The SL of the forelimb is commonly injured in horses that participate in a variety of disciplines, including racehorses and sport horses.1–5 Suspensory ligament desmitis is often associated with decreased performance and can be a career-ending injury.1–5 Lesions of the SL can develop at its proximal, midbody, or distal region,6 and the prognosis and rate of recurrence following an SL injury vary and are dependent on the anatomic region involved.2,6,7 Injuries to the midbody region and distal branches of the SL tend to heal poorly and have a higher rate of recurrence than do injuries to the proximal region of the SL.2,6,7 Unlike horses with lesions of the midbody region or distal branches of the SL, up to 90% of horses with acute lesions of the proximal region of the SL return to their previous level of activity following stall rest.8 Event horses with desmitis of the midbody region of the SL have a high rate of desmitis recurrence despite extended rest, which might be caused by failure of the ligament to heal completely.2 Additionally, although sport horses with lesions of the distal branches of the SL generally have a fair prognosis, the lesion recurrence rate can be high.2,7,8
The reason for regional variations in the healing and reinjury rates of the SL is unclear and may be caused by zones of hypovascularity within the midbody region and distal branches of the SL in a manner analogous to zones of hypovascularity identified within the SDFTs9 and deep digital flexor tendons10 that have been associated with a predisposition to injury and incomplete healing. In human patients, results of multiple studies11–18 suggest that regions of hypovascularity are associated with ruptured tendons and a poor healing response in those regions following injury to the tendons of the rotator cuff,15–17 calcaneus,12,13 biceps brachii,14 and quadriceps femoris18 and in the common extensor origin of the elbow joint.11
The principal and microvascular anatomy of the SDFTs9 and deep digital flexor10 tendons of horses have been described. To our knowledge, a detailed study to describe the microvascular anatomy of the forelimb SL of horses has not been performed. Therefore, the purpose of the study reported here was to use results of contrast-enhanced CT, microvascular injection (ie, Spalteholz tissue-clearing technique19), and routine histologic evaluation to describe the blood supply of the SL of the forelimb of horses. It was hypothesized that zones of hypovascularity would exist in the midbody and distal regions of the SL. The presence of hypovascular zones in these areas could provide a possible mechanistic explanation for the poor healing and high rate of recurrence for injuries to the midbody region and distal branches of the SL.
Materials and Methods
Seventeen cadaveric forelimbs were used for the study. The forelimbs were obtained from 9 adult horses that were euthanized for reasons unrelated to the study and had no history of forelimb lameness or gross pathological lesions in the forelimbs used. The distal aspect of the limbs was harvested at the junction of the middle and distal third of the radius. The horses ranged in age from 4 to 18 years (mean, 8.7 years; median, 9 years) and included 4 mares and 5 geldings. Breeds represented included Arabian and Arabian cross (n = 2), Quarterhorse (2), Paint (2), Standardbred (1), and Thoroughbred (2). The forelimbs were frozen and stored at −20°C until analysis, at which time they were thawed prior to injection of the contrast media or India ink.
Contrast-enhanced CT—To identify the major vessels that supply the SL, the median artery of 2 forelimbs was cannulated just proximal to the carpus and injected with 60 mL of contrast medium.a The limbs were then imaged with a 16-slice CT scannerb at a slice thickness of 0.625 mm. The CT images were processed with computer softwarec to highlight and identify the major vascular supply to the SL. Regions of interest were automatically selected on the basis of the radiopacity (Hounsfield units) of contrast medium20 for vasculature and manually corrected on a slice-by-slice basis to outline the vessels.
Microvascular perfusion by the Spalteholz tissue-clearing technique—To identify the microvascular anatomy of the SL specimens, the median artery of 12 forelimbs was cannulated just proximal to the carpus, and 120 to 180 mL of India inkd was injected under constant manual pressure.19 Complete vascular filling was confirmed by the presence of India ink in the dermal capillaries following a small incision at the coronary band of the hoof. The limbs were then frozen at −20°C for a minimum of 48 hours. Five-millimeter-thick sections of the limb were then cut in either the sagittal (n = 7) or transverse (5) plane from the middle carpal joint to the metacarpophalangeal joint with a band saw and fixed in neutral-buffered 10% formalin. Tissue clearing was performed by means of the modified Spalteholz technique as described.19
Histologic evaluation—Three additional forelimbs were processed for routine histologic evaluation. Briefly, 5-mm-thick sections were cut in the transverse axial plane and fixed in neutral-buffered 10% formalin. Selected sections that represented the proximal, midbody, and distal regions of the SL from each limb were further sectioned into 5-μm-thick sections, stained with H&E stain, and evaluated histologically. The histologic vascular anatomy was descriptively compared with the microvascular anatomy determined by the Spalteholz technique.
