longer, but more slender than its thoracic counterpart. According to Smith and Eliashar (2008), a normal ALDDFT in the hindlimb is usually <1 cm in width and approximately 2 mm in thickness but the authors do not say at what level the measurements were obtained. The results of the present study suggest that there was substantial morphometric variation in the dimensions of the ALDDFT. The length of the pelvic ALDDFT varied from 7.9 to 18.5 cm. Near its origin at the plantar tarsometatarsal ligament, the lateral-to-medial width of the ALDDFT varied from 0.2 to 3.2 cm and the plantar-to-dorsal thickness measured 0.1– 3.3 mm. Near the fusion with the DDFT, the lateral-to-medial width varied from 0.2 to 2.6 mm. The ALDDFT ranged from slender and poorly developed to large (Figs. 4 and 5). An awareness of the existence of variable ALDDFT dimensions may be useful
Fig. 4. Latero-plantar view of a right hindlimb with a slender accessory ligament of the deep digital flexor tendon (ALDDFT) (arrowheads). The lateral plantar neurovascular string is drawn back by tweezers. Superficial digital flexor tendon (SDFT) (1), deep digital flexor tendon (DDFT) (2) and suspensory ligament (SL) (4).
during an ultrasonographic examination of the metatarsal region in the horse, but the measurements of the present study do not provide accurate or definitive morphometric criteria as there was no information available about the age, breed or size of the horses. Unfortunately, there was no clinical history for these animals, and it was also not known whether some of the limbs may or may not have been paired. In the thoracic limb, the development of the ALDDFT is believed to be breed-dependent, with much better development in heavy draught horses compared to saddle animals (Nickel et al., 1986). According to van den Belt (1995), differences in ALDDFT dimensions in the forelimb are related to breed, age, bodyweight (BW) and height at the withers. Celimli et al. (2004) reported that breed-related body conformation and training appeared to have a greater influence on ligament and tendon dimensions than age, BW and height. In the present study breed, age, BW and trainingstatus of the horses were unknown. There was no significant correlation, however, between the weight of the disarticulated hindlimbs and the dimensions of the ALDDFT. The ALDDFT was absent in 6% of the examined hindlimbs, but no correlation could be found between the weight of the limb and the presence or absence of an ALDDFT. The ALDDFT was missing in some lighter weight hindlimbs (1.9 kg, 2.3 kg and 2.5 kg), but also in two of the heaviest specimens (6.2 kg and 6.6 kg). The results confirmed the assumption of Barone (2000) and Reef (1998b) that the ALDDFT of the hindlimb may be absent in some horses, but contradicted the statement of Smith and Eliashar (2008) who suggested that the ALDDFT in the hindlimb is present in every horse. The current study also confirmed the findings reported by Barone (2000), in a more limited study (n = 12) that the ALDDFT was absent in donkeys.
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Fig. 5. Latero-plantar view of a left hindlimb with a well developed ALDDFT (arrowheads). The lateral plantar neurovascular string is drawn back by forceps. Superficial digital flexor tendon (SDFT) (1), deep digital flexor tendon (DDFT) (2), tendon of medial digital flexor (3) joining DDFT and suspensory ligament (SL) (4).
Conclusions The results of this limited study have demonstrated that the morphology of the ALDDFT in the hindlimb is variable. Irrespective of the limb’s weight, the ALDDFT may be absent or very slender and poorly developed, but it can also be prominent. The variations in length, width, thickness and general development of the ALDDFT in the hindlimb should be noted during a clinical and, in particular, during ultrasonographic examination of the lame horse. The existence of this variable morphology combined with the lack of literature data describing consequent malfunctions suggests that both the presence and the size of the ALDDFT are of minor importance as far as the supporting function in the hindlimb is concerned. Conflict of interest statement None of the authors of this paper has a financial or personal relationship with other people or organisations that could inappropriately influence or bias the content of this paper. Acknowledgements The authors wish to acknowledge Patrick Vervaet for his dedicated technical assistance. Ward De Spiegelaere is acknowledged for his professional advice. References Back, W., Schamhardt, H.C., Savelberg, H.H., van den Bogert, A.J., Bruin, G., Hartman, W., Barneveld, A., 1995. How the horse moves: 2. Significance of graphical
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