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THE ADHERENCE BETWEEN THE FREE END OFTHE BOVINE PENIS AND ITS SHEATH

BY R. R. ASHDOWNDepartment of Veterinary Anatomy, The University, Bristol 8

INTRODUCTION

The free end of the penis of the ox is firmly adherent to its sheath at the time ofbirth (Colucci, 1872). The embryological development of the penis in the domesti-cated ruminants has been described in detail by Bohm (1905) and Broman (1947),but they were principally concerned with the early stages during which the penisis formed from the genital tubercle and the primitive penis pendulus is transformedinto the definitive penis appositus. Little has been written about the later changesthat take place in the penis and sheath. As a basis for further studies on the post-natal development of these organs in the bull I have therefore investigated theanatomical relationship between penis and sheath in young calves and foetuses.

MATERIALS AND METHODS

Histological material consisting of the whole of the free end of the penis with itsadherent sheath was taken from five calves aged between 1 and 3 weeks and tenfoetuses (135 mm., 23, 26, 36, 37, 43 5, 49, 58, 70, 73 cm. C.R. length). The specimenswere fixed in formal saline, Bouin's fluid or Heidenhain's Susa; embedded for trans-verse sectioning in paraffin wax; serially sectioned at thicknesses of 10, 15, or 20,u;and mounted at intervals of 100,#. In the three smallest foetuses and one calf allsections were mounted. Sections were stained with haematoxylin and eosin, orhaematoxylin and van Gieson's stain.

RESULTS

The penis of the ox lies beneath the skin of the ventral body wall and its apex isenclosed by the penile portion of the sheath. The orifice of the sheath lies justcaudal to the umbilicus. The lumen of the pre-penile portion of the sheath is patentthroughout foetal life, but the wall of the penile portion is adherent to the free end ofthe penis during foetal and early postnatal life. Two distinct tissues are involved inthis adherence. Over the surface of the penis a thin lamella of ectodermal cells isadherent to the penis and to the sheath. This is the 'glandar lamella' of Bohm andthe 'glando-preputial invagination' of Retterer. Near the urethra the ectodermallamella is incomplete; its edges overlap without joining and a frenulum of connectivetissue joins the penis to the sheath. Text-fig. 1 shows the arrangement of thesetissues in the young calf and Text-fig. 2 shows this for a foetus of 23 cm. C.R. length.In the following account the tissues are described in the calf and then compared withthe foetal material.

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(1) The ectodermal lamellaIn these specimens the lamella was not intact at the urethral orifice; a rim 50-

lOOts in height was more or less free from the sheath and small cavities extended intothe lamella alongside the urethral process to a depth of 1 mm. Immediately behindthe urethral orifice the lamella completely encloses the apical one-sixth of the penisand in transverse section it is a solid, uninterrupted ring of tissue (Text-fig. 1 A-C).However, over the remaining length of the free end the ventral borders meet oroverlap leaving a frenulum of varying shape and size between them. Over most ofthe free end the lamella is an almost complete circle in transverse section (Text-fig. 1D-G), but at the base of the free end it is semicircular (Text-fig. 1 H).

Over-all, the lamella is 130-150/t thick: at the apex of the penis it is irregular incross-sectional shape and its thickness may exceed 500,s, while at the base of the freeend, in the dorsal diverticulum, it decreases to 80-100u. The ventral sector of thelamella is somewhat thicker than the dorsal sector and is often corrugated.The histological structure of the ectodermal lamella is shown in PI. 1, figs. 1-4.

It comprises from 5 to 40 layers of cells; over most of its extent it is 10-12 cellsthick. It can be divided into three distinct zones (PI. 1, fig. 3).The outer zone (stratum germinativum of the penile sheath) comprises 1-3 layers

of columnar cells resting upon an eosinophilic basement membrane.The inner zone (stratum germinativum of the penile epithelium) is similar in

structure to the outer zone. Where the frenulum is thin the cells of the apposedgerminal zones become cuboidal and merge with the middle zone (PI. 1, fig. 1).The middle zone is a mass of cells joining the inner and outer zones. The nuclei stain

less intensely than those of the germinal zones. Keratinization is found in the middlezone of the lamella in the young bull calf. Generally it is concentrically developedfrom small balls of prickle cells, resulting in the formation of epithelial pearls.Longitudinal keratinization is less common. Where keratinization occurs there isa tendency for the cells of the middle zone to clump together, forming cigar-shaped basophilic masses of four to twelve nuclei. These 'clumps' are often arrangedirregularly around the periphery of the epithelial pearls (PI. 1, fig. 4) and occuronly at the sites of keratinization. In these calves keratinization was almost entirelyrestricted to apical levels. The thick middle zone of the lamella around the urethralprocess was usually riddled with epithelial pearls (PI. 1, fig. 2) and pearls oftenoccurred in the arms of the lamella bordering the frenulum. Inner and outer zonesappear not to be affected by the keratinization except where large epithelial pearlsbulge the outer zone into the tissues of the sheath.

