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. 2014 Jan 29;224(4):499–508. doi: 10.1111/joa.12157

Distribution of sensory nerve endings around the human sinus tarsi: a cadaver study

Susanne Rein 1,✉, Suzanne Manthey 1, Hans Zwipp 1, Andreas Witt 2
PMCID: PMC4098683  PMID: 24472004

Abstract

The aim of this study was to analyse the pattern of sensory nerve endings and blood vessels around the sinus tarsi. The superficial and deep parts of the fat pads at the inferior extensor retinaculum (IER) as well as the subtalar joint capsule inside the sinus tarsi from 13 cadaver feet were dissected. The distribution of the sensory nerve endings and blood vessels were analysed in the resected specimens as the number per cm2 after staining with haematoxylin-eosin, S100 protein, low-affinity neurotrophin receptor p75, and protein gene product 9.5 using the classification of Freeman and Wyke. Free nerve endings were the predominant sensory ending (P < 0.001). Ruffini and Golgi-like endings were rarely found and no Pacini corpuscles were seen. Significantly more free nerve endings (P < 0.001) and blood vessels (P = 0.01) were observed in the subtalar joint capsule than in the superficial part of the fat pad at the IER. The deep part of the fat pad at the IER had significantly more blood vessels than the superficial part of the fat pad at the IER (P = 0.012). Significantly more blood vessels than free nerve endings were seen in all three groups (P < 0.001). No significant differences in distribution were seen in terms of right or left side, except for free nerve endings in the superficial part of the fat pad at the IER (P = 0.003). A greater number of free nerve endings correlated with a greater number of blood vessels. The presence of sensory nerve endings between individual fat cells supports the hypothesis that the fat pad has a proprioceptive role monitoring changes and that it is a source of pain in sinus tarsi syndrome due to the abundance of free nerve endings.

Keywords: ankle, immunohistochemistry, mechanoreceptors, proprioception, sinus tarsi

Introduction

Adipose tissues are organized to form a large organ with discrete anatomy, specific vascular and nerve supplies, complex cytology, and high physiological plasticity. The composition of the adipose organ varies in different anatomical locations and under different conditions, contributing to many crucial survival needs: thermogenesis, lactation, immune responses and metabolism processes. Two main types of adipocytes are distinguished by morphology, white and brown adipocytes (Cinti, 2012), which are quite different in their physiology. White adipocytes store energy, whereas brown adipocytes burn energy for thermogenesis (Cinti, 2012). Three different types of white adipose tissue (WAT) are differentiated on the basis of structural and ultrastructural features: deposit, structural, and fibrous WAT (Sbarbati et al. 2010). Deposit WAT is found in the periumbilical area, the cells are tightly packed, linked with a weak net of isolated collagen fibres, and few blood vessels are present. Structural WAT is composed of more stromal fat and is located in limited adipose areas, such as in armpits, inner faces of the knees, thighs, pectoral and mammary areas and hips. It is a non-lobular adipose tissue, wrapped by a basket of collagen fibres. Fibrous WAT has a pronounced fibrous component and is located in areas of high mechanical load (Sbarbati et al. 2010). There is an indication that WAT is innervated (Bartness & Bamshad, 1998). Different functions of adipose tissue in periarticular regions have been proposed, including facilitating movement between ligament and bone, dissipating stress concentration at attachment sites, and sensory perception (Benjamin et al. 2004).

The sinus tarsi is an anatomical space bounded by the talus and calcaneus, the talocalcaneonavicular joint anteriorly and the posterior facet of the subtalar joint. The sinus tarsi continues medially with the canalis tarsi and contains the three roots of the inferior extensor retinaculum (IER), the talocalcaneal oblique as well as the canalis tarsi ligaments, the subtalar joint capsule, fat and blood vessels (Schmidt, 1978).

The subtalar joint capsule provides not only passive stability by limiting movements and sealing joint space, but is also suggested to be involved in the sensorimotor control of joint movements (Ralphs & Benjamin, 1994). Recently, the innervation of sinus tarsi ligaments has been studied with immunohistochemical markers (Rein et al. 2013a,2013b). However, there are no exact innervation studies of the periarticular structures around the sinus tarsi. Fat pads can be a significant source of joint pain, which is referred from its sensory innervation (Biedert & Sanchis-Alfonso, 2002; Benjamin et al. 2004; Shaw et al. 2007). This raises the hypothesis that sensory nerve endings in fat tissue and subtalar joint capsule could contribute to sinus tarsi syndrome (Kjaersgaard-Andersen et al. 1989; Zwipp et al. 1991; Pisani et al. 2005).

