Direct intraoperative measurement of isometric contractile properties in living human muscle

Skeletal muscle's isometric contractile properties are one of the classic structure–function relationships in all of biology allowing for extrapolation of single fibre mechanical properties to whole muscle properties based on the muscle's optimal fibre length and physiological cross‐sectio...

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Veröffentlicht in:The Journal of physiology 2023-05, Vol.601 (10), p.1817-1830
Hauptverfasser: Binder‐Markey, Benjamin I., Persad, Lomas S., Shin, Alexander Y., Litchy, William J., Kaufman, Kenton R., Lieber, Richard L.
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container_end_page 1830
container_issue 10
container_start_page 1817
container_title The Journal of physiology
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creator Binder‐Markey, Benjamin I.
Persad, Lomas S.
Shin, Alexander Y.
Litchy, William J.
Kaufman, Kenton R.
Lieber, Richard L.
description Skeletal muscle's isometric contractile properties are one of the classic structure–function relationships in all of biology allowing for extrapolation of single fibre mechanical properties to whole muscle properties based on the muscle's optimal fibre length and physiological cross‐sectional area (PCSA). However, this relationship has only been validated in small animals and then extrapolated to human muscles, which are much larger in terms of length and PCSA. The present study aimed to measure directly the in situ properties and function of the human gracilis muscle to validate this relationship. We leveraged a unique surgical technique in which a human gracilis muscle is transferred from the thigh to the arm, restoring elbow flexion after brachial plexus injury. During this surgery, we directly measured subject specific gracilis muscle force–length relationship in situ and properties ex vivo. Each subject's optimal fibre length was calculated from their muscle's length‐tension properties. Each subject's PCSA was calculated from their muscle volume and optimal fibre length. From these experimental data, we established a human muscle fibre‐specific tension of 171 kPa. We also determined that average gracilis optimal fibre length is 12.9 cm. Using this subject‐specific fibre length, we observed an excellent fit between experimental and theorical active length‐tension curves. However, these fibre lengths were about half of the previously reported optimal fascicle lengths of 23 cm. Thus, the long gracilis muscle appears to be composed of relatively short fibres acting in parallel that may not have been appreciated based on traditional anatomical methods. Key points Skeletal muscle's isometric contractile properties represent one of the classic structure–function relationships in all of biology and allow scaling single fibre mechanical properties to whole muscle properties based on the muscle's architecture. This physiological relationship has only been validated in small animals but is often extrapolated to human muscles, which are orders of magnitude larger. We leverage a unique surgical technique in which a human gracilis muscle is transplanted from the thigh to the arm to restore elbow flexion after brachial plexus injury, aiming to directly measure muscles properties in situ and test directly the architectural scaling predictions. Using these direct measurements, we establish human muscle fibre‐specific tension of ∼170 kPa. Furthermore, we show that the
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However, this relationship has only been validated in small animals and then extrapolated to human muscles, which are much larger in terms of length and PCSA. The present study aimed to measure directly the in situ properties and function of the human gracilis muscle to validate this relationship. We leveraged a unique surgical technique in which a human gracilis muscle is transferred from the thigh to the arm, restoring elbow flexion after brachial plexus injury. During this surgery, we directly measured subject specific gracilis muscle force–length relationship in situ and properties ex vivo. Each subject's optimal fibre length was calculated from their muscle's length‐tension properties. Each subject's PCSA was calculated from their muscle volume and optimal fibre length. From these experimental data, we established a human muscle fibre‐specific tension of 171 kPa. We also determined that average gracilis optimal fibre length is 12.9 cm. Using this subject‐specific fibre length, we observed an excellent fit between experimental and theorical active length‐tension curves. However, these fibre lengths were about half of the previously reported optimal fascicle lengths of 23 cm. Thus, the long gracilis muscle appears to be composed of relatively short fibres acting in parallel that may not have been appreciated based on traditional anatomical methods. Key points Skeletal muscle's isometric contractile properties represent one of the classic structure–function relationships in all of biology and allow scaling single fibre mechanical properties to whole muscle properties based on the muscle's architecture. This physiological relationship has only been validated in small animals but is often extrapolated to human muscles, which are orders of magnitude larger. We leverage a unique surgical technique in which a human gracilis muscle is transplanted from the thigh to the arm to restore elbow flexion after brachial plexus injury, aiming to directly measure muscles properties in situ and test directly the architectural