ANNACS OF ANATOMY

Morphological characterization of the female prostate

(Skene's gland or paraurethral gland)
of Lagostomus maximus maximus
Mirta A. Fl ami ni 1, Cl audi o G. Barbei t o a'2, Eduardo J. Gi me no 2 and
Enri que L. Portiausky 2
1 Department of Histology and Embryology and 2 Institute of Pathology,
School of Veterinary Sciences, National University of La Plata, R O. Box 2 96,
1900 La Plata, Argentina
Summary. The Skene' s (parauret hral ) gland is t he histolo-
gic homol ogue to the mal e prostate. Much experi ment al
work has been done on women and on various rodents.
In this study we describe for t he first time t he anatomical
and histological characteristics of t he parauret hral gland
in t he plain viscacha (Lagostomus maximus maximus).
This gland is f or med by t ubul oal veol ar adenomers sur-
r ounded by connect i ve tissue and smoot h muscle fibers.
The adenomers are lined by cuboidal or col umnar epithe-
lium. In t he l umen of t he adenomers, PAS positive secre-
tions coul d be det ect ed. The conduits are lined by
bi-stratified epithelium. In some aspects this gland is simi-
lar t o t hat of ot her mammals.
Key words: Parauret hral gland - Skene' s gland - Femal e
Prost at e - Lagostomus rnaximus maximus - Histricog-
nathi - Mor phomet r y
I nt r oduc t i on
In 1672, de Gr aaf for t he first t i me descri bed t he presence
of a gland l ocat ed around a woman' s uret hra, which be-
came known as t he "f emal e pr ost at e" due to its similarity
with t he masculine prost at e (de Gr aaf 1672). In 1853,
Vi rchow descri bed t he presence of prostatic concretions
as "amyl aceous bodi es" present in this femal e gland
(Virchow 1853). Years later, Al exander Skene published
a work describing t he presence of two glands closely re-
l at ed t o t he ur et hr a (Skene 1880). Ther e onwards, this or-
Correspondence to: M. A. Flamini
E-mail: aflamini@fcv.unlp.edu.ar
gan became known as Skene' s gland (Zavia~i~ and Abl i n
2000). Fur t her studies (Zavia~i6 1999) detailed the anato-
my and the histological st ruct ure of bot h t he ducts and
the characteristics of t he glandular secretion.
For a long time this gland was consi dered to be a vesti-
gial organ wi t hout much functional i mport ance for the
woman. It possesses a microscopic st ruct ure similar to the
masculine prostate, presenting numerous ducts, adeno-
mers and a rich st roma of smoot h muscular tissue (Za-
via~i~ et al. 2000). The presence of an acidophilic
secret i on inside t he adenomers and ducts, which has been
studied with enzymat i c labeling techniques and i mmuno-
histochemistry, was also descri bed (Tepper et al. 1984; Za-
via~i~ 1985, 1997; Zavia~i~ and Abl i n 2000). These studies
showed that a mar ked enzymat i c activity exists in t he fe-
male prost at i c gland and t hat its cells pr oduce an exo-
crine and neuro-endocri ne secretion, produci ng a "femal e
ej acul at i on" (Zavia~i~ 1993).
Not only have structural and physiological descriptions
poi nt to this gland, but di fferent pathological alterations
have also been described; such as glandular hyperplasia
(Folsom and O' Br i an 1943), adenocarci nomas ( Dodson
1994; Zavia~i~ et al. 1993; Sl oboda et al. 1998), cysts (Ishi-
gooka et al. 1995; Romer o P6rez et al. 1999) and calculi
i nduced by Ureaplasma urealyticum (Gel l man and Der-
shewitz 1986).
The presence of this gland is not const ant in t he differ-
ent animal species but has been descri bed in some insecti-
vorous species (Grass6 1969) and in di fferent rodents:
Rattus rattus (Shehat a 1972), Avicantis nUoticus, Meriones
lybicus (Shehat a 1975), Rattus norvegicus (Shehat a 1980),
Mastornys erytholeucus (Ichihara 1976), Paraomys (Mast-
omys) natalensis (Smith et al. 1978; Gross and Di Di o
1987).