This study set out to determine whether the superficial and deep parts of the fat pad at the IER as well as the subtalar sinus tarsi capsule have features that enable proprioceptive functions. The aim of this study was to analyse the pattern and types of mechanoreceptors of the different sinus tarsi structures using designated immunohistochemical markers, as well as the overall vascularity.

Materials and methods

Cadaver specimens

All protocols in this study were approved by the local ethics committee review board. Thirteen feet (six left and seven right feet) from seven subjects (three women and four men) with a mean age of 58 ± 16 years (range: 36–86 years) were included in this study. The cadavers were refrigated (4 °C) pending capsule and fat pad harvest, and the mean time between death and harvest was 3.3 ± 2.1 days (range: 1–7 days). All feet were assessed macroscopically and showed no signs of injury or structural abnormality.

A lateral semicircular skin incision was made over the ankle. The superficial part of the fat pad at the IER was resected. Furthermore the subtalar joint capsule in the sinus tarsi and the deep part of the fat pad at the IER were dissected.

Immunohistochemistry

Specimens were immediately fixed in 4% buffered formaldehyde solution (pH 7.4) for 24 h at 4 °C, decalcified with diaminoethanetetraacetic acid (EDTA) and embedded in paraffin. Sections of 4 μm were cut and mounted on silane-coated slides for conventional staining and immunohistochemistry. All specimens were cut at five levels, with a 50-μm cutting interval between each level. The immunohistochemical protocol has been described in detail previously (Hagert et al. 2004; Rein et al. 2013a). The antibodies are listed in Table 1.

Table 1.

Immunohistochemical antibodies.

Antibody Source Dilution Characteristics
S100 Code: Z 0311; DakoCytomation, Glostrup, Denmark 1 : 500 Polyclonal antisera against S100
p75 Code: N-3908; Sigma, St. Louis, MO, USA 1 : 50 Polyclonal rabbit antisera against p75
PGP 9.5 Code: 7863-0504; AbD Serotec, Düsseldorf, Germany 1 : 300 Polyclonal rabbit antisera against PGP 9.5
sm-actin Code: M 0851; DakoCytomation 1 : 750 Monoclonal mous anti-human smooth muscle-actin 1A4
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Details of the immunohistochemical antibodies are shown. S100,  S-100 protein; p75,  nerve growth factor receptor p75; PGP 9.5,  protein gene product 9.5; sm-actin,  smooth muscle-actin.

Morphological analysis and cell counting

Histological examination of the stained tissue sections was performed using a Leica light microscope (Leitz DMRBE, Wetzlar, Germany) with a Leica camera (Leica DC 300; Leica Microsystems CMS GmbH, Heerbrugg, Switzerland).

Haematoxylin-eosin (H&E)-and Elastica van Gieson (EvG)-stained slices were used for determination of tissue morphology. Mechanoreceptors were analysed according to the classification of Freeman & Wyke (1967), modified by Hagert (2008). Ruffini, Pacini, Golgi-like and free nerve endings as well as unclassifiable corpuscles were counted in the S100, p75 and PGP 9.5 stainings in all five levels with respect to total cell count per section at an original magnification of 400× (high-power field). A standard 10 × 10 grid was used for determination of mechanoreceptor size. Sensory corpuscles that could not be clearly defined as Ruffini, Pacini, Golgi-like corpuscles or as nerve fascicles were deemed unclassifiable according to Hagert (2008).

Blood vessels were counted at two representative levels in the sm-actin stain, identified by specific immunoreactivity of sm-actin of the smooth muscle cells in the wall of the vessels. All specimens were examined blind for cell counts.

Visual fields were counted at an original magnification of ×100 to calculate the size of the analysed slice, which is reported in square centimetres.

Statistical analysis

Means ± standard deviations have been used for descriptive statistics throughout the article. The values represent the number of corpuscles per cm2.

The first purpose was to analyse the general distribution of sensory nerve endings between the three specimen types. The Kolmogorov–Smirnov test was performed to investigate data distribution. As all groups were found to not have normal distributions, the subsequent statistical analysis was performed using the Kruskal–Wallis test followed by the Mann–Whitney test with post hoc Bonferroni adjustment, with a final level of significance of P ≤ 0.017, due to three tests of significance between the three specimen types with the Bonferroni adjustment.

