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. 2022 Oct 29;242(3):354–361. doi: 10.1111/joa.13785

An assessment of the variation of the intramuscular innervation of the gracilis muscle, with the aim of determining its neuromuscular compartments

Konrad Kurtys 1, Michał Podgórski 2, Bartosz Gonera 1, Teresa Vazquez 3, Łukasz Olewnik 1,✉
PMCID: PMC9919504  PMID: 36308488

Abstract

Some muscles present neuromuscular compartments, one of which is the gracilis muscle. The aim of the present study is to determine the number of compartments present within the gracilis muscle based on its intramuscular innervation patterns; such knowledge could be of value in free functional muscle transfer. The study comprised 72 gracilis muscles (38 women, 34 men), fixed in 10% formalin solution. The muscles were removed and then stained using Sihler's method. When sufficient transparency was achieved, some measurements were made. Three different types of intramuscular innervation were distinguished. Type I (70.8%) was featured by at least one direct proximal nerve branch. Type II (23.6%) presented at least one indirect proximal nerve branch. Type III (5.6%) did not possess any proximal nerve branch. The median of descended nerve branches was five. Considerable anatomical variation is possible within the intramuscular innervation of the gracilis muscle. The muscle presents neuromuscular compartments, but the exact number depends on the type of its intramuscular innervation and the number of the main descendent nerve branches. All three types seem to be appropriate for free functional muscle transfer. Our findings may be of great value for surgeons carrying out complex reconstructions with the use of the gracilis muscle.

Keywords: free functional muscle transfer, gracilis muscle, innervation, muscle compartments, nerve, Sihler's staining

All three types seem to be appropriate for free functional muscle transfer. Our findings may be of great value for surgeons carrying out complex reconstructions with the use of the gracilis muscle. The intramuscular innervation of the gracilis muscle is variable. The muscle presents neuromuscular compartments, but the exact number depends on the type of its intramuscular innervation and the number of the main descendent nerve branches.

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1. INTRODUCTION

The term “muscle compartment” was introduced in 1974 by Letbetter (1974). This phrase refers to a muscle part distinguished from the rest of muscle tissue by specific and identical muscle fiber orientation and the possession of a single direct nerve branch supplying an entire compartment. Additionally, septa composed of connective tissue exist between compartments. It has been proposed that some striated muscles consist of functionally independent neuromuscular subunits (compartments). A muscle presenting two or more compartments could be divided into entirely separately functioning muscle subunits, with potentially important clinical applications (English et al., 1993; English & Letbetter, 1982; English & Weeks, 1987; Kumar et al., 1998; Letbetter, 1974; Lim et al., 2004; Segal et al., 2002; Yu et al., 2010).

Free functional muscle transfer (FFMT) is a challenging surgical procedure in which a part of a muscle with its own vascularity and innervation (free functional muscle flap) is transplanted into a recipient site. The procedure has so far been performed using the gracilis muscle (GM), latissimus dorsi muscle, pectoralis minor muscle, serratus anterior muscle, and gastrocnemius muscle (Chwei‐Chin Chuang, 2009; Seal & Stevanovic, 2011). The main purpose of the procedure is to restore the lost function of a muscle, or muscles, in the case of long‐lasting facial palsy, traumatic loss of forearm muscle function, Volkmann's ischemic contracture or congenital muscle absence (Chwei‐Chin Chuang, 2009; Seal & Stevanovic, 2011).

The GM is a long, narrow, and relatively thin muscle located on the medial side of the thigh. The neural supply comes from the anterior branch of the obturator nerve, and its vascularity mainly from the deep femoral artery and medial circumflex femoral artery. The innervation and blood supply of the GM have been described previously (An et al., 2016; Crystal et al., 2005; Dziedzic et al., 2018; Fattah et al., 2013; Kumar et al., 1998; Kwon et al., 2009; Macchi et al., 2008; Magden et al., 2010; McKee et al., 1990; Meyers et al., 2005; Morris & Yang, 1999; Yan et al., 2019; Yu et al., 2010). Such knowledge is very valuable in planning transplant surgeries. In addition to FFMT, the GM can be used in surgery as a pedicled flap or free microsurgery flap (Chwei‐Chin Chuang, 2009; Morris & Yang, 1999; Vigato et al., 2007; Macchi et al., 2008).