Ann Anat (2002) 184:341-345
Urban & Fischer Verlag
http:llwww.urbanfischer.deljournalslannanat
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Fig. 1. Anatomical localization of paraurethral gland (PG). Two PG glands are surrounding the urethra (U). Vagina (V) and urinary
bladder (UB) are also observed. Bar represents 0.3 cm.
Fig. 2. Section of Lagostomus maxirnus maximus parauretral gland (PG) and its two ducts (D) entering the urethra (U). HE. Bar re-
presents 400 pm,
Fig. 3. Section of the paraurethral gland showing lobular aspect. HE, 40.
Fig. 4. Section of the paraurethral gland showing smooth muscle fibers (arrows). CF = connective fibers. Massons's Trichrome, 40.
342
The plains vi scacha (Lagost omus maxi mus maximus), is
a ma mma l bel ongi ng to t he or der Rodentia, sub- or der
Histricognathi, fami l y Chinchillidae. They i nhabi t t he
fields of Ar gent i na, f or mi ng colonies in deep caves called
vi scacha' s burrows. The light governs t hei r habits: duri ng
t he day t hey r emai n in t he caves and l eave t hei r burrows
in t he eveni ng to carry out t hei r out door activities. Ther e
is a mar ked size and wei ght di fference bet ween t he mal es
and f emal es of t he species (Ll anos and Crespo 1952).
Thei r r epr oduct i ve cycle is charact eri zed by a mai n zeal
in Mar ch- Apr i l and a secondar y zeal aft er a gest at i on of
153.7 + 0.5 days (Weir 1971 a).
To our knowl edge, t her e are no publ i cat i ons concerni ng
t he pr esence of t he par aur et hr al gl and in any species of
t he sub- or der Histricognathi. I n this st udy t he pr esence of
t he par aur et hr al gl and or f emal e pr ost at e in Lagost omus
rnaximus rnaximus (pl ai n viscacha, Blainville 1817) will
be descri bed, for t he first time, t oget her wi t h its anat omi -
cal localization and histological structure.
Materials and methods
Animals. Seventeen mature females of Lagostomus maximus
maximus weighing approximately 4.5 to 5 kg were used. They
were captured at different periods (December-January, March-
April and July-August), with the goal of including pregnant and
non-pregnant animals in the study. Animals were anesthetized
with intramuscular doses of ketamine-chlorohydrate (50 mg/kg
body weight) and sacrificed by bleeding. The complete urogenital
system was extracted and fixed in a 10% buffered formaldehyde
solution. The material was then processed for its embedding in
paraffin.
Histological processing. Three micron thick histological slides
were stained with the following techniques: routine Hematoxy-
lin-Eosine (HE); Masson's trichrome method to differentiate
muscular from connective tissue; Gomori' s argentic impregnation
for the observation of reticular fibers; Pranter's orceine to identi-
fy elastic fibers, and PAS for histochemical demonstration of mu-
cin.
Morphometrical study. For the macroscopic study a stereo-
scopic microscope (SZ40, Olympus, Japan) was used.
To carry out the morphometric study, 5 histological images
(magnification 200 x) were captured from each slide (Olympus
BX50 microscope, Japan) and digitized using an attached analo-
gue RGB video-camera (Sony DXC-151A CCD) connected to a
frame grabber (Flashpoint 128, Integral Technologies, Inc, India-
napolis, IN, USA). Twenty-four bits, TIFF format images were
then analyzed using the Image Pro Plus v4.5 image analyzer soft-
ware.
The following measurements were registered: major and minor
diameters (length of the longest and shortest lines joining two
outline points and passing through the centroid) of adenomers
and excretory ducts; height (caliper length along a major axis of
the object) and width (caliper length along a minor axis of the
object) of the adenomers' epithelial cells.
Statistical analysis. All data were expressed as mean + SD. A
Student's t test was used to identify significant differences be-
tween adenomer and epithelial cell parameters.
Statistical significance was accepted at the level of p < 0.05.