scaling predictions. Using these direct measurements, we establish human muscle fibre‐specific tension of ∼170 kPa. Furthermore, we show that the gracilis muscle actually functions as a muscle with relatively short fibres acting in parallel vs. long fibres as previously assumed based on traditional anatomical models. figure legend Schematic of a unique surgical procedure in which the gracilis muscle is removed from the medial thigh and transplanted into the bed of the biceps brachii muscle to restore elbow flexion after brachial plexus injury as a free functioning muscle transfer (top). During this surgery and prior to removal of the gracilis from the lower limb, we have the unique opportunity to measure the subject specific gracilis muscle force–length relationship directly. The muscle's nerve was stimulated to produce an isometric contraction during which gracilis force was measured at the distal insertion tendon using a buckle force transducer (bottom left). By moving the lower limb into four positions, we can recreate the normalized muscle force–length relationship (bottom right) and, using subject‐specific fibre lengths (solid grey line), we can accurately predict the muscle properties. By contrast, literature anatomical fascicle length values (dashed grey line) do not accurately predict the muscle's properties. 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However, this relationship has only been validated in small animals and then extrapolated to human muscles, which are much larger in terms of length and PCSA. The present study aimed to measure directly the in situ properties and function of the human gracilis muscle to validate this relationship. We leveraged a unique surgical technique in which a human gracilis muscle is transferred from the thigh to the arm, restoring elbow flexion after brachial plexus injury. During this surgery, we directly measured subject specific gracilis muscle force–length relationship in situ and properties ex vivo. Each subject's optimal fibre length was calculated from their muscle's length‐tension properties. Each subject's PCSA was calculated from their muscle volume and optimal fibre length. From these experimental data, we established a human muscle fibre‐specific tension of 171 kPa. We also determined that average gracilis optimal fibre length is 12.9 cm. Using this subject‐specific fibre length, we observed an excellent fit between experimental and theorical active length‐tension curves. However, these fibre lengths were about half of the previously reported optimal fascicle lengths of 23 cm. Thus, the long gracilis muscle appears to be composed of relatively short fibres acting in parallel that may not have been appreciated based on traditional anatomical methods. Key points Skeletal muscle's isometric contractile properties represent one of the classic structure–function relationships in all of biology and allow scaling single fibre mechanical properties to whole muscle properties based on the muscle's architecture. This physiological relationship has only been validated in small animals but is often extrapolated to human muscles, which are orders of magnitude larger. We leverage a unique surgical technique in which a human gracilis muscle is transplanted from the thigh to the arm to restore elbow flexion after brachial plexus injury, aiming to directly measure muscles properties in situ and test directly the architectural scaling predictions. Using these direct measurements, we establish human muscle fibre‐specific tension of ∼170 kPa. Furthermore, we show that the gracilis muscle actually functions as a muscle with relatively short fibres acting in parallel vs. long fibres as previously assumed based on traditional anatomical models. figure legend Schematic of a unique surgical procedure in which the gracilis muscle is removed from the medial thigh and transplanted into the bed of the biceps brachii muscle to restore elbow flexion after brachial plexus injury as a free functioning muscle transfer (top). During this surgery and prior to removal of the gracilis from the lower limb, we have the unique opportunity to measure the subject specific gracilis muscle force–length relationship directly. The muscle's nerve was stimulated to produce an isometric contraction during which gracilis force was measured at the distal insertion tendon using a buckle force transducer (bottom left). By moving the lower limb into four positions, we can recreate the normalized muscle force–length relationship (bottom right) and, using subject‐specific fibre lengths (solid grey line), we can accurately predict the muscle properties. By contrast, literature anatomical fascicle length values (dashed grey line) do not accurately predict the muscle's properties. The long gracilis muscle appears to be composed of relatively short fibres that may not have been appreciated based on traditional anatomical methods.