Muscles demonstrate extramuscular and intramuscular innervation, distinguished by the motor entry point. An understanding of nerve patterns inside the muscle belly plays an important role in determining the number of neuromuscular compartments present in a specific muscle (An et al., 2016; Fattah et al., 2013; Kumar et al., 1998; Lim et al., 2004; Sanders et al., 1994; Segal, 1992; Segal et al., 2002; Yu et al., 2010, 2016). Intramuscular innervation can be investigated by (1) anatomical microdissection, (2) computerized reconstruction, or (3) Sihler's staining method (Gülekon et al., 2007; Yu et al., 2010). The most accurate method appears to be Sihler's staining, which was proven many times to visualize innervation patterns inside muscles, mucosa, and organs (Gülekon et al., 2007; Mu & Sanders, 2010; Won et al., 2012; Yu et al., 2010). The method stains myelinated nerve fibers while leaving other structures transparent or translucent (Mu & Sanders, 2010; Won et al., 2012).

Many muscles present variability with regard to its morphology, vascularity, and innervation (de Bonnecaze et al., 2019; Kaur et al., 2014; Magden et al., 2010; McKee et al., 1990; Olewnik, Karauda, et al., 2020; Olewnik, Kurtys, et al., 2020; Olewnik et al., 2019, 2021; Yang et al., 2003; Zielinska et al., 2021). The purpose of this study is to provide a complete description of the intramuscular innervation of GM. Such data will provide a better understanding of the neuromuscular compartments present in the GM, and a classification system of GM intramuscular innervation may prove to be a valuable tool for reconstructive surgeons performing FFMT.

2. MATERIALS AND METHODS

In total, 72 lower limbs (38 female and 34 male, 37 left and 35 right) were included in the research. They were fixed in a 10% formalin solution. The mean age of the cadavers “at death” 78.1 years (59–90). The cadavers were the property of the Department of Anatomical Dissection and Donation of Medical University of Lodz, Poland, and the Donors and Dissecting Rooms Center, Universidad Complutense de Madrid, Spain, 47 and 25 respectively. Any lower limbs that had undergone surgical intervention in the dissected region were excluded. The protocol of the study was accepted by the Bioethics Committee of the Medical University of Lodz (resolution RNN/259/21/KE).

In the first step, classical anatomical dissection was carried out. To reach the GM, the skin and subcutaneous tissue on the medial side of the thigh were first removed. Following this, the GM origin and insertion were revealed and cleansed. The anterior branch of the obturator nerve and the muscular nerve branch directed to the GM were then identified, and the origin, insertion, and muscular nerve branch were cut to remove the muscle from the body. Each GM was cleansed properly and prepared for modified Sihler's staining. This method included eight stages: (1) Fixation, (2) Maceration and depigmentation, (3) Decalcification, (4) Staining, (5) Destaining, (6) Neutralization, (7) Clearing, (8) Transparency. Each stage required a specific solution. After staining, for each GM the type of the intramuscular innervation was determined. Specific measurements were collected using a Mitutoyo electronic digital caliper (Mitutoyo Corporation, Kawasaki‐shi, Kanagawa, Japan). Each measurement was carried out twice with an accuracy of up to 0.1 mm.

2.1. Statistical analysis

The Statistica 13 software [TIBCO Software Inc. (2017). Statistica. http://statistica.io.] was used. Continuous data in subgroups had a distribution other than normal (according to Shapiro–Wilk test), thus nonparametric tests were used. In a comparison of morphometric parameters between sexes and body sides, the Many–Whitney and Wilcoxon tests were used, respectively. While in comparison of parameters between innervation types, the Kruskal–Wallis test by ranks with the dedicated post‐hoc test was employed. A p‐value of less than 0.05 was considered significant and modified for multiple testing with Bonferroni correction. Results are presented as mean and standard deviation unless otherwise stated.