The second purpose was to compare the quantity of the different types of mechanoreceptors within each group. The Friedman test, followed by the Wilcoxon test with post hoc Bonferroni adjustments, was performed. The final level of significance was P ≤ 0.005, as 10 tests of significance between the five mechanoreceptor groups were performed with the Bonferroni adjustment.

The third purpose was to compare the right-and left-sided distribution of the mechanoreceptors of each specimen type, using the Mann–Whitney test. The level of significance was considered high with P ≤ 0.05.

The fourth purpose was to test correlations between free nerve endings and blood vessels. Correlation analysis was performed with Spearman's rho coefficient with a two-sided significance level of P ≤ 0.05. All 39 specimens were examined together for the correlation analysis.

Results

General observations

Adipose tissue of the superficial and deep part of the fat pad at the IER showed a polymorphic structure. No strictly ordered lobular morphology of the fat pads was seen. Numerous bundles of coarse branched connective tissue were observed (Fig. 1), which had a multidirectional course, containing, besides collagen, a high proportion of elastic fibres, verified in the EvG staining (Fig. 1). Both types of fat pads had a pronounced vascularization; larger blood vessels were embedded in the connective tissue septa but smaller blood vessels passed through the fat tissue directly (Fig. 1). All analysed fat tissue specimen were classified in structural WAT according to Sbarbati et al. (2010).

Figure 1.

Figure 1

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A deep part of the fat pad at the IER is seen in the H&E (a, b, c), and EvG stainings (d, e, f) as well as with immunoreactivity for S100 (g, h, i), and sm-actin (j, k, l). Numerous coarse branched collagenous tissue bundles are observed in the H&E staining. Polyhexagonale fat cells are seen, most of them have the typical marginal nucleus (arrow in c and l). Abundant elastic fibers (arrows in d, e, f) are located in the collagen fibrers, seen in the EvG staining. Numerous free nerve endings are noted in higher magnifications (arrow in i), which are immunoreactive for S100. The marked vascularity of adipose tissue in the sinus tarsi is detected by immunoreactivity for sm-actin (j, k, l). Larger vessels lying in the collagen-elastic fiber bundles, whereas smaller vessels are also found between adipocytes (arrows in k and i). Original magnification x25 (a, d, g, j), x100 (b, e, h, k) and ×200 (c, f, i, l).

The subtalar joint capsule consisted of an outer layer of dense fibrous connective tissue, lined with synovium and made of collagen bundles (Fig. 2). An abundance of blood vessels as well as elastic fibres were observed in both layers of the capsule. Free nerve endings were seen particularly in the subsynovial layer of the capsule tissue. A few Ruffini endings and Golgi-like endings were found only in the outer layer of fibrous tissue.

Figure 2.

Figure 2

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Subtalar joint capsule of the sinus tarsi as stained for H&E (a–c), EvG (d–f), S100 (g–i), and sm-actin (j–l). The two-layer structure of the joint capsule, including the synovial (b,e,h,k, arrows in b) and fibrous layers (c,f,i,l), is already visible in the overview magnification (a,d,g,j). The fibrous layer consists of compactly arranged and wavy aligned collagen bundles (arrows in c) as well as numerous elastic fibres (arrows in d,f). Small elastic fibres are also detected in the subsynovial layer (arrow in e). Free nerve endings are mainly found in the subsynovial layer, showing immunoreactivity for S100 (g, arrow in h). Pronounced vascularization is shown with immunoreactivity for sm-actin in blood vessels (j–l). A dense network of small blood vessels exists in the synovial layer (arrows in k).The fibrous layers contain larger blood vessels (arrows in j). Original magnification ×25 (a,d,g,j) and ×200 (b,c,e,f,h,i,k,l).

Distribution of mechanoreceptors and blood vessels

Free nerve endings were the predominant sensory ending (Fig. 3). Ruffini endings (Fig. 4) and Golgi-like endings (Fig. 5) were rarely observed. No Pacini corpuscles were determined in the investigated specimens in this study.

Figure 3.

Figure 3

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Free nerve endings in the superficial part of the fat pad at the IER is shown as stained with H&E (a), for S100 (b), p75 (c), and PGP 9.5 (d) immunoreactivity. There is an intensive immunoreactivitiy for S100 (arrow in b), p75 (arrow in c) and PGP 9.5 (arrow in d) of the nerve. The nerve (arrow in a) can only be localized due to the anatomical orientation next to blood vessels (*a, b, c, d) in the H&E staining. Original magnification ×200.

Figure 4.

