American Society of Biomechanics Journal of Biomechanics Award 2022: Computer models do not accurately predict human muscle passive muscle force and fiber length: Evaluating subject-specific modeling impact on musculoskeletal model predictions.

Musculoskeletal models are valuable for studying and understanding the human body in a variety of clinical applications that include surgical planning, injury prevention, and prosthetic design. Subject-specific models have proven to be more accurate and useful compared to generic models. Nevertheless, it is important to validate all models when possible. To this end, gracilis muscle-tendon parameters were directly measured intraoperatively and used to test model predictions. The aim of this study was to evaluate the benefits and limitations of systematically incorporating subject-specific variables into muscle models used to predict passive force and fiber length. The results showed that incorporating subject-specific values generally reduced errors, although significant errors still existed. Optimization of the modeling parameter "tendon slack length" was explored in two cases: minimizing fiber length error and minimizing passive force error. The results showed that using all subject-specific values yielded the most favorable outcome in both models and optimization cases. However, the trade-off between fiber length error and passive force error will depend on the specific circumstances and research objectives due to significant individual errors. Notably, individual fiber length and passive force errors were as high as 20% and 37% respectively. Finally, the modeling parameter "tendon slack length" did not correlate with any real-world anatomical length.

Optimal Distal Tendon Insertion Point for Elbow Flexion in Free-Functioning Gracilis Muscle Transfer for Panbrachial Plexus Injuries: A Cadaveric Study.

PURPOSE: Following pan-brachial plexus injuries, restoration of elbow flexion is widely accepted as the reconstructive priority. A gracilis free functioning muscle transfer (FFMT) can be used to restore elbow flexion alone with insertion into the biceps brachii (BIC) or brachioradialis (BRD) tendons or restore combined elbow and finger flexion with a more distal insertion into the flexor digitorum profundus (FDP) tendons. Using cadaveric experiments, we determined the peak instantaneous moment arm for each insertion option. METHODS: Six simulated gracilis transfer surgeries were performed using both arms of three fresh-frozen full body cadaveric specimens (age: 79 + 10 years. 2 female). The gracilis muscles from both legs were harvested and transferred to the contralateral upper extremity. The elbow was manually moved through three flexion-extension cycles while the instantaneous moment arm was calculated from measurements of gracilis excursion and elbow joint angle for the three distal insertion sites. RESULTS: Peak instantaneous moment arm for all three insertions occurred at an elbow angle between 83° to 92° with a magnitude ranging from 33 mm to 54 mm. The more distal (FDP/BRD) insertions produced a significantly greater (∼1.5 times) peak elbow flexion instantaneous moment arm compared to the BIC insertion. CONCLUSIONS: Based on the instantaneous moment arm, the gracilis FFMT distal insertion locations could result in greater reconstructed elbow flexion strength. In addition, direct measurement of the shape and magnitude of the moment arm curve for differing insertion sites allows high resolution surgical planning and model testing. CLINICAL RELEVANCE: This study presents the first direct experimental quantification of the gracilis FFMT instantaneous moment arm. The experimental evidence supports the use of FDP/BRD insertion locations by providing a quantitative explanation for the increased elbow flexion torque observed clinically in patients with a gracilis FFMT and distal FDP insertion.

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-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 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.

Procedures for obtaining muscle physiology parameters during a gracilis free-functioning muscle transfer in adult patients with brachial plexus injury.

A complete understanding of muscle mechanics allows for the creation of models that closely mimic human muscle function so they can be used to study human locomotion and evaluate surgical intervention. This includes knowledge of muscle-tendon parameters required for accurate prediction of muscle forces. However, few studies report experimental data obtained directly from whole human muscle due to the invasive nature of these experiments. This article presents an intraoperative, in vivo measurement protocol for whole muscle-tendon parameters that include muscle-tendon unit length, sarcomere length, passive tension, and active tension in response to external stimulation. The advantage of this protocol is the ability to obtain these rare experimental data in situ in addition to muscle volume and weight since the gracilis is also completely removed from the leg. The entire protocol including the surgical steps for gracilis harvest takes ~ 3 h. Actual testing of the gracilis where experimental data is measured takes place within a 30-min window during surgery.

In vivo human gracilis whole-muscle passive stress-sarcomere strain relationship.

We measured the passive mechanical properties of intact, living human gracilis muscles (n=11 individuals, 10 male and 1 female, age: 33±12 years, mass: 89±23 kg, height: 177±8 cm). Measurements were performed in patients undergoing surgery for free-functioning myocutaneous tissue transfer of the gracilis muscle to restore elbow flexion after brachial plexus injury. Whole-muscle force of the gracilis tendon was measured in four joint configurations (JC1-JC4) with a buckle force transducer placed at the distal tendon. Sarcomere length was also measured by biopsy from the proximal gracilis muscle. After the muscle was removed, a three-dimensional volumetric reconstruction of the muscle was created via photogrammetry. Muscle length from JC1 to JC4 increased by 3.3±1.0, 7.7±1.2, 10.5±1.3 and 13.4±1.2 cm, respectively, corresponding to 15%, 34%, 46% and 59% muscle fiber strain, respectively. Muscle volume and an average optimal fiber length of 23.1±0.7 cm yielded an average muscle physiological cross-sectional area of 6.8±0.7 cm2 which is approximately 3 times that measured previously from cadaveric specimens. Absolute passive tension increased from 0.90±0.21 N in JC1 to 16.50±2.64 N in JC4. As expected, sarcomere length also increased from 3.24±0.08 µm at JC1 to 3.63±0.07 µm at JC4, which are on the descending limb of the human sarcomere length-tension curve. Peak passive muscle stress was 27.8±5.5 kPa in JC4 and muscle modulus ranged from 44.8 MPa in JC1 to 125.7 MPa in JC4. Comparison with other mammalian species indicates that human muscle passive mechanical properties are more similar to rodent muscle than to rabbit muscle. These data provide direct measurements of whole-human muscle passive mechanical properties that can be used in modeling studies and for understanding comparative passive mechanical properties among mammalian muscles.

Measuring and modeling in vivo human gracilis muscle-tendon unit length.

Musculoskeletal models rely heavily on the use of an anatomical dataset and clearly defined assumptions to accurately model the subject being studied. Therefore, it is important to understand the limitations of using musculoskeletal models to study individuals. This paper describes a method of measuring in vivo gracilis muscle-tendon unit length and presents a comparison of experimental data versus predictions from four musculoskeletal models in OpenSim. The largest errors occurred when the knee was fully extended. At this position, the absolute average muscle-tendon unit length error was 7% and the absolute average fiber length error was between 15% and 32%. However, the variability of these errors was significant. Manual linear scaling based on an anthropometric database did not capture the variability observed in subjects. The fiber length errors observed are predicted to have a significant impact on muscle force production that may not represent true subject specific force-length relationship of the gracilis.