3. RESULTS

A three‐fold classification of GM intramuscular innervation was created:

Type I (70.8%; 23 F; 28 M; 26 R; 25 L)—characterized by at least one direct proximal nerve branch. “Direct” means that this branch runs toward the proximal part of the muscle before it enters the muscle belly (Figure 1).

FIGURE 1.

FIGURE 1

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Type I intramuscular innervation of the gracilis muscle (right side). Blue arrows indicate direct proximal nerve branches intramuscularly. Green arrows indicate motor entry points of direct proximal nerve branches. Red arrows indicate descendent nerve branches.

Type II (23.6%; 11 F; 6 M; 9 R; 8 L)—characterized by at least one indirect proximal nerve branch. “Indirect” means that the proximal direction of this branch is visible only after it pierces the muscle belly (Figure 2).

FIGURE 2.

FIGURE 2

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Type II intramuscular innervation of the gracilis muscle (left side). Blue arrows indicate the indirect proximal nerve branch intramuscularly. The green arrow indicates motor entry point of the indirect proximal nerve branch. Red arrows indicate descendent nerve branches.

Type III (5.6%; 4 F; 0 M; 2 R; 2 L)—characterized by a lack of any proximal nerve branch (Figure 3).

FIGURE 3.

FIGURE 3

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Type III intramuscular innervation of the gracilis muscle (right side). Red arrows indicate descendent nerve branches.

All types demonstrated repetitive neural pattern in the distal two thirds of the muscle belly length: the nerve branches ran mostly longitudinally toward the distal end of the muscle belly, parallel to each other, vessels, and muscle fibers. The median of descendent nerve branches is 5 (ranges 3–7) and proximal intramuscular nerve branches 2 (ranges 0–4). Differences in morphometric parameters between sexes and body sides are presented in Table 1., whereas differences in morphometric parameters between intramuscular innervation types are presented in Table 2.

TABLE 1.

Differences in morphometric parameters between sexes and body sides

Parameter Sex Body side
F M p L R p
Muscle belly length 291.59 (36.43) 309.46 (27.24) 0.0113 299.45 (34.77) 300.58 (32.58) 0.8569
Distance from the origin to the first intramuscular nerve branch 59.09 (16.46) 50.51 (16.18) 0.0299 55.79 (15.76) 54.33 (17.87) 0.9461
Distance from the origin to the beginning of the greatest nerve branches density zone 88.88 (13.15) 94.53 (11.55) 0.0429 91.03 (11.96) 92.04 (13.42) 0.6850
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TABLE 2.

Differences in morphometric parameters between intramuscular innervation types

Parameter Muscle innervation types
I II III p
Muscle belly length 302.22 (32.08) 302.01 (35.46) 263.64 (26.73) 0.0936
Distance from the origin to the first intramuscular nerve branch 55.24 (17.65) 49.80 (12.15) 74.66 (3.46) 0.0151
Distance from the origin to the beginning of the greatest nerve branches density zone 93.67 (13.25) 85.94 (10.43) 88.26 (3.91) 0.0423
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We also calculated the coefficient between the distance from the origin to the beginning of the greatest nerve branches density zone (Figure 4a) and the muscle belly length. The mean for the whole group was 31.1% ± 3.5%, while for each type was as follows: type I: 31.0 ± 3.3; type II: 28.7 ± 3.6; type III: 33.6 ± 2.3. The difference between types was significant (p = 0.0179) and according to post hoc test, it was because the difference between types II and III.

FIGURE 4.

FIGURE 4

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(a) The approximate site where the zone of the greatest nerve branches density starts. The beginning of this zone is indicated by the green line. (b) Proximal (red surround) and distal (blue surround) neuromuscular compartments, as exemplified by type I. (c) A possible division of the distal two thirds of the muscle belly into three neuromuscular compartments. Dashed yellow lines indicate borders between neuromuscular compartments.