</description><subject>Animals</subject><subject>Arm</subject><subject>Biomechanical Phenomena</subject><subject>Brachial plexus</subject><subject>Elbow</subject><subject>Humans</subject><subject>Isometric Contraction</subject><subject>Mechanical properties</subject><subject>muscle architecture</subject><subject>Muscle contraction</subject><subject>Muscle Fibers, Skeletal - physiology</subject><subject>muscle modelling</subject><subject>Muscle, Skeletal - physiology</subject><subject>Musculoskeletal system</subject><subject>orthopaedic surgery</subject><subject>Physiology</subject><subject>Skeletal muscle</subject><subject>specific tension</subject><subject>Structure-function relationships</subject><subject>Surgical techniques</subject><issn>0022-3751</issn><issn>1469-7793</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2023</creationdate><recordtype>article</recordtype><sourceid>24P</sourceid><sourceid>WIN</sourceid><sourceid>EIF</sourceid><recordid>eNp1kEtLJTEQhYM4jFcd8BdIwI2bdlKppJMsxbcI48LZCU13uloj_bgm3Vf899MXXyDMqqD4zuHwMbYH4ggA8Pf1rbRKOLnBFqBylxnjcJMthJAyQ6Nhi22n9CQEoHDuJ9vC3AkthViw-9MQyY889GMshyXFcgwr4h2VaYrUUT_yoeEhDR2NMXjuhzXox9ASX8Z1YAyU5jhvwyr0D_xx6sqed1PyLe2yH03ZJvr1fnfY3_Ozu5PL7ObPxdXJ8U3m0SqTealRVgqdrJtaqspbhRqstlUDtja2RAvK5_X8qYUBCaL2zjR1XlkkSYg77PCtd170PFEaiy4kT21b9jRMqZDG5iCUBj2jB9_Qp2GK_byukBZQS0R0X4U-DilFaoplDF0ZXwsQxdp48WF8RvffC6eqo_oT_FA8A0dvwMvs7PW_RcXd9S1o5Qz-AwBliKg</recordid><startdate>20230501</startdate><enddate>20230501</enddate><creator>Binder‐Markey, Benjamin I.</creator><creator>Persad, Lomas S.</creator><creator>Shin, Alexander Y.</creator><creator>Litchy, William J.</creator><creator>Kaufman, Kenton R.</creator><creator>Lieber, Richard L.</creator><general>Wiley Subscription Services, Inc</general><scope>24P</scope><scope>WIN</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QP</scope><scope>7QR</scope><scope>7TK</scope><scope>7TS</scope><scope>8FD</scope><scope>FR3</scope><scope>P64</scope><scope>7X8</scope><orcidid>https://orcid.org/0000-0001-8920-4381</orcidid><orcidid>https://orcid.org/0000-0002-7203-4520</orcidid></search><sort><creationdate>20230501</creationdate><title>Direct intraoperative measurement of isometric contractile properties in living human muscle</title><author>Binder‐Markey, Benjamin I. ; 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However, this relationship has only been validated in small animals and then extrapolated to human muscles, which are much larger in terms of length and PCSA. The present study aimed to measure directly the in situ properties and function of the human gracilis muscle to validate this relationship. We leveraged a unique surgical technique in which a human gracilis muscle is transferred from the thigh to the arm, restoring elbow flexion after brachial plexus injury. During this surgery, we directly measured subject specific gracilis muscle force–length relationship in situ and properties ex vivo. Each subject's optimal fibre length was calculated from their muscle's length‐tension properties. Each subject's PCSA was calculated from their muscle volume and optimal fibre length. From these experimental data, we established a human muscle fibre‐specific tension of 171 kPa. We also determined that average gracilis optimal fibre length is 12.9 cm. Using this subject‐specific fibre length, we observed an excellent fit between experimental and theorical active length‐tension curves. However, these fibre lengths were about half of the previously reported optimal fascicle lengths of 23 cm. Thus, the long gracilis muscle appears to be composed of relatively short fibres acting in parallel that may not have been appreciated based on traditional anatomical methods. Key points Skeletal muscle's isometric contractile properties represent one of the classic structure–function relationships in all of biology and allow scaling single fibre mechanical properties to whole muscle properties based on the muscle's architecture. This physiological relationship has only been validated in small animals but is often extrapolated to human muscles, which are orders of magnitude larger. We leverage a unique surgical technique in which a human gracilis muscle is transplanted from the thigh to the arm to restore elbow flexion after brachial plexus injury, aiming to directly measure muscles properties in situ and test directly the architectural scaling predictions. Using these direct measurements, we establish human muscle fibre‐specific tension of ∼170 kPa. Furthermore, we show that the gracilis muscle actually functions as a muscle with relatively short fibres acting in parallel vs. long fibres as previously assumed based on traditional anatomical models. figure legend Schematic of a unique surgical procedure in which the gracilis muscle is removed from the medial thigh and transplanted into the bed of the biceps brachii muscle to restore elbow flexion after brachial plexus injury as a free functioning muscle transfer (top). During this surgery and prior to removal of the gracilis from the lower limb, we have the unique opportunity to measure the subject specific gracilis muscle force–length relationship directly. The muscle's nerve was stimulated to produce an isometric contraction during which gracilis force was measured at the distal insertion tendon using a buckle force transducer (bottom left). By moving the lower limb into four positions, we can recreate the normalized muscle force–length relationship (bottom right) and, using subject‐specific fibre lengths (solid grey line), we can accurately predict the muscle properties. By contrast, literature anatomical fascicle length values (dashed grey line) do not accurately predict the muscle's properties. 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subjects Animals
Arm
Biomechanical Phenomena
Brachial plexus
Elbow
Humans
Isometric Contraction
Mechanical properties
muscle architecture
Muscle contraction
Muscle Fibers, Skeletal - physiology
muscle modelling
Muscle, Skeletal - physiology
Musculoskeletal system
orthopaedic surgery
Physiology
Skeletal muscle
specific tension
Structure-function relationships
Surgical techniques
title Direct intraoperative measurement of isometric contractile properties in living human muscle
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