Results
Contrast-enhanced CT—The principal blood supply to the SL consisted of small branches of the medial and lateral palmar and palmar metacarpal arteries beginning at its most proximal aspect and continuing throughout its length (Figure 1). Branches of these vessels entered the proximal region of the SL at the deep palmar arch. A branch of the medial palmar metacarpal artery entered the midbody region of the SL opposite of where the nutrient artery entered the nutrient foramen of the third metacarpal bone. The distal region and branches of the SL were supplied by branches of the lateral and medial palmar digital vessels and the associated superficial palmar arch as well as branches of the lateral and medial palmar metacarpal vessels and the associated deep palmar arch.
Three-dimensional CT reconstruction of the caudal aspect of the forelimb SL (blue) of a horse with (A) and without (B) the associated bones included and the cranial aspect of the forelimb SL of a horse without the associated bones included (C). The major blood vessels supplying the SL appear in red. DDPA = Distal deep palmar arch. LDV = Lateral digital vessels. LPMV = Lateral palmar metacarpal vessels. LPV = Lateral palmar vessels. MDV = Medial digital vessels. MPMV = Medial palmar metacarpal vessels. MPV = Medial palmar vessels. PDPA = Proximal deep palmar arch.
Citation: American Journal of Veterinary Research 74, 12; 10.2460/ajvr.74.12.1481
Three-dimensional CT reconstruction of the caudal aspect of the forelimb SL (blue) of a horse with (A) and without (B) the associated bones included and the cranial aspect of the forelimb SL of a horse without the associated bones included (C). The major blood vessels supplying the SL appear in red. DDPA = Distal deep palmar arch. LDV = Lateral digital vessels. LPMV = Lateral palmar metacarpal vessels. LPV = Lateral palmar vessels. MDV = Medial digital vessels. MPMV = Medial palmar metacarpal vessels. MPV = Medial palmar vessels. PDPA = Proximal deep palmar arch.
Citation: American Journal of Veterinary Research 74, 12; 10.2460/ajvr.74.12.1481
Three-dimensional CT reconstruction of the caudal aspect of the forelimb SL (blue) of a horse with (A) and without (B) the associated bones included and the cranial aspect of the forelimb SL of a horse without the associated bones included (C). The major blood vessels supplying the SL appear in red. DDPA = Distal deep palmar arch. LDV = Lateral digital vessels. LPMV = Lateral palmar metacarpal vessels. LPV = Lateral palmar vessels. MDV = Medial digital vessels. MPMV = Medial palmar metacarpal vessels. MPV = Medial palmar vessels. PDPA = Proximal deep palmar arch.
Citation: American Journal of Veterinary Research 74, 12; 10.2460/ajvr.74.12.1481
Microvascular perfusion by the Spalteholz tissue-clearing technique—The entire length of the SL had a substantive microvascular supply without distinct variation in the intraligamentous vascular density among the proximal, midbody, and distal regions. The uniformly abundant intraligamentous vasculature was consistently visible on all sagittal (Figure 2) and transverse sections (Figure 3) from all 12 limbs evaluated with the Spalteholz technique with minimal variability among specimens. Similarly, an abundant, periligamentous vascular plexus was observed on sagittal and transverse sections that surrounded the SL throughout its length, and those vessels were generally oriented longitudinally, parallel with the long axis of the bone.
Representative photograph of the substantive microvascular anatomy (black lines) of a midsagittal section of a forelimb of a horse following application of the Spalteholz tissue-clearing technique. The proximal (A), midbody (B), and distal (C) regions of the SL are indicated (arrows).
Citation: American Journal of Veterinary Research 74, 12; 10.2460/ajvr.74.12.1481
Representative photograph of the substantive microvascular anatomy (black lines) of a midsagittal section of a forelimb of a horse following application of the Spalteholz tissue-clearing technique. The proximal (A), midbody (B), and distal (C) regions of the SL are indicated (arrows).
Citation: American Journal of Veterinary Research 74, 12; 10.2460/ajvr.74.12.1481
Representative photograph of the substantive microvascular anatomy (black lines) of a midsagittal section of a forelimb of a horse following application of the Spalteholz tissue-clearing technique. The proximal (A), midbody (B), and distal (C) regions of the SL are indicated (arrows).