4. DISCUSSION

The intramuscular innervation of the GM has been the subject of previous studies (An et al., 2016; Fattah et al., 2013; Kumar et al., 1998; Morris & Yang, 1999; Won et al., 2012; Yan et al., 2019; Yu et al., 2010). Yan et al. (2019) indicated two groups of nerve branches inside the muscle belly: the first consisting of four or five thin branches heading to the origin, insertion, and anterior margin of the muscle, and the second consisting of eight or nine small branches creating a fan‐shaped distribution toward the posterior muscle boundary. Some of these nerve branches run toward the muscle origin and others toward the insertion. Yu et al. (2010) described three intramuscular nerve divisions. An upper group innervated the proximal part of the muscle, while the two others descended distally to the musculotendinous junction, running parallel to each other, and dividing into thinner branches. Some connections between these two divisions running distally were observed. Similarly, Kumar et al. (1998) and Morris and Yang (1999) indicate the presence of some parallel intramuscular nerve branches directed distally with one or two smaller ones running proximally. Morris and Yang (1999) found the proximally oriented branches to be parallel to the muscle fibers, while Kumar et al. (1998) report that those branches did not present any organized structure or crossed muscle fibers. According to our proposed classification, such cases where the proximal part of the muscle is innervated by the nerve branch(es) which proximal direction is visible only intramuscularly are classified as Type II (Figure 2). Such proximal nerve branch is called indirect and means that the branch emerges from one of the main nerve branches after it enters the muscle belly. Fattah et al. (2013) report the presence of above‐mentioned proximal branch(es) in 16 of 20 studied cases. The remaining four GMs demonstrated Type III intramuscular innervation (Figure 3), according to our proposed classification, because the proximal part of the muscle was not innervated. Won et al. (2012) describe the presence of four to seven nerve branches running distally, parallel to each other, after entering the muscle belly. Interestingly, there was no mention of branches innervating the proximal part of the GM; therefore, all muscles from the study also presented Type III intramuscular innervation (Figure 3). In contrast to the above‐mentioned studies, An et al. (2016) report the presence of a small nerve branch in all cases; this arose from one of the main extramuscular branches and innervated the proximal part of the muscle belly. Its intramuscular course was assessed as oblique to the muscle fibers, while other nerve branches run parallel in the direction of the musculotendinous junction; this corresponds to our proposed type I (Figure 1), characterized by a direct proximal nerve branch(es) emerging from the main nerve branch yet before it enters the muscle belly. As a result, its proximal direction is well visible intramuscularly as well as extramuscularly. Apart from more visible differences, all our types (I, II, III), presented various numbers of intramuscular nerve branches running longitudinally toward the musculotendinous junction, parallel to muscle fibers (on average 5, ranges 3–7).

FFMT is performed by clinicians when restoration of a muscle function is needed. The GM, because of its really precious anatomical features, was used as the first muscle in this surgical procedure (Chwei‐Chin Chuang, 2009; Harii et al., 1976; Seal & Stevanovic, 2011). Nowadays, other muscles are also utilized in FFMT but the GM still remains one of the best options. Generally, as a free functional muscle flap, it is possible to use either a whole muscle or only part of it (Chwei‐Chin Chuang, 2009; Seal & Stevanovic, 2011). However, if only part of the muscle is harvested, the rest of the muscle tissue remains denervated, because an entire main motor nerve twig is cut. It has been noted that some muscles can be divided into a few independent neuromuscular compartments with their own innervation supplied by a single main nerve branch (English et al., 1993; English & Letbetter, 1982; English & Weeks, 1987; Kumar et al., 1998; Letbetter, 1974; Lim et al., 2004; Sanders et al., 1994; Segal, 1992; Segal et al., 2002; Yu et al., 2010). This feature could greatly extend the possibilities for muscles to be used as free functional muscle flaps. When a muscle presents at least two neuromuscular compartments, it would allow reconstructive surgeons to utilize a segment as an independently functioning subunit without any failure of the remaining muscle part. Furthermore, some muscles which consist of a few compartments may be used for complex reconstructions needing more than one free functional muscle flap (Kumar et al., 1998; Lim et al., 2004; Morris & Yang, 1999; Yu et al., 2016).

