Ligamentous structures in human glans penis

Abstract

The corpus spongiosum reportedly occupies a larger proportion of the human glans penis than does the penile body, embedding the end of the corpus cavernosus (CC). However, anatomic descriptions about the fibrous structures of glans penis in the literature cause confusion during dissection and reconstructive surgery. Forty‐five penises of formalin‐embalmed cadavers were dissected sagittally along the course of the distal urethra and observed macroscopically. Dense connective tissues adjacent to the fossa navicularis and spongiosum parts of the glans were cropped, and underwent Masson's trichrome and Verhoeff‐Van‐Gieson staining. Most (55.5%) of the specimens had distinct fibrous bands toward the distal tips of the glans penis, which elongated from the tunica albuginea of the CC. They comprised longitudinal collagen bundles continuous to the outer longitudinal layer of the tunica albuginea covering the CC and were intermingled with sparse elastic fibres. This architecture either did not reach the distal end of the glans penis (35.5% of cases), or was obscure or dispersed in all directions (9.0% of cases). The structural dimorphism and the variations in the ratio of dense connective tissue components of the fibrous skeleton are considered to contribute to the varying degrees of flexibility, distensibility and rigidity of the human glans penis.

Introduction

The male genital organ of mammalians is composed of three erectile cylinders: the bilateral corpus cavernosus (CC) and the underlying corpus spongiosum (CS; Goldstein & Padma‐Nathan, 1990; Hsu et al. 2004; Hsu, 2006). Moulded on top of the tip of the CC is the cap of the glans that continues to CC tissues in the human penis (Shafik et al. 2007; Hsieh et al. 2012; Kureel et al. 2015). When the CC is detached from the CS by blunt dissections, a distal cap of the glans is not easily divided from an apex of the CC due to firm attachments via a fibrous frame (Shafik et al. 2004; Hsu et al. 2005). These connections appear consistently on the distal urethra, but the associated gross and histological structures are not described well in the textbooks and medical illustrations used to guide reconstruction surgeries. An accurate knowledge of the fibrous frame of penile erectile tissues is needed to understand the pathophysiology of the human penis and further refine reconstruction techniques.

The aim of this study was to determine the macroscopic and microscopic morphological features of these unique ligamentous structures around the distal urethra of the human glans penis.

Materials and methods

The glands of 45 penises of formalin‐embalmed cadavers were investigated. The donors had died at an age of 74 ± 11.9 years (rage 47–95 years), before which they had signed documents agreeing to their participation in the body donation program of the medical school and the use of their body for clinical studies. None of the specimens showed signs of hypospadia or penile cancer. The specimens were sagittally and parasagittally dissected parallel to the course of the distal urethra, and the morphology of the fibrous frame was assessed macroscopically (Fig. 1). The specimen ages in the groups were compared using the Kruskal–Wallis H‐test with P < 0.05.

Figure 1.

Gross observations of the glans penis dissected mid‐sagittally. (A) In half of the samples (N = 25), the ligamentous tissues (arrowheads) were laid on the urethra throughout the glans penis. The fibrous bands were discontinuous by the vessels (red arrows) or spongiosum tissues (asterisk). CC, corpus cavernosus; CS, corpus spongiosum; E, external urethral orifice; F, fossa navicularis; yellow arrow, distal urethra. (B) Ligamentous tissues (arrowheads) on the upper wall of the distal urethra not reaching the distal tip of the glans (N = 16). The tunica albuginea and ligamentous tissues in the glans penis appeared darkly pigmented in some specimens (right). (C) Dense connective tissues with undulated or radiating features appeared in the spongiosum parts of the glans penis (N = 4).

Histological specimens were obtained from the longitudinal axis of the glans penis, immersed in 4% phosphate‐buffered formalin (pH 7.4) and processed using routine histological methods. Ten‐micron‐thick longitudinal sections underwent Masson's trichrome staining for dense connective tissues (appearing blue) and Verhoeff‐Van‐Gieson staining to highlight elastic fibres (appearing dark blue). The compositions of collagen and elastic fibres were examined microscopically to identify regional differences in the ligamentous structures of the glans penis (Figs 2, 3, 4).

Figure 2.

Histology of the ligamentous tissues throughout the glandular urethra. The lower image is a magnified view of the boxed area. Distinct fibrous bundles (black arrows) are elongated longitudinally from the outer layers of the tunica albuginea (red arrow) encompassing the apex of the corpus cavernosus (CC).

Figure 3.