Citation: American Journal of Veterinary Research 74, 12; 10.2460/ajvr.74.12.1481
Small vascular branches that originated from the palmar metacarpal vessels were observed invaginating into the dorsal aspect of the medial and lateral lobes of the SL beginning at its proximal aspect (Figure 3). The proximal segment of the SL where the periligamentous vessels were most prominent corresponded with the location of the proximal deep palmar arch.21–23 In this area, the palmar aspect of the SL had additional small vessels, which communicated with the proximal deep palmar arch and the medial and lateral palmar vessels.
Representative photographs of transverse sections of a forelimb of a horse at the proximal (A), midbody (B), and distal (C) regions of the SL following application of the Spalteholz tissue-clearing technique. A—Section obtained at the level of the proximal deep palmar arch; abundant periligamentous vasculature (arrows) and grossly visible vessels entering the SL from immediately adjacent to the third metacarpal bone (arrowhead) are present. B—Section obtained at the level of the nutrient artery of the third metacarpal bone (white arrowhead); a vessel entering the SL (open arrowhead) opposite from the nutrient artery as well as the continued presence of the periligamentous plexus (arrows) can be seen. C—Section obtained at the level of the medial and lateral branches of the SL; an abundant periligamentous (arrows) and an intraligamentous vascular supply are present. AL = Accessory ligament of the deep digital flexor tendon. DDFT = Deep digital flexor tendon. LBSL = Lateral branch of the SL. MBSL = Medial branch of the SL. MCIII = Third metacarpal bone. MPA = Medial palmar artery. MPMA = Medial palmar metacarpal artery. MPV = Medial palmar vein. PDA = Palmar digital artery. PMA = Palmar metacarpal artery.
Citation: American Journal of Veterinary Research 74, 12; 10.2460/ajvr.74.12.1481
Representative photographs of transverse sections of a forelimb of a horse at the proximal (A), midbody (B), and distal (C) regions of the SL following application of the Spalteholz tissue-clearing technique. A—Section obtained at the level of the proximal deep palmar arch; abundant periligamentous vasculature (arrows) and grossly visible vessels entering the SL from immediately adjacent to the third metacarpal bone (arrowhead) are present. B—Section obtained at the level of the nutrient artery of the third metacarpal bone (white arrowhead); a vessel entering the SL (open arrowhead) opposite from the nutrient artery as well as the continued presence of the periligamentous plexus (arrows) can be seen. C—Section obtained at the level of the medial and lateral branches of the SL; an abundant periligamentous (arrows) and an intraligamentous vascular supply are present. AL = Accessory ligament of the deep digital flexor tendon. DDFT = Deep digital flexor tendon. LBSL = Lateral branch of the SL. MBSL = Medial branch of the SL. MCIII = Third metacarpal bone. MPA = Medial palmar artery. MPMA = Medial palmar metacarpal artery. MPV = Medial palmar vein. PDA = Palmar digital artery. PMA = Palmar metacarpal artery.
Citation: American Journal of Veterinary Research 74, 12; 10.2460/ajvr.74.12.1481
Representative photographs of transverse sections of a forelimb of a horse at the proximal (A), midbody (B), and distal (C) regions of the SL following application of the Spalteholz tissue-clearing technique. A—Section obtained at the level of the proximal deep palmar arch; abundant periligamentous vasculature (arrows) and grossly visible vessels entering the SL from immediately adjacent to the third metacarpal bone (arrowhead) are present. B—Section obtained at the level of the nutrient artery of the third metacarpal bone (white arrowhead); a vessel entering the SL (open arrowhead) opposite from the nutrient artery as well as the continued presence of the periligamentous plexus (arrows) can be seen. C—Section obtained at the level of the medial and lateral branches of the SL; an abundant periligamentous (arrows) and an intraligamentous vascular supply are present. AL = Accessory ligament of the deep digital flexor tendon. DDFT = Deep digital flexor tendon. LBSL = Lateral branch of the SL. MBSL = Medial branch of the SL. MCIII = Third metacarpal bone. MPA = Medial palmar artery. MPMA = Medial palmar metacarpal artery. MPV = Medial palmar vein. PDA = Palmar digital artery. PMA = Palmar metacarpal artery.