Results
Macroscopic analysis. All t he ani mal s studied pr es ent ed
t wo par aur et hr al glands. Anat omi cal l y, t he glands were
l ocat ed l at eral l y in t he vicinity of t he f emal e uret hra, near
t he uri nary bl adder - one at each side of t he uret hra,
wi t hout compl et el y surroundi ng it (Fig. 1). The size of
each gl and r anged f r om 0.6 to 1 mm long. Each unit ter-
mi nat ed at t he uret hra, in i ndependent form, t hr ough a
mai n duct.
Microscopic analysis. Microscopically, a l obul ar pat t er n
was obser ved (Figs. 2, 3). The mai n ducts had an oval
shape with a maj or axis of 220.18 + 67.77 gm and a mi nor
axis of 103.91 + 42.39 gm (Fig. 2). The lobules were sepa-
r at ed by t r abecul ae of connect i ve tissue with abundant
smoot h muscul ar fibers, seen with Masson' s t r i chr ome
t echni que (Fig. 4). The connect i ve tissue pr esent ed reticu-
lar fibers ( Gomor i ' s t echni que) t hat were mor e evi dent
ar ound t he adenomer s and ducts (Fig. 5) The orcei ne
t echni que showed t he pr esence of elastic fibers in t he
per i l obul ar tissue surroundi ng t he adenomer s (Fig. 6).
Each l obul e pr esent ed a mai n duct with a wide l umen
tlaat occasionally showed an i rregul ar pat t ern. It was gen-
erally cover ed by a bi -st rat i fi ed epi t hel i um (Fig. 7). I n its
l umen, a secret i on of acidic nat ur e similar to t hat found
in t he mal e pr ost at e coul d be observed.
The adenomer s had a t ubul oal veol ar pat t ern. Th e dia-
met er of t he adenomer s did not vary statistically bet ween
pr egnant and non- pr egnant femal es (Table 1). The epi t he-
l i um of t he adenomer s was simple, bei ng cuboi dal in t he
non- pr egnant femal es and cylindrical in t he pr egnant vis-
cachas (Table 2). The cells pr esent ed a r ounded or oval
nucleus l ocat ed in t he basal region. The apical por t i on of
t he cyt opl asm had a granul ar aspect. The small and scarce
granul es pr esent in t he apical por t i on of t he cyt opl asm
and t he secret i on found in t he l umen of t he adenomer s
were posi t i ve to t he PAS t echni que (Fig. 8).
Fig. 5. Female prostate section showing reticular fibers (arrows). Gomori, x 40.
Fig. 6. Elastic fibers in the connective tissue of the paraurethral gland (arrows). Orcein, x 200.
Fig. 7. Female prostate duct showing bi-stratified epithelium with eosinophilic secretion in the lumen. HE, x 200.
Fi g. 8. a: Columnar epithelium showing PAS positive granules at the supranuclear area. PAS, x 1000. b: PAS positive prostatic con-
cretions in the lumen of a lobule. PAS, x 100.
3 4 3
Table 1. Morphometrical pattern of the adenomers
Morphometrical Pregnant Non-pregnant Significance
parameter
Major diameter 93.05 + 15.57 92.14 + 13.26 NS
Minor diameter 52.77 + 9. 59 50.32 + 3.90 NS
All the numbers are expressed in pm _+ Standard Deviation. NS:
no significance.
Table 2. Morphometrical pattern of the adenomer ceils
Morphometrical Pregnant Non-pregnant Significance b
paramenter
Height 12.66 + 2. 28 11.24 + 3.70 NS
Width 6.34 + 0.55 6.65 + 0.94 NS
Significance a * NS
All the numbers are expressed in gm+Standard Deviation.
a. Significance between height and width of the same animal
group; b. Significance between either height or width of both
groups. * p <0.05, NS: no significance
Discussion
Few studies have been carri ed out on t he reproduct i ve
t ract of t he f emal e Lagostomus maximus maximus (Weir
1971 a, b), and no previ ous obser vat i on has r eveal ed t he
presence of t he f emal e pr ost at e or par aur et hr al gland in
this species. Some researchers have found this gland to be
present in di fferent species of mammal s of t he or der Ro-
dentia, al t hough with some di fferences in t he size, anat o-
mi cal l ocat i on and posi t i on of t he organel l es inside t he
cells of t he adenomers. The const ant pr esence of a bilat-
eral wel l -devel oped f emal e prost at e in some species of
t he Muridae family, for exampl e Rattus rattus, Rattus nor-
vegicus and in Avicantis niloticus has been descri bed
(Shehat a 1972, 1975, 1980). In t he Cricetidae family, t he
Skene' s gland could onl y be l ocat ed in Meriones lybicus.