Regional distribution of the elastic fibres in the ligamentous tissues of the glans penis. (A) The lower image is a magnified view of the boxed area stained by Verhoeff‐Van‐Gieson. (B) Magnification of a box (B) in (A). A central region of the fibrous band consists of buckling collagen bundles impregnated with a few elastic fibres (arrows). (C) An abundance of elastic fibres with large diameters in the peripheral region of the fibrous band. (D) A high proportion of fine elastic fibres compared with (B) in the distal region of the fibrous bands.

Figure 4.

Connective tissues of the glans penis without ordered fibrous bands macroscopically. (A) Malformation of the tunica albuginea covering the distal tip of the corpus cavernosus (CC) (red arrow). (B) Distributions of buckling small‐diameter collagen bundles despite the absence of distinct ligamentous bands on the distal urethra by gross observation. (C) Dispersed collagen bundles in all directions with space in the distal region of the spongiosum parts of the glans.

Results

Gross observations of the fibrous skeleton of the glans penis

While the bilateral CC ended blindly under cover of the glans penis, the distal elongations of the tunica albuginea surrounding the CC pierced the spongiosum part of the glans penis. The morphology of the blind ends of the CC and their fibrous connection toward the distal cap of the glans exhibited significant interpersonal variations (Fig. 1). Most (55.5%) of the specimens had distinct fibrous bands that elongated from the tunica albuginea of the CC to the external urethral orifice throughout the fossa navicularis. The fibrous bands firmly attached to the urethral wall with a constant thickness, or undulated while interrupted by the arteries of carvenospongiosum shunts (Diallo et al. 2013) and spongiosum tissues. This architecture did not reach the distal tip of the glans penis when it had a blunt end or radial shape (35.5% of cases). The remaining specimens were supported by obscure networks of fibrous tissues in all directions and a thin tunica albuginea of the CC (9.0% of cases). The morphology in each group was not affected by the specimen age.

Histological patterns of collagen and elastic fibres

The tunica albuginea of the CC was composed of two layers, each of which comprised two–nine sublayers of collagen bundles (Hsu et al. 1994; Shafik et al. 2006). The Masson's trichrome blue staining of the thick collagen bundles allowed them to be distinguished from surrounding structures, while fine elastic fibres were detected in dense connective tissue by their blue‐black colour from Verhoeff‐Van‐Gieson staining. Distinct ligamentous structures around the glandular urethra were composed mainly of thick collagen bundles elongated from outer longitudinal layers of the tunica albuginea covering the CC (Fig. 2). The spatial arrangement of the elastic fibres varied according to the relative locations of the fibrous frame of the glans penis: while the medial region of the ligamentous tissue consisted of excessive collagen impregnated with sparse elastic fibres, those of the peripheral regions were interwoven by dense elastic networks comprising elastic fibrils of varying diameters (Fig. 3).

Despite the absence of ligamentous structures in Fig. 1c, a longitudinal arrangement of a few collagen bundles was observable in the nearby sinusoidal spaces. Fibrous glans tissue with a disarranged morphology resulted in the tunica albuginea of the CC being malformed with insufficient thickness (Fig. 4).

Discussion

It has been argued that the morphology of male intromittent organs has been subject to more‐rapid evolutionary divergence than any other structure in the animal kingdom (Kahn et al. 2010; Simmons & Firman, 2013; Brindle & Opie, 2016). The baculum (also called the os penis) is an extraskeletal bone with a low mineral density that is derived from connective tissue and is found within the distal end of certain mammals, including many primates, rodents, bats, carnivores and some insectivores (Sharir et al. 2011; Stockley, 2012). The diversity of the baculum morphology to obtain the required mechanical and stimulatory fit to female genitalia stems from the sexual selection hypothesis implying that the genital morphology influences the success rate of male fertilization (Ramm et al. 2010; Herdina et al. 2015; Schultz et al. 2016).

Despite some reported speculation relating to an upright posture and changing mating strategies, it is unknown why the baculum was lost within the hominid lineage (Ramm, 2007; Stockley, 2012). Although there is no baculum in the human penis, an equivalent ligamentous structure is arranged centrally along the distal urethra as a supporting trunk for the glans penis (Hsu et al. 2005; Hsu, 2006). The distal tips of the CC are capped by the glans penis, which is itself a continuation of the CS that surrounds the urethra (Yiee & Baskin, 2010). The fibroelastic properties of this CS are more complicated than thought previously. In contrast to the CC, the trabecular smooth muscles are rare and parasinusoidal fibroelastic shells are abundant in the spongiosum part of the CS (data not shown). Distinct ligamentous structures around the glandular urethra visible in gross observations were correlated with the histological composition of thick collagen bundles. The fibrous bands in the human glans penis are composed of collagen bundles elongated from outer longitudinal layers of the tunica albuginea covering the CC. This characteristic does not appear to result from aging, because the proportion of collagen is reportedly greater in the CS than in the CC throughout the foetal period (Gallo et al. 2014).