Figure 4

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A Ruffini ending from the deep part of the fat pad at the IER is seen in the H&E staining (a), with S100 (b), p75 (c), and PGP 9.5 immunoreactivity (d). Dendritic terminal nerve endings are clearly delineated with S100, p75 and PGP 9.5 (b-d). The central axon (arrow) of the corpuscle does not show immunoreactivity in the p75 staining (c). Original magnification ×400.

Figure 5.

Figure 5

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A Golgi-like ending in the deep part of the fat pad at the IER is shown as stained with H&E (a), for S100 (b), p75 (c), and PGP 9.5 (d) immunoreactivity. The Golgi-like ending is larger than the Ruffini or Pacini corpuscles. Smaller corpuscles within the Golgi-like endings are seen, each of them containing terminal nerve endings (arrows c). Original magnification ×200.

Significantly more free nerve endings (88.8 ± 71.3 cm2) were found in the joint capsule than in the superficial part of the fat pad at the IER (47.8 ± 31.3 cm2; P < 0.001; Fig. 6). Also, the subtalar joint capsule (393.4 ± 306.5 cm2) had significantly more blood vessels than the superficial part of the fat pad at the IER (210.1 ± 193.8 cm2; P = 0.01; Fig. 6). A significantly larger number of blood vessels than free nerve endings were seen in all three specimen types (P < 0.001; Fig. 6). Significantly more blood vessels were observed in the deep part of the fat pad (373.9 ±269.9 cm2) than in the superficial part of the fat pad at the IER (210.1 ± 193.8 cm2; P = 0.012; Fig. 6).

Figure 6.

Figure 6

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Means ± standard deviation per cm2 for the free nerve endings and blood vessels are shown. The deep part of the fat pad (*) had significantly more blood vessels than the superficial part of the fat pad at the IER (P = 0.012). Significantly more free nerve endings (§P < 0.001) and blood vessels (#P = 0.01) were observed in the joint capsule than in the superficial part of the fat pad at the IER. Significantly more blood vessels (+) than free nerve endings were seen in all three groups (P < 0.001).

Free nerve endings were found significantly more often than Ruffini endings, Pacini corpuscles, Golgi-like endings and unclassifiable corpuscles within each specimen type (P < 0.001, respectively). Significantly more blood vessels than free nerve endings were seen within each group (P < 0.001, respectively; Fig. 6).

No significant differences between the Ruffini endings, Pacini corpuscles, Golgi-like endings and unclassifiable corpuscles were observed between and within each specimen type (Fig. 7).

Figure 7.

Figure 7

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Means ± standard deviation per cm2 of mechanoreceptors around the sinus tarsi are shown. No significant differences between the corpuscles were observed.

Side-related distribution

No significant differences were seen for any sensory nerve endings or blood vessels in the three specimen types between left and right feet, except for free nerve ending in the superficial part of the fat pad at the IER, the right feet having significant more nerve endings (54.9 ± 24.9 cm2) compared with the left feet (39.4 ± 36 cm2; P = 0.003).

Correlation analysis

A greater number of free nerve endings correlated significantly with a greater number of blood vessels (P < 0.0001; r = 0.73; Fig. 8).

Figure 8.

Figure 8

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A higher number of free nerve endings was correlated significantly with a higher number of free nerve endings (P < 0.0001; r = 0.73).

Discussion

Both the superficial and deep parts of the fat pad at the IER had the composition of structural WAT according to Sbarbati et al. (2010). Structural WAT is located in very limited adipose areas, where its function goes beyond the depot itself (Sbarbati et al. 2010). It is widely acknowledged that adipose tissue mixed with fibrous tissue acts as pressure-tolerant material in the palms and soles, dissipating stress, and that fat allows movement between adjacent structures (Benjamin et al. 2004). Morphological aspects of these functions are that the adipose tissue is separated by thin collagen sheaths, which contain a notable number of elastic fibres. Elastic fibres modulate the distensibility of the fat tissue when subjected to compressive stresses and its return to normal resting tensile state, whereas collagen fibres provide rigid constraints that limit overdistension of the fat pad (Kimani, 1984). Therefore, adipose tissue contributes to the viscoelastic properties of supporting limbs and enhances stability during locomotion (Falcon et al. 2011).