(2) The frenulumThe frenulum extends over the basal five-sixths of the free end of the penis. Its

shape, as seen on transverse section, varies at different levels and four distinct seg-ments can be distinguished:

(a) An apical segment where the left arm of the lamella overlaps the right arm andis bent back on itself so that the inner zones of the right and leftarms are apposed andthe frenulum is oblique (Text-fig. ID).

(b) A transitional segment where either the two arms do not overlap and the

201

202 R. R. Ashdonfrenulum is vertical or one or both arms are forked and by their overlapping de-limit a forked frenulum (Text-fig. 1E).

(c) A basal segment where the overlapping is reversed: the right arm overlaps theleft, its outer zone lies apposed to the inner zone of the left arm, and the frenulum isoblique (Text-fig. IF).

(d) Where the dorsal diverticulum of the sheath extends over the base of the freeend the frenulum becomes wider, passing dorsally and caudally along the caudaledge of the sheath at its point of reflexion (Text-fig. 1 G, H).The relative lengths of these segments vary between specimens. Apical and basal

segments both occupy about one-third to one-quarter, the transitional segmentone-sixth, and the dorsal sac of the sheath one-tenth, of the total length of the freeend. The transitional segment occurs near the base of the terminal swelling.The frenulum is a thin band of connective tissue, predominantly collagenous. It

is irregular in shape and size; in a transverse section its minimum width is usually20-30/s. However, in two of these calves the frenulum was considerably wider for3-4 mm. of the apical segment; the minimum width was in some sections 300,u. Inboth cases a vein passed through the frenulum at this point forming an anastomosisbetween the veins of the corpus cavernosum urethrae and the sheath.

(3) The foetal ectodermal lamellaIn the smallest foetus (135 mm.) the transformation of the penis pendulus into a

penis appositus had only just been completed. At the apex of the penis the epitheliaof penis and sheath were separate, but over the basal two-thirds of the free end theywere joined, forming an ectodermal lamella. This was very thick in parts, and not soclearly divided into zones as in the calves, though over the apex of the free end thecells of the inner zone were columnar and very distinctive. These cells were similar inthe 23 and 26 cm. foetuses. In all but the two largest foetuses the urethral processlay close to the ventral wall of the sheath and ventrally the lamella was very thin(Text-fig. 2A).

Keratinization was seen in the ectodermal lamellae of all these foetuses exceptthe 135 mm. specimen. Epithelial pearls in the 23 cm. foetus were small and in-frequent; in the largest foetuses (70, 73 cm.) they were less well developed than inthe born calves and were mainly found alongside the urethral process and thefrenulum. Nuclear 'clumps' were infrequent.

(4) The foetalfrenulumIn the 135 mm. foetus there was no overlapping of the arms of the lamella; the

frenulum was vertical throughout its length and very wide near the apex of thepenis. In the other foetuses the shape of the frenulum varied at different levels in thesame way as in the young calves. Overlapping of the arms of the lamella was mostmarked in the largest foetuses. In many places the arms of the lamella came veryclose together, and the frenulum was reduced to a single layer of connective tissuecells. Over a length of 500/s the frenulum of the 49 cm. calf was exceptionally wide,reaching a minimum width of 130/s. A large vein, anastomosing between the veinsof the corpus cavernosum urethrae and those of the sheath, traversed the frenulumat this point.

The free end of the bovine penis and its sheath 203

DISCUSSION

In general, this examination of the penis and sheath of foetal and young calves agreeswith the descriptions of embryological development of the external genitalia ofruminants given by Retterer (1890, 1915) and Bohm (1905).During the first half of pregnancy the ectodermal lamella shows evidence of the

keratinization that eventually splits it into two epithelial surfaces. These cell-changes are very similar to those described in the human lamella by Stieve (1930)and Deibert (1933), but these authors do not describe the nuclear 'clumping' that isso noticeable in the lamella of the young calf. Keratinization is well established atthe tip of the penis in the calf shortly after birth, but there is no macroscopicalseparation at this stage and the penis does not become completely free until the bullis nearly one year old (Ashdown, 1959). It has been shown in many mammals thatkeratinization of the ectodermal lamella is controlled by testicular hormone(Wiesner, 1934; Raynaud & Lacassagne, 1937; Lyons, Berlin & Friedlander, 1942;Wells & Lund, 1947) and this is almost certainly so in the ruminants (Retterer &Neuville, 1916; Wiggins & Terrill, 1953). The keratinization of the lamella in thesefoetuses seems indicative of androgenic stimulation during the second half of preg-nancy.During separation of the bovine penis from its sheath the frenulum ruptures;

fragments of tissue remain, however, forming the raphe on the penis and sheath ofthe adult bull. Fleischmann (1907) and Bohm (1905) both believed that the frenulumof the domesticated ruminants is obliterated before birth by the active growth ofthe ectodermal lamella. Retterer (1890) agreed with this, but later (1915) stated thatthe obliteration is not completed till after birth. My material shows clearly that thefrenulum of the ox persists into postnatal life. However, the progressive over-lapping shown by the arms of the lamella during the second half of pregnancysuggests some active growth of the cells of the lamella and seems to support theview of Fleischmann, Bohm and Retterer on the dynamic role of ectodermal cells indevelopment of this region. The early and extensive appearance of keratinizationalong the edges of the lamella abutting the frenulum suggests the possibility thatthis too may play some part in rupturing the thin band ofconnective tissue. Increasedwidth of the frenulum at those places where a traversing blood vessel occurs could,perhaps, affect the process of frenular rupture in some young bulls.