Citation: American Journal of Veterinary Research 74, 12; 10.2460/ajvr.74.12.1481
At the junction of the proximal and midbody regions of the SL, the periligamentous vascular plexus remained visible, with small branches that extended into the SL, particularly on its dorsal aspect (Figures 2 and 3). Near the nutrient foramen of the medullary cavity of the third metacarpal bone, a branch of the medial palmar metacarpal artery extended in a palmar direction with accessory branches that extended into the midbody region of the SL. The periligamentous vascular plexus remained present at the distal region of the SL where it divided into medial and lateral branches. At this level, palmar metacarpal vessels were observed with multiple small branches that supplied the medial and lateral branches of the SL (Figure 3). Small branches from the palmar digital vessels also contributed to the vascularity of the medial and lateral branches of the SL. Additionally, an abundant intraligamentous blood supply was observed in the distal region of the SL.
Histologic evaluation—Histologic findings for sections from the proximal, midbody, and distal regions of the SL were consistent with the microvascular anatomy observed in corresponding sections that were evaluated with the Spalteholz technique. Additionally, small arteries and veins were observed within the connective tissue septa in all regions of the SL, which contributed to an abundant intraligamentous blood supply (Figure 4). A periligamentous plexus of connective tissue that contained small arteries and veins surrounded the SL throughout its length. Branches of the medial palmar metacarpal artery, which give rise to the nutrient artery of the third metacarpal bone, also supplied the periligamentous vascular plexus at the midbody region of the SL (Figures 3 and 4). The distal branches of the SL also had an abundant intraligamentous blood supply from the periligamentous vascular plexus.
Photomicrographs of sections of a forelimb of a horse obtained at the proximal (A and B), midbody (C), and distal (D) regions of the SL. A—Multiple connective tissue septa are present within the SL, which contains cross sections of multiple small arteries and veins (arrows). H&E stain; bar = 50 μm. B—Multiple cross sections of small arteries and veins are shown within a connective tissue plexus (CTP) that surrounds the SL. H&E stain; bar = 50 μm. C—The nutrient artery (NA) of the third metacarpal bone (MCIII) is adjacent and contributes vascular branches to the periligamentous vascular plexus of the SL; intraligamentous connective tissue septa with associated small vessels continue to be present. H&E stain; bar = 100 μm. D—The periligamentous vascular plexus that contributes to the CTP which enters the SL and provides an extensive intraligamentous blood supply (arrows), is evident. H&E stain; bar = 100 μm. Sectioning artifacts within the SL are present in all panels. NF = Nutrient foramen of MCIII.
Citation: American Journal of Veterinary Research 74, 12; 10.2460/ajvr.74.12.1481
Photomicrographs of sections of a forelimb of a horse obtained at the proximal (A and B), midbody (C), and distal (D) regions of the SL. A—Multiple connective tissue septa are present within the SL, which contains cross sections of multiple small arteries and veins (arrows). H&E stain; bar = 50 μm. B—Multiple cross sections of small arteries and veins are shown within a connective tissue plexus (CTP) that surrounds the SL. H&E stain; bar = 50 μm. C—The nutrient artery (NA) of the third metacarpal bone (MCIII) is adjacent and contributes vascular branches to the periligamentous vascular plexus of the SL; intraligamentous connective tissue septa with associated small vessels continue to be present. H&E stain; bar = 100 μm. D—The periligamentous vascular plexus that contributes to the CTP which enters the SL and provides an extensive intraligamentous blood supply (arrows), is evident. H&E stain; bar = 100 μm. Sectioning artifacts within the SL are present in all panels. NF = Nutrient foramen of MCIII.
Citation: American Journal of Veterinary Research 74, 12; 10.2460/ajvr.74.12.1481
Photomicrographs of sections of a forelimb of a horse obtained at the proximal (A and B), midbody (C), and distal (D) regions of the SL. A—Multiple connective tissue septa are present within the SL, which contains cross sections of multiple small arteries and veins (arrows). H&E stain; bar = 50 μm. B—Multiple cross sections of small arteries and veins are shown within a connective tissue plexus (CTP) that surrounds the SL. H&E stain; bar = 50 μm. C—The nutrient artery (NA) of the third metacarpal bone (MCIII) is adjacent and contributes vascular branches to the periligamentous vascular plexus of the SL; intraligamentous connective tissue septa with associated small vessels continue to be present. H&E stain; bar = 100 μm. D—The periligamentous vascular plexus that contributes to the CTP which enters the SL and provides an extensive intraligamentous blood supply (arrows), is evident. H&E stain; bar = 100 μm. Sectioning artifacts within the SL are present in all panels. NF = Nutrient foramen of MCIII.
