Equine Veterinary Journal ISSN 0425-1644 DOI: 10.1111/evj.12330
The cross-sectional area changes in digital flexor tendons and suspensory ligament in foals by ultrasonographic examination K. KOROSUE*, Y. ENDO, H. MURASE, M. ISHIMARU, Y. NAMBO and F. SATO Hidaka Training and Research Center, Japan Racing Association, Urakawa-gun, Hokkaido, Japan. *Correspondence email: [email protected]; Received: 09.12.13; Accepted: 07.08.14
Summary Reasons for performing study: Flexural deformities are common conditions of growing horses and are suggested to have a relationship with the contraction of musculotendinous units. However, limited studies have documented the changes in each tendon and ligament in the metacarpal region with age. Objectives: To investigate the changes in the cross-sectional area (CSA) of each tendon and ligament in the metacarpal region with age by ultrasonographic examination. Study design: Longitudinal study of foals from Day 1 to age 24 months. Methods: The CSA of the superficial digital flexor tendon, deep digital flexor tendon, accessory ligament of the deep digital flexor tendon and suspensory ligament was measured by ultrasonographic examination at monthly intervals from Day 1 to age 24 months in 7 Thoroughbred foals. Results: Changes in superficial digital flexor CSA in all regions were larger than those of other structures from 10 months to 15 months. The suspensory ligament CSA was significantly larger than those of other structures on Day 1 in both the region of suspensory origin (RSO) and region of suspensory body (RSBO). This condition continued until 2 months in the RSO and until 5 months in the RSBO. The changes in deep digital flexor CSA were larger than those of other structures from 2 to 5 months in both the RSO and RSBO. Conclusions: The rate of change in each structure varies with age. Thus, the functional adaptation with age that takes place may differ among structures because the primary function of each structure differs. Keywords: horse; foal; distal limb; conformation change; radiographic evaluation
Introduction The horse is genetically programmed for rapid early skeletal development. The musculoskeletal structure of a newborn foal is able to adapt for maximising locomotor efficiency to avoid potential predators within hours of birth. This is made possible by diminishing limb weight with reduced distal muscle mass and number of bones. The second and fourth metacarpal/metatarsal bones are greatly reduced in size and transfer the load across the carpo-metacarpal and tarso-metatarsal joints to the third metacarpal (McIII)/third metatarsal bone (MtIII) through interosseous ligaments. There is only one digit (the third), consisting of proximal, middle and distal phalangeal bones [1]. Therefore, extension of the metacarpo-phalangeal joint during the weightbearing and stance phases of the stride is resisted by the superficial digital flexor tendon (SDFT), the deep digital flexor tendon (DDFT) and the suspensory ligament (SL). Thus, the tendons and ligaments of the distal limb play an important role in the musculoskeletal system during standing and locomotion. In particular, the SL is a critical component of the much larger suspensory apparatus that prevents excessive extension of the fetlock when the limb is loaded. Mild digital hyperextension is common in newborn foals. It is caused by flaccidity of the flexor muscles and usually corrects itself within a few weeks due to negative allometric growth of the tendons relative to the bones and increased muscle tone. Therefore, it may be considered to be a physiological variant rather than disease-related [2,3]. In contrast, flexural deformities tend to occur in fast-growing horses or in those following a growth spurt. Flexural deformities are common conditions of growing horses in which a joint is held in an abnormally flexed position. They affect soft tissue structures and occur in the sagittal plane, as opposed to angular limb deformities, which primarily affect osseous structures and occur in the frontal plane [4]. It is suggested that there are differences in the timing of the appearance of acquired flexural deformities between the distal interphalangeal joint (DIPJ), which usually occurs between ages 6 weeks and 6 months [5], and the metacarpophalangeal joint (MCPJ), which usually occurs between the ages of 10 and 18 months [5,6]. In addition, it is suggested that the flexural deformities have a relationship with contraction of the musculotendinous units [5]. Furthermore there is a report that, although the SDFT has reached maturity by the age of 2 years,
548
the DDFT remains immature at the age of 2 years and continues to grow [7]. In other words, there may be a difference in the rate of change and in tendon strength with age between the SDFT and DDFT. Meanwhile, tendon strength may be related to the cross-sectional area (CSA) of a tendon [8]. Therefore, the presumptive strength and the stiffness of each tendon can be measured by the changes in CSA of each structure with age. Only a few studies have documented the change in the SDFT CSA with age during development [8,9]. However, these studies have only described the influence of exercise on the change in the SDFT CSA in foals. Moreover, there have been no studies documenting the change in the DDFT and SL CSA with age during development. In this study, we investigated the changes in the SDFT, DDFT, accessory ligament of the DDFT (ALDDFT) and SL CSA with age by ultrasonographic examination.