A significantly greater number of blood vessels were found in the subtalar joint capsule as well as in the deep part of the fat pad compared with the superficial part of the fat pad at the IER. Interestingly, more blood vessels were observed in the subtalar joint capsule (393.4 ±306.5 cm2) and the deep part of the fat pad at the IER (373.9 ± 269.9 cm2) than in sinus tarsi ligaments (241.6 ± 143.1), as reported recently (Rein et al. 2013a). In addition, a greater number of free nerve endings correlated with a higher number of blood vessels. Therefore, periarticular tissue around the sinus tarsi is important for nutrition, protection, and support of the neurovascular bundles. White adipose tissue is no longer considered an inert tissue mainly devoted to energy storage but is emerging as an active participant in regulating physiologic and pathologic processes, including immunity, inflammation, and proprioception (Fantuzzi, 2005).

Free nerve endings were the predominant mechanoreceptor type seen in the superficial and deep parts of the fat pads at the IER as well as the subtalar joint capsule. This is in accordance with a previous publication, which describes abundant free nerve endings, but also several Ruffini-endings, Pacini corpuscles and Golgi-like endings in fatty and synovial membranes of lateral sinus tarsi tissue in patients with sinus tarsi syndrome. The greatest density of sensory nerve endings was found in the synovial tissue of the sinus tarsi (Akiyama et al. 1999). Similarly, the present study showed the highest amount of free nerve endings in the subtalar joint capsule. Furthermore, recent immunohistochemical studies reported that free nerve endings were the predominant mechanoreceptor in ankle ligaments (Rein et al. 2013a,2013b). In contrast to the results of Akiyama et al. (1999) no Pacini corpuscles were seen in this study, although all specimens were investigated in five levels with designated immunohistochemical markers. One reason for these differences may be that Akiyama et al. (1999) used the gold chloride technique, which impregnates not only nerve tissue but also blood vessels and reticular fibres, thus providing nonspecific imaging of neural elements in tissue (Soule, 1962; Koch et al. 1995; Gómez-Barrena et al. 1999). Based on the results of this study, it may be assumed that the pain of sinus tarsi syndrome originates mainly from nociceptors due to their abundant occurrence in sinus tarsi structures.

Our presented anatomical results are also supported by an electromyographic study, in which a delayed peroneal reaction time (PRT) was found in 18 patients with functional instability of the ankle. A significant shortening of the prolonged PRT in these patients to normal level was observed after injection of an anesthetic blockade into the sinus tarsi, whereas the PRT in healthy controls remained unchanged (Khin Myo et al. 1999). This suggests that irritability of free nerve endings, induced by inflammation at the sinus tarsi, may suppress the activities of gamma motor neurons of peroneal muscles, which in turn might cause the symptoms of functional instability and prolonged PRT (Khin Myo et al. 1999). Therefore, treatment strategies of sinus tarsi syndrome should address nociceptors in the sinus tarsi. One conservative treatment option includes injection of a steroid and local anaesthetic agent into the sinus tarsi. Surgical intervention of sinus tarsi syndrome comprises resection of the deep part of the fat pad at the IER and debridement of the synovia after a capsulotomy of the subtalar joint. The synovial fold at the talus and calcaneus is electrocauterized (Kjaersgaard-Andersen et al. 1989; Zwipp et al. 1991). Denervation of the sinus tarsi by resection of the appropriate branch of the deep peroneal nerve has also been reported in the literature (Dellon & Barrett, 2005). Moreover, arthroscopy of the sinus tarsi can identify further pathologic findings of sinus tarsi syndrome (Frey et al. 1999; Oloff et al. 2001; Lee et al. 2008).

In conclusion, free nerve endings were the predominant receptor type found, but only few Ruffini and Golgi-like endings and no Pacini corpuscles were observed. This suggests a significant source of pain in sinus tarsi syndrome. Joint position sense, mediated by Ruffini endings, and detection of extreme movements, mediated by Golgi-like endings, play a minor proprioceptive role in fat pads and joint capsule in the sinus tarsi.

Acknowledgments

The authors thank the following individuals for their contributions to this article: Ursula Range for statistical support, Dorothea Liebeheim for histological preparation, Thomas Albrecht for photographical work as well as Reinhold Krentscher and Hans-Dieter Tröger for logistical support. The authors declare that they have no competing interests. This study has been financially supported by the Medical Faculty of the Technical University, Dresden, Germany, and the Willi & Partner AG, Wetzikon, Switzerland. The authors have disclosed all financial conflicts of interest that may influence interpretation of this study and/or results.

Authors’ contributions

All authors made substantive intellectual contributions to this study, in conception and design (S.R., H.Z.), acquisition of data (S.R., S.M., A.W.), analysis and interpretation of data (S.R., H.Z., A.W.) and drafting and revising the manuscript critically (S.R., S.M., H.Z., A.W.).

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