Some interesting studies have examined the neuromuscular compartments present in different muscles (An et al., 2016; English & Letbetter, 1982; English & Weeks, 1987; Kumar et al., 1998; Liu et al., 1997; Olewnik, Karauda, et al., 2020, Olewnik, Kurtys, et al., 2020; Ravichandiran et al., 2012; Sanders et al., 1994; Segal, 1992; Segal et al., 2002; Yu et al., 2010, 2016). Lim et al. (2004) propose a threefold classification for the muscles of the upper limb based on their shape and tendon morphology, with each muscle type having specific patterns of intramuscular innervation. Based on this classification, it was suggested that some muscles (types IIb and III) present neuromuscular compartments, and are hence appropriate for splitting into at least two subunits, while others (types I and IIa) do not. Flat, trapezoidal, or triangular muscles were categorized as type I (e.g., deltoid muscle), spindle‐shaped unipennate ones as type IIa (e.g., extensor pollicis longus), spindle‐shaped bipennate ones as type IIb (e.g., flexor carpi ulnaris muscle), and those possessing more than one head of origin (e.g., biceps brachii muscle) or tendon of insertion (e.g., flexor digitorum profundus muscle) as type III. Yu et al. (2010) report that, according to Lim's classification (Lim et al., 2004), the GM should be categorized as type IIa (uni‐pennate muscles). However, this type of a muscle is considered inappropriate for splitting into entirely separate functional subunits. In contrast to Lim's classification (Lim et al., 2004), Yu et al. (2010) indicate that intramuscular innervation of the GM can be divided into two independent subunits within the distal two thirds of the muscle belly. Kumar et al. (1998) indicate that the GM can be split longitudinally into two or more neuromuscular compartments, with each compartment possessing its own nerve twig and hence potentially being suitable for transfer as a free functional muscle flap. This was confirmed by Fattah et al. (2013). Finally, despite not reporting the number of possible compartments some researchers (An et al., 2016; Morris & Yang, 1999) agreed that due to the intramuscular course of nerve branches, i.e. longitudinal and parallel to muscular fibers, the GM seems to be a very good choice for division and use in FFMT.

The existence of muscle compartments has also been confirmed in vivo by electrical nerve stimulation (Kumar et al., 1998;Manktelow & Zuker, 1984; McKee et al., 1990). In this case, all extramuscular terminal nerve branches were separately stimulated. While stimulating each branch, the relevant longitudinal muscle segment responded and contracted as the remaining parts were relaxed, or some of them twitched subtly (Manktelow & Zuker, 1984; McKee et al., 1990). According to Kumar et al. (1998), after splitting the muscle, innervation was preserved in both parts, and the stimulation of each separate nerve subdivision (anterior and posterior) caused an independent contraction in the respective muscle segment. Although some connections between intramuscular nerve branches were also noticed in two of the above‐mentioned studies (Kumar et al., 1998; McKee et al., 1990). Kumar et al. (1998) suggest that for clinical purposes, this was unimportant.

The studied GMs were found to present different numbers of neuromuscular compartments. Type I, characterized by a direct proximal nerve branch, has at least two neuromuscular compartments: proximal and distal (Figure 4b). In our opinion, it is feasible to divide the distal one into more compartments, but this would depend on the number of main nerve branches running intramuscularly. In type II, the proximal part is innervated, but by the indirect proximal nerve branch; therefore, the proximal part cannot be assessed as a distinct compartment, because it appears to be unsplittable. Nevertheless, dividing the muscle into neuromuscular subunits may be also possible, considering that the other intramuscular nerve branches follow a longitudinal and organized course (Figure 4c). Type III, in contrast, demonstrates a lack of innervation in the proximal part. In this case, the muscle has a similar potential for splitting as type II, and this possibility depends on the number of intramuscular nerve branches heading distally. Comparing our results with Lim's classification (Lim et al., 2004), we suggest that it is inappropriate to generalize muscular innervation on the basis of muscle shape and tendon morphology. Rather, each particular muscle should be subjected to a specific and exhaustive examination with regard to its innervation to confirm whether separate neuromuscular compartments are present.

The coefficient between the distance from the origin of GM to the beginning of the greatest nerve branches density zone and the muscle belly length is another significant finding from our research. For the whole examined group, the mean coefficient was 31.1% ± 3.5%. The zone of the greatest nerve branches density starts at this length (Figure 4a) and ends near the musculotendinous junction. This is possible that for the best clinical results, muscle part(s) used in FFMT should originate from aforementioned zone, because in this length range the GM seems to be innervated the best.