Materials and methods Animals Seven Thoroughbred foals (4 colts and 3 fillies), born within 2 months from late February to late April 2010, were employed for this study at the Hidaka Training and Research Center in Hokkaido, Japan. The foals were born healthy without any conformational malformations, and none of them developed any throughout the research period. The foals were kept at pasture, approximately 40,000 m2, for approximately 20 h/day, until November. The foals were turned out to the same pasture covered by snow for around 7 h/day and stabled individually overnight from December to April. The foals were weaned at 155.1 ± 15.5 days of age (mean ± s.d.). The foals and their dams were given supplementary grass hay and a balanced ration concentrate to maintain the dam’s body condition score [10] of 5.5–6.5 until weaning and the foal’s body condition score of 5.0–6.0 after weaning. Training for potential racing was begun at age 18–19 months and continued beyond the end of the study at 24 months. Ultrasonographic examination was performed on the day after birth (Day 1), at age one week, then at monthly intervals to age 12 months, and thereafter at 3 month intervals to age 24 months. Equine Veterinary Journal 47 (2015) 548–552 © 2015 EVJ Ltd
K. Korosue et al.
Cross-sectional area changes in distal limb tendon and ligament in foals
TABLE 1: Changes in superficial flexor tendon (SDFT), deep digital flexor tendon (DDFT), accessory ligament of the deep digital flexor tendon (ALDDFT) and suspensory ligament (SL) cross-sectional area (CSA) at each region measured by ultrasonography RSO
1D 1W 1M 2M 3M 4M 5M 6M 7M 8M 9M 10M 11M 12M 15M 18M 21M 24M
RSBO
SDFT
DDFT
ALDDF
SL
0.34 ± 0.06 0.35 ± 0.07 0.41 ± 0.07 0.48 ± 0.05 0.57 ± 0.09 0.66 ± 0.10 0.75 ± 0.10 0.81 ± 0.11 0.91 ± 0.12 0.97 ± 0.14†† 1.01 ± 0.14†† 1.02 ± 0.11†† 1.07 ± 0.10†† 1.13 ± 0.13†† 1.64 ± 0.25†† 1.53 ± 0.33†† 1.28 ± 0.21†† 1.28 ± 0.30††
0.41 ± 0.09 0.38 ± 0.08 0.46 ± 0.07* 0.51 ± 0.06 0.65 ± 0.08** 0.75 ± 0.08** 0.85 ± 0.10** 0.92 ± 0.09†* 0.93 ± 0.08 0.88 ± 0.09 0.83 ± 0.05 0.83 ± 0.06 0.86 ± 0.08 0.94 ± 0.09 1.07 ± 0.08 1.01 ± 0.10 0.82 ± 0.10 0.85 ± 0.07
0.32 ± 0.09 0.32 ± 0.07 0.39 ± 0.05** 0.47 ± 0.06** 0.54 ± 0.08 0.59 ± 0.10 0.66 ± 0.06** 0.69 ± 0.09 0.68 ± 0.09 0.61 ± 0.06 0.63 ± 0.08 0.57 ± 0.04 0.63 ± 0.05 0.69 ± 0.07 0.94 ± 0.10 0.92 ± 0.10 0.78 ± 0.07 0.84 ± 0.08
0.44 ± 0.07 0.53 ± 0.19†† 0.54 ± 0.09††* 0.64 ± 0.10††** 0.70 ± 0.09* 0.74 ± 0.08 0.80 ± 0.08 0.79 ± 0.14 0.76 ± 0.10 0.71 ± 0.09 0.69 ± 0.06 0.63 ± 0.04 0.68 ± 0.05 0.66 ± 0.05 1.01 ± 0.14 1.05 ± 0.10 0.98 ± 0.07 0.89 ± 0.05 †
RSBI
SDFT
DDFT
ALDDF
SL
0.30 ± 0.05 0.32 ± 0.05 0.37 ± 0.05 0.44 ± 0.05 0.55 ± 0.10** 0.67 ± 0.08* 0.74 ± 0.11 0.84 ± 0.13* 0.91 ± 0.12 0.92 ± 0.13 0.91 ± 0.15 0.86 ± 0.10 0.91 ± 0.08†† 0.96 ± 0.09†† 1.46 ± 0.15†† 1.43 ± 0.27†† 1.15 ± 0.18†† 1.07 ± 0.20††
0.26 ± 0.05 0.26 ± 0.06 0.31 ± 0.06 0.36 ± 0.06** 0.42 ± 0.06 0.49 ± 0.06 0.53 ± 0.05 0.54 ± 0.10 0.57 ± 0.09 0.58 ± 0.07 0.59 ± 0.05 0.57 ± 0.07 0.61 ± 0.05 0.65 ± 0.05 0.85 ± 0.14 0.77 ± 0.10 0.65 ± 0.09 0.67 ± 0.07
0.24 ± 0.06 0.23 ± 0.05 0.25 ± 0.03 0.32 ± 0.06** 0.42 ± 0.10 0.48 ± 0.05* 0.57 ± 0.08* 0.59 ± 0.09 0.59 ± 0.06 0.59 ± 0.09 0.61 ± 0.09 0.60 ± 0.06 0.66 ± 0.08 0.67 ± 0.10 0.87 ± 0.11 0.80 ± 0.06 0.67 ± 0.10 0.68 ± 0.05