Citation: American Journal of Veterinary Research 74, 12; 10.2460/ajvr.74.12.1481
Discussion
Results of the present study indicated that the SL of the equine forelimb has an abundant microvascular supply, which did not vary substantially among its proximal, midbody, and distal regions. The abundant intraligamentous microvasculature originated from a periligamentous vascular plexus that surrounded the entire length of SL including its distal branches. The vascular supply to this periligamentous plexus originated from branches of the medial and lateral palmer metacarpal arteries as well as branches of the medial and lateral palmar arteries. These findings were consistent with those of other investigators, which suggested that branches of the medial and lateral palmar metacarpal arteries24 and branches of the medial palmar artery22 constituted the major vascular supply to the SL. These small branches penetrate the SL and anastomose with a longitudinally oriented network of intraligamentous vessels that pass between the fascicular bundles of collagen fibers. Although the techniques used to identify the microvascular anatomy of the SL in the present study only reflected the structural components of the vascular supply and not the physiologic parameters of blood flow and perfusion, results of other studies25–27 indicate an excellent correlation between the microvascular anatomy of connective tissue structures and their vascular response to acute injury. The findings of the present study confirmed previous observations22,24 regarding the principal vascular supply of the SL and provided the first detailed description of the microvascular anatomy in each region of the SL.
The intraligamentous microvascular pattern observed for the SL in this study is analogous to the intratendinous microvascular supply for the SDFT of horses, which was described as an extensive, interlacing network of longitudinally oriented, intratendinous microvessels.9 However, contrary to the findings of the present study, the site of the SDFT that is most commonly injured in horses corresponded to a zone of relative avascularity,9 and the investigators9 concluded that this hypovascular zone predisposed the tendon to degenerative injury and contributed to the poor healing response in that area. In human patients, similar hypovascular regions have been identified at common injury sites for various tendons.11–18
Although the results of the present study did not identify any hypovascular areas in the SL, damage to the periligamentous vascular supply of the SL secondary to traumatic or degenerative injury could contribute to a compromised healing response and increase the risk for reinjury. This hypothesis is supported by findings of other studies, which indicate that disruption of the periligamentous vasculature of the cranial cruciate ligament of dogs results in an immediate decrease in intraligamentous blood flow28 and impairment of the early (2.5 weeks) intraligamentous vascular response to injury.25 However, the periligamentous vascular plexus was reestablished, and the intraligamentous microvascular response for dogs with cranial cruciate ligament injury was similar to that of control dogs (no disruption of the periligamentous vascular supply) by 8 weeks after injuy.25 In horses, vascular contrast CT studies following acute injury of the SL may provide insight into the integrity of its periligamentous vascular supply and help elucidate the potential role of vascular disruption in chronic SL injuries.
Although an area of diminished vascular supply has been implicated in the predisposition of the SDFT to injury,9 biomechanical factors can also affect the biology of connective tissue healing. A compromised microvascular response secondary to excessive loading has been implicated in the failure to heal of some degenerative tendon lesions in horses.29 Repetitive stresses on healing tendons can disrupt the microvascular healing response, resulting in the formation of poorly vascularized scar tissue, which fails to adapt and remodel into functional repair tissue.29 This disruption of the microvascular healing response in tendons is similar to the mechanism of delayed healing or nonunion of fractured bones, in which excessive, repetitive stresses at the fracture site continually disrupt capillary migration into the repair tissue, resulting in the development of a fibrous or fibrocartilagenous repair tissue instead of bone.27 Fatigue of the flexor tendons that support the metacarpophalangeal or metatarsophalangeal (fetlock) joint during high-speed exercise leads to increased stresses on the SL apparatus, which in turn result in acute or degenerative lesions of the SL.2 Continued mechanical loading of the fatigued or injured tendons could result in a dysfunctional repair response and the production of poorly vascularized scar tissue, which could predispose the SL to reinjury.2
Results of the present study do not support an anatomic microvascular supply basis for the regional variations in the healing response of the SL to injury in horses, and the precise relationship between the microvasculature of the SL and the regional variation in its healing response remains to be elucidated. The regional variation in the healing and reinjury rates reported for the SL of horses might be related to topographic heterogeneity in its structural, compositional, and functional characteristics.30 Additional studies to examine the sequence of biological events following injury to specific areas of the SL are necessary to identify the precise factors responsible for regional variations in outcome.
ABBREVIATIONS
| SDFT | Superficial digital flexor tendon SL Suspensory ligament |
| SL | Suspensory ligament |
75% Iopamidol, Bracco Diagnostics, Princeton, NJ.
GE Brightspeed, GE Healthcare, Waukesha, Wis.
Mimics, Materialise, Leuven, Belgium.
Black Magic, Higgins, Bellwood, Ill.
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