This study presents a new classification system derived from an exhaustive examination of the intramuscular innervation of the GM. Our findings expand existing knowledge about GM anatomy, which may help clinicians to improve the possibilities of FFMT. They also confirm that precise and comprehensive research is necessary to find and understand the variability of muscle innervation. Nevertheless, this study has some limitations. Firstly, no electrical nerve stimulation was carried out, and hence it is not possible to correlate it with our findings. In addition, this research does not indicate the best method for determining the type of intramuscular innervation of the GM in vivo.

5. CONCLUSION

The GM is variable with regard to innervation; however, our findings allow the intramuscular innervation to be classified into three types, all of which seem to be suitable for FFMT. The GM can be divided into neuromuscular compartments, but their number depends on the type of intramuscular innervation, and the number of intramuscular main nerve branches running longitudinally toward the musculotendinous junction. Our findings also emphasize the importance of examining the innervation of each individual muscle rather than generalizing their neural patterns based on shape or tendon morphology. The demonstrated classification system may be a valuable tool for reconstructive surgeons performing FFMT using GM.

AUTHOR CONTRIBUTIONS

Konrad Kurtys (M.D.)—assistant—project development, data collection and management, photographic documentation, data analysis, and manuscript writing. Michał Podgórski (M.D., Ph.D.)—associate professor—data analysis, statistical analysis, and manuscript editing. Bartosz Gonera (M.D.)—assistant—data analysis and manuscript editing. Teresa Vazquez (M.D., Ph.D.)—professor—data analysis and manuscript editing. Łukasz Olewnik (D.P.T., Ph.D.)—associate professor—data analysis and manuscript editing. All authors have read and approved the manuscript.

FUNDING INFORMATION

This research received no external funding.

CONFLICT OF INTEREST

The authors declare that they have no competing interests.

ETHICS APPROVAL AND CONSENT TO PARTICIPATE

The protocol of the study was accepted by Bioethics Committee of Medical University of Lodz (resolution RNN/259/21/KE). The cadavers were the property of the Department of Anatomical Dissection and Donation, Medical University of Lodz, Poland and the Donors and Dissecting Rooms Center, Universidad Complutense de Madrid, Spain. Informed consent was obtained from all participants before they died.

ACKNOWLEDGMENTS

The authors wish to express their gratitude to all those who donated their bodies to medical science.

Kurtys, K. , Podgórski, M. , Gonera, B. , Vazquez, T. & Olewnik, Ł. (2023) An assessment of the variation of the intramuscular innervation of the gracilis muscle, with the aim of determining its neuromuscular compartments. Journal of Anatomy, 242, 354–361. Available from: 10.1111/joa.13785

DATA AVAILABILITY STATEMENT

Konrad Kurtys (MD, PhD) ‐ assistant ‐ project development, data collection and management, data analysis and manuscript writing; Michał Podgórski (MD, PhD) ‐ Associate Professor. ‐ radiological data collection, analysis and manuscript writing; Bartosz Gonera (MD)‐ assistant ‐ data analysis and manuscript writing; Teresa Vazquez (MD, PhD) ‐ professor ‐ data analysis and manuscript editing; Łukasz Olewnik (MD, PhD) ‐ Professor ‐ numerous consultations, observations, suggestions related to the paper, data analysis and manuscript editing.

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Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Data Availability Statement

Konrad Kurtys (MD, PhD) ‐ assistant ‐ project development, data collection and management, data analysis and manuscript writing; Michał Podgórski (MD, PhD) ‐ Associate Professor. ‐ radiological data collection, analysis and manuscript writing; Bartosz Gonera (MD)‐ assistant ‐ data analysis and manuscript writing; Teresa Vazquez (MD, PhD) ‐ professor ‐ data analysis and manuscript editing; Łukasz Olewnik (MD, PhD) ‐ Professor ‐ numerous consultations, observations, suggestions related to the paper, data analysis and manuscript editing.

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