0.38 ± 0.04 0.44 ± 0.08†† 0.51 ± 0.09††** 0.61 ± 0.08††* 0.66 ± 0.09†† 0.77 ± 0.08††** 0.84 ± 0.09†† 0.87 ± 0.10 0.87 ± 0.09 0.86 ± 0.09 0.85 ± 0.12 0.79 ± 0.10 0.84 ± 0.11 0.79 ± 0.09 1.05 ± 0.10 1.10 ± 0.12 1.00 ± 0.10 0.93 ± 0.08 ††
SDFT
DDFT
SL
0.28 ± 0.04 0.30 ± 0.05 0.38 ± 0.04 0.45 ± 0.06 0.57 ± 0.10* 0.68 ± 0.09* 0.77 ± 0.10 0.86 ± 0.13 0.91 ± 0.16 0.91 ± 0.15 0.86 ± 0.12 0.83 ± 0.08 0.88 ± 0.12 0.91 ± 0.09 1.44 ± 0.18 1.37 ± 0.25 1.06 ± 0.15 1.02 ± 0.14
0.33 ± 0.04 0.40 ± 0.05 0.54 ± 0.07†** 0.67 ± 0.07††** 0.84 ± 0.12††** 1.01 ± 0.08††** 1.06 ± 0.09†† 1.10 ± 0.08†† 1.17 ± 0.07†† 1.17 ± 0.10†† 1.14 ± 0.08†† 1.15 ± 0.06†† 1.25 ± 0.07†† 1.24 ± 0.09†† 1.54 ± 0.15 1.44 ± 0.09 1.25 ± 0.10†† 1.28 ± 0.06††
0.34 ± 0.04 0.40 ± 0.07 0.48 ± 0.05** 0.54 ± 0.08 0.64 ± 0.10** 0.78 ± 0.09** 0.84 ± 0.09 0.87 ± 0.11 0.87 ± 0.12 0.86 ± 0.11 0.87 ± 0.08 0.84 ± 0.06 0.82 ± 0.08 0.76 ± 0.04 1.07 ± 0.12 1.12 ± 0.12 0.94 ± 0.07 0.91 ± 0.04
RSO: region of suspensory origin; RSBO: region of the suspensory body; RSBI: region of suspensory bifurcation. *Within a group, value indicates that CSA is significantly larger than in the previous month (*P
The cross-sectional area changes in digital flexor tendons and suspensory ligament in foals by ultrasonographic examination K. KOROSUE*, Y. ENDO, H. MURASE, M. ISHIMARU, Y. NAMBO and F. SATO Hidaka Training and Research Center, Japan Racing Association, Urakawa-gun, Hokkaido, Japan. *Correspondence email: [email protected]; Received: 09.12.13; Accepted: 07.08.14
Summary Reasons for performing study: Flexural deformities are common conditions of growing horses and are suggested to have a relationship with the contraction of musculotendinous units. However, limited studies have documented the changes in each tendon and ligament in the metacarpal region with age. Objectives: To investigate the changes in the cross-sectional area (CSA) of each tendon and ligament in the metacarpal region with age by ultrasonographic examination. Study design: Longitudinal study of foals from Day 1 to age 24 months. Methods: The CSA of the superficial digital flexor tendon, deep digital flexor tendon, accessory ligament of the deep digital flexor tendon and suspensory ligament was measured by ultrasonographic examination at monthly intervals from Day 1 to age 24 months in 7 Thoroughbred foals. Results: Changes in superficial digital flexor CSA in all regions were larger than those of other structures from 10 months to 15 months. The suspensory ligament CSA was significantly larger than those of other structures on Day 1 in both the region of suspensory origin (RSO) and region of suspensory body (RSBO). This condition continued until 2 months in the RSO and until 5 months in the RSBO. The changes in deep digital flexor CSA were larger than those of other structures from 2 to 5 months in both the RSO and RSBO. Conclusions: The rate of change in each structure varies with age. Thus, the functional adaptation with age that takes place may differ among structures because the primary function of each structure differs. Keywords: horse; foal; distal limb; conformation change; radiographic evaluation