SUMMARY

Penis and sheath have been examined in young calves up to 3 weeks of age and infoetuses ranging in size from 135 mm. to 73 cm. C.R. length. In these specimens thepenis was united to the penile sheath by a lamella of ectodermal cells and a frenulumof connective tissue: these structures are described. Keratinization, which separatespenis from sheath in later life, was proceeding in the ectodermal lamella of eachspecimen except the smallest foetus.

Most of this work was done during my tenure of an A.R.C. Research Studentship,under the supervision of Prof. C. W. Ottaway. Dr E. H. Batten gave me muchadvice in the preparation of this paper and took the photomicrographs. Miss P.Morgan helped me with the histological preparations.

204 R. R. Ashdown

REFERENCESASHDOWN, R. R. (1959). J. agric. Sci. (in the Press).BROM, J. (1905). Die ausseren Genitalien des Schafes. Morph. Jb. 34, 248-320.BROMAN, I. (1947). tber die Entstehung und sekundare Verschiebung der ausseren Geschlecht-

steile bei Wiederkauern. Acta Anat. 3, 15-54.COLUccM, V. (1872). Alcune osservazioni sulla fimosi congenita dei neonati della specie umana.

Rivista Clinica di Bologna, pp. 80-84.DEIBERT, G. A. (1933). The separation of the prepuce in the human penis. Anat. Rec. 57, 387-399.FLEISCHMANN, A. (1907). Die Stilcharaktere am Urodaum und Phallus. Morph. Jb. 36, 570-601.LyoNs, W. R., BERLIN, I. & FRIEDLANDER, S. (1942). Cornification of balano-preputial epithelium

in normal rats and in castrated rats treated with testosterone propionate. Endocrinology, 31,659-663.

RAYNAUD, A. & LACASSAGNE, A. (1937). Influence de l'hormone mile et de l'hormone femelle surla structure histologique du penis de la souris. C.R. Soc. Biol., Paris, 126, 868-871.

RETrERER, E. (1890). Du developpement du fourreau et de la partie libre de la verge des mammi-feres quadrupedes. C.R. Soc. Biol., Paris, 42, 551-554.

RETTERER, E. (1915). Developpement et histogenese comparee des organes genitaux externes.J. Urol. med. Chir. 6, 327-344.

RETTERER, E. & NEUVILLE, H. (1916). Adherence, chez le bceuf, du gland au prepuce ou fourreau.C.R. Soc. Biol., Paris, 79, 1110.

STIEVE, H. (1930). 'Mannliche Genitalorgane'. In Handbuch der mikroskopischen Anatomie desMenschen, Band 7 (2), ed. W. von Mollendorf. Berlin: Springer.

WELLS, L. J. & LUND, C. J. (1947). Effects of steroid hormones upon the developmental separationof the prepuce from the glans penis. J. clin. Endocrin. 7, 192-200.

WIESNER, B. P. (1934). The post-natal development of the genital organs in the albino rat. J.Obstet. Gynaec., Brit. Emp. 41, 867-922.

WIGGINS, E. L. & TERRILL, C. E. (1953). Variation in penis development in ram lambs. J. Anim.Sci. 12, 524-535.

EXPLANATION OF PLATE

Fig. 1. Transverse section through penis and sheath of a young bull calf, passing through theapical segment of the frenulum. (Formal saline; 10,u; H. &E.)The frenulum is thin and oblique.Where the ectodermal lamella borders the frenulum the apposed inner zones are almostindistinguishable from the middle zones.

Fig. 2. Transverse section through urethral process and sheath of a young bull calf showingexten-sive keratinization of the ectodermal lamella. (Bouin; 1041; H. & E.)

Fig. 3. A higher power view of a section adjacent to that of fig. 2, showing the structure of theectodermal lamella. The columnar cells of the outer (OZ) and inner (IZ) zones have intenselystaining nuclei lying at right angles to the basement membranes. The nuclei of the middle zone(MZ) stain less intensely. At this point three epithelial pearls lie in the middle zone.

Fig. 4. A higher power view of a field adjacent to that of fig. 3, showing two large epithelial pearls.In the centre of each is a cellular eosinophilic mass. The surrounding cells are swollen, withfaintly staining cytoplasm, eosinophilic granules and pycnotic nuclei. Arrows indicate someof the places where nuclei have clumped together forming characteristic basophilic massesaround the periphery of the epithelial pearls.

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