The integrity of the fibroelastic tissue in the glans penis could be essential to facilitate reproductive strategies, and not only as the principal source of afferent information for the induction and maintenance of sexual responses (Yang & Bradley, 1999). While the main function of collagen fibres is to provide tensile strength, the elastic fibres provide stretchability and flexibility (Kazlouskaya et al. 2013). The spatial arrangement of the elastic fibres varies according to the region of the fibrous frame of the glans penis (Figs 3 and 5). The suspected function of the spatial arrangement of ligamentous tissues with the central integration of collagen bundles and peripheral infiltration of elastic components is to avoid excessive tissue stretching that would lead to severe damage of external genitalia, while also providing firm support for the glans architecture during thrusting (Stockley, 2012). Furthermore, ligamentous tissues in the glans penis are speculated to firmly support the distal urethra during the surge pressure related to ejaculation, and to prevent overstretching or compression of the channel while maintaining an adequate flexural stiffness (Hsieh et al. 2012). In addition to morphomechanical studies of external genitalia, future experiments should attempt to shed light on the interspecific divergence of the genital evolution of mammals, which has the by‐product effect of the selection of other traits (Birkhead & Pizzari, 2002).

Figure 5.

Schematics of ligamentous tissues of the human glans penis. (A) A firm trunk with buckling collagen bundles (red striped areas) supports the maintenance of shape and force during coitus. Flexibility during thrusting due to peripheral arrangement of elastic fibres (purple) could provide the required flexural stiffness. (B) Dense connective tissues consisting of concentrated collagen bundles formed compact trunks in the central glans (91% of cases) or were dispersed as sparse bundles penetrating the sinusoidal space (9% of cases). Red networks in the glans and the penile shafts indicate the fibrous frame consisting of collagen bundles. F, fossa navicularis.

Quantitative and qualitative alterations in the collagen and elastic fibres due to aging or inflammation may render adequate sustainment. The degenerative and atrophic changes in collagen and elastic fibres increase with age, and are significantly smaller in impotent than potent patients (Akkus et al. 1997; Shafik et al. 2007; Andrade et al. 2012). Furthermore, many studies have delineated the significance of structural alterations such as the calcification or ossification in fibroelastic components of the tunica albuginea in common penile diseases (Frank et al. 1989; Sarma & Weilbaecher, 1990; Brock et al. 1997; Piao et al. 2008; Levine et al. 2013). The development of new surgical techniques of glans preservation that consider the core structures of the glans penis that have delineated in the present study could contribute to tension‐free reconstruction and the maintenance of superior penile function (Yang et al. 2014; Kureel et al. 2015; Özbey & Kumbasar, 2017).

Approximately 10% of the human glans specimens in the present study comprised scattered fibroelastic trabeculae (Fig. 5). However, one limitation of such investigation is the difficulty of differentiating between atrophic changes of penile fibroskeletons due to aging (Pingel et al. 2014) and innate morphological differences among individuals. A systematic epidemiological survey is needed to determine whether this results from congenital morphology, tendinopathic regions or degenerative signs. Nevertheless, the morphological diversity of a firm trunk is suspected to contribute to the varying degrees of flexibility, distensibility and rigidity of the human glans penis (Shafik et al. 2006). The findings of the present morphological investigation indicate that the physiological function of the glandular fibrous frame needs to be explored in detail.

Conclusions

A central ligamentous structure penetrated the glans penis by the course of the fossa navicularis in 91% of the individuals in this study. This structure consisted of excessive amounts of collagen impregnating similar to the tunica albuginea of the CC, and the ratio of elastic to collagen fibres increased toward peripheral regions. Fibroelastic components dispersed to the parasinusoidal spaces of the glans penis in 9% of the present cases. The unique fibrous frame of erectile tissues is considered to provide the human penis with its required flexural stiffness.

Authors’ contributions

S.H.L. designed and conceived the study, acquired the data, analysed and interpreted the data, drafted and illustrated the article. T.J.H. acquired the data. K.S.K. critically revised the article, reviewed the submitted version of the manuscript, and supervised the study. W.C.S. was involved in administrative/technical/material support, critically revised the article, and reviewed the submitted version of the manuscript.

Ethics statement

The cadavers came from people who had given their informed consent to use their bodies.