Introduction The horse is genetically programmed for rapid early skeletal development. The musculoskeletal structure of a newborn foal is able to adapt for maximising locomotor efficiency to avoid potential predators within hours of birth. This is made possible by diminishing limb weight with reduced distal muscle mass and number of bones. The second and fourth metacarpal/metatarsal bones are greatly reduced in size and transfer the load across the carpo-metacarpal and tarso-metatarsal joints to the third metacarpal (McIII)/third metatarsal bone (MtIII) through interosseous ligaments. There is only one digit (the third), consisting of proximal, middle and distal phalangeal bones [1]. Therefore, extension of the metacarpo-phalangeal joint during the weightbearing and stance phases of the stride is resisted by the superficial digital flexor tendon (SDFT), the deep digital flexor tendon (DDFT) and the suspensory ligament (SL). Thus, the tendons and ligaments of the distal limb play an important role in the musculoskeletal system during standing and locomotion. In particular, the SL is a critical component of the much larger suspensory apparatus that prevents excessive extension of the fetlock when the limb is loaded. Mild digital hyperextension is common in newborn foals. It is caused by flaccidity of the flexor muscles and usually corrects itself within a few weeks due to negative allometric growth of the tendons relative to the bones and increased muscle tone. Therefore, it may be considered to be a physiological variant rather than disease-related [2,3]. In contrast, flexural deformities tend to occur in fast-growing horses or in those following a growth spurt. Flexural deformities are common conditions of growing horses in which a joint is held in an abnormally flexed position. They affect soft tissue structures and occur in the sagittal plane, as opposed to angular limb deformities, which primarily affect osseous structures and occur in the frontal plane [4]. It is suggested that there are differences in the timing of the appearance of acquired flexural deformities between the distal interphalangeal joint (DIPJ), which usually occurs between ages 6 weeks and 6 months [5], and the metacarpophalangeal joint (MCPJ), which usually occurs between the ages of 10 and 18 months [5,6]. In addition, it is suggested that the flexural deformities have a relationship with contraction of the musculotendinous units [5]. Furthermore there is a report that, although the SDFT has reached maturity by the age of 2 years,
548
the DDFT remains immature at the age of 2 years and continues to grow [7]. In other words, there may be a difference in the rate of change and in tendon strength with age between the SDFT and DDFT. Meanwhile, tendon strength may be related to the cross-sectional area (CSA) of a tendon [8]. Therefore, the presumptive strength and the stiffness of each tendon can be measured by the changes in CSA of each structure with age. Only a few studies have documented the change in the SDFT CSA with age during development [8,9]. However, these studies have only described the influence of exercise on the change in the SDFT CSA in foals. Moreover, there have been no studies documenting the change in the DDFT and SL CSA with age during development. In this study, we investigated the changes in the SDFT, DDFT, accessory ligament of the DDFT (ALDDFT) and SL CSA with age by ultrasonographic examination.
Materials and methods Animals Seven Thoroughbred foals (4 colts and 3 fillies), born within 2 months from late February to late April 2010, were employed for this study at the Hidaka Training and Research Center in Hokkaido, Japan. The foals were born healthy without any conformational malformations, and none of them developed any throughout the research period. The foals were kept at pasture, approximately 40,000 m2, for approximately 20 h/day, until November. The foals were turned out to the same pasture covered by snow for around 7 h/day and stabled individually overnight from December to April. The foals were weaned at 155.1 ± 15.5 days of age (mean ± s.d.). The foals and their dams were given supplementary grass hay and a balanced ration concentrate to maintain the dam’s body condition score [10] of 5.5–6.5 until weaning and the foal’s body condition score of 5.0–6.0 after weaning. Training for potential racing was begun at age 18–19 months and continued beyond the end of the study at 24 months. Ultrasonographic examination was performed on the day after birth (Day 1), at age one week, then at monthly intervals to age 12 months, and thereafter at 3 month intervals to age 24 months. Equine Veterinary Journal 47 (2015) 548–552 © 2015 EVJ Ltd
K. Korosue et al.
Cross-sectional area changes in distal limb tendon and ligament in foals
TABLE 1: Changes in superficial flexor tendon (SDFT), deep digital flexor tendon (DDFT), accessory ligament of the deep digital flexor tendon (ALDDFT) and suspensory ligament (SL) cross-sectional area (CSA) at each region measured by ultrasonography RSO
1D 1W 1M 2M 3M 4M 5M 6M 7M 8M 9M 10M 11M 12M 15M 18M 21M 24M
RSBO
SDFT
DDFT
ALDDF
SL
0.34 ± 0.06 0.35 ± 0.07 0.41 ± 0.07 0.48 ± 0.05 0.57 ± 0.09 0.66 ± 0.10 0.75 ± 0.10 0.81 ± 0.11 0.91 ± 0.12 0.97 ± 0.14†† 1.01 ± 0.14†† 1.02 ± 0.11†† 1.07 ± 0.10†† 1.13 ± 0.13†† 1.64 ± 0.25†† 1.53 ± 0.33†† 1.28 ± 0.21†† 1.28 ± 0.30††
0.41 ± 0.09 0.38 ± 0.08 0.46 ± 0.07* 0.51 ± 0.06 0.65 ± 0.08** 0.75 ± 0.08** 0.85 ± 0.10** 0.92 ± 0.09†* 0.93 ± 0.08 0.88 ± 0.09 0.83 ± 0.05 0.83 ± 0.06 0.86 ± 0.08 0.94 ± 0.09 1.07 ± 0.08 1.01 ± 0.10 0.82 ± 0.10 0.85 ± 0.07
0.32 ± 0.09 0.32 ± 0.07 0.39 ± 0.05** 0.47 ± 0.06** 0.54 ± 0.08 0.59 ± 0.10 0.66 ± 0.06** 0.69 ± 0.09 0.68 ± 0.09 0.61 ± 0.06 0.63 ± 0.08 0.57 ± 0.04 0.63 ± 0.05 0.69 ± 0.07 0.94 ± 0.10 0.92 ± 0.10 0.78 ± 0.07 0.84 ± 0.08
0.44 ± 0.07 0.53 ± 0.19†† 0.54 ± 0.09††* 0.64 ± 0.10††** 0.70 ± 0.09* 0.74 ± 0.08 0.80 ± 0.08 0.79 ± 0.14 0.76 ± 0.10 0.71 ± 0.09 0.69 ± 0.06 0.63 ± 0.04 0.68 ± 0.05 0.66 ± 0.05 1.01 ± 0.14 1.05 ± 0.10 0.98 ± 0.07 0.89 ± 0.05 †
RSBI
SDFT
DDFT
ALDDF
SL
0.30 ± 0.05 0.32 ± 0.05 0.37 ± 0.05 0.44 ± 0.05 0.55 ± 0.10** 0.67 ± 0.08* 0.74 ± 0.11 0.84 ± 0.13* 0.91 ± 0.12 0.92 ± 0.13 0.91 ± 0.15 0.86 ± 0.10 0.91 ± 0.08†† 0.96 ± 0.09†† 1.46 ± 0.15†† 1.43 ± 0.27†† 1.15 ± 0.18†† 1.07 ± 0.20††
0.26 ± 0.05 0.26 ± 0.06 0.31 ± 0.06 0.36 ± 0.06** 0.42 ± 0.06 0.49 ± 0.06 0.53 ± 0.05 0.54 ± 0.10 0.57 ± 0.09 0.58 ± 0.07 0.59 ± 0.05 0.57 ± 0.07 0.61 ± 0.05 0.65 ± 0.05 0.85 ± 0.14 0.77 ± 0.10 0.65 ± 0.09 0.67 ± 0.07
0.24 ± 0.06 0.23 ± 0.05 0.25 ± 0.03 0.32 ± 0.06** 0.42 ± 0.10 0.48 ± 0.05* 0.57 ± 0.08* 0.59 ± 0.09 0.59 ± 0.06 0.59 ± 0.09 0.61 ± 0.09 0.60 ± 0.06 0.66 ± 0.08 0.67 ± 0.10 0.87 ± 0.11 0.80 ± 0.06 0.67 ± 0.10 0.68 ± 0.05
0.38 ± 0.04 0.44 ± 0.08†† 0.51 ± 0.09††** 0.61 ± 0.08††* 0.66 ± 0.09†† 0.77 ± 0.08††** 0.84 ± 0.09†† 0.87 ± 0.10 0.87 ± 0.09 0.86 ± 0.09 0.85 ± 0.12 0.79 ± 0.10 0.84 ± 0.11 0.79 ± 0.09 1.05 ± 0.10 1.10 ± 0.12 1.00 ± 0.10 0.93 ± 0.08 ††
SDFT
DDFT
SL
0.28 ± 0.04 0.30 ± 0.05 0.38 ± 0.04 0.45 ± 0.06 0.57 ± 0.10* 0.68 ± 0.09* 0.77 ± 0.10 0.86 ± 0.13 0.91 ± 0.16 0.91 ± 0.15 0.86 ± 0.12 0.83 ± 0.08 0.88 ± 0.12 0.91 ± 0.09 1.44 ± 0.18 1.37 ± 0.25 1.06 ± 0.15 1.02 ± 0.14
0.33 ± 0.04 0.40 ± 0.05 0.54 ± 0.07†** 0.67 ± 0.07††** 0.84 ± 0.12††** 1.01 ± 0.08††** 1.06 ± 0.09†† 1.10 ± 0.08†† 1.17 ± 0.07†† 1.17 ± 0.10†† 1.14 ± 0.08†† 1.15 ± 0.06†† 1.25 ± 0.07†† 1.24 ± 0.09†† 1.54 ± 0.15 1.44 ± 0.09 1.25 ± 0.10†† 1.28 ± 0.06††
0.34 ± 0.04 0.40 ± 0.07 0.48 ± 0.05** 0.54 ± 0.08 0.64 ± 0.10** 0.78 ± 0.09** 0.84 ± 0.09 0.87 ± 0.11 0.87 ± 0.12 0.86 ± 0.11 0.87 ± 0.08 0.84 ± 0.06 0.82 ± 0.08 0.76 ± 0.04 1.07 ± 0.12 1.12 ± 0.12 0.94 ± 0.07 0.91 ± 0.04
RSO: region of suspensory origin; RSBO: region of the suspensory body; RSBI: region of suspensory bifurcation. *Within a group, value indicates that CSA is significantly larger than in the previous month (*P