I n t he l at t er case this is also bi l at eral but much smal l er
t hat in the ot her above ment i oned species. Gross and Di -
Di o (1987) descri bed t he f emal e pr ost at e in Praomys
(Mastomys) natalensis, poi nt i ng out t hat it is f or med by
two lobes ext ended medially, cranially to the uri ne blad-
der and can be ent er ed in cont act in t he vent ral por t i on
of t he uret hra. This anat omi cal posi t i on differs to what
was observed in Lagostomus maximus maximus. In our
observat i ons, t he viscacha par aur et hr al gland appear ance
is const ant , bi l at eral and wi t hout cont act bet ween t he t wo
glands. Cont r ar y to what has been descri bed in t he ot her
mammal s, in t he woman t he gland is f or med by ver y
rami fi ed ducts ( Huf f man 1948).
I n Rattus rattus, Rattus norvegicus, Avicantis niloticus
and Meriones lybicus t he adenomer s are cover ed by a sin-
gle l ayer ed cuboi dal or low col umnar epi t hel i um, which
contains acidophilic secret i on in its cyt opl asm (Shehat a
1972, 1975, 1980).
The st r oma t hat support s t he glands is f or med by con-
nect i ve tissue and smoot h muscul ar fibers. I n Praomys
(Mastomys) natalensis col umnar cells and small basal
cells f or m t he epi t hel i um t hat cover t he adenomers.
Gross and Di Di o (1987) also descri bed t he presence of
PAS posi t i ve granules in t he cells, as well as a secret ory
pr oduct with t he same staining characteristics. The histo-
logical st ruct ure descri bed in this wor k for Lagostomus
maximus maximus coincides in some aspects wi t h t hat
ment i oned for ot her rodent s; i.e. t he f or m of t he adeno-
mers, t he tissue t hat forms t he st r oma and t he charact er-
istics of t he secret i on product . With regard to t he cell
types, we have obser ved t hat t he epi t hel i um t hat sur-
rounds t he gl andul ar units is single cuboi dal or col um-
nar, similar to t hat descri bed for Rattus rattus and Rattus
norvegicus (Shehat a 1972, 1975, 1980), whilst we have
not found basal cells as in Praomys (Mastomys) nataIen-
sis.
In some rodent s t he Skene' s gl and mai nt ai ns its histo-
logical st ruct ure t hr oughout its l i fet i me (Gross and Di -
Di o 1987). I t was also descri bed t hat its size increases
during gest at i on and also duri ng t he nursing peri od in fe-
mal e rodents. We found di fferences in t he f or m of t he
gl andul ar cells, bei ng cylindrical or col umnar in t he preg-
nant femal es and cuboi dal in t he non- pr egnant animals.
I t is possible t hat such a di fference has some rel at i onshi p
to t he hor monal changes t hat t ake pl ace during t he preg-
nancy.
The adenomer s of mucous t ype t hat Shehat a (1972) de-
scribed for Rattus rattus were not obser ved in Lagostomus
maximus maximus.
In t he woman, t he f emal e pr ost at e has been studied
f r om several aspects. I t has been demonst r at ed t hat the
cells react positively to pr ost at e specific ant i gen of the
mal e and also to alkaline phosphat ase. I t could also be
demonst r at ed t hat t he hi st oenzymafi c par amet er s of
t he prost at i c gland in the woman were compar abl e to
t hose of t he mal e pr ost at e (Zavia~i~ 1985). The rele-
vance t hat it acquires in human beings resides not only
in t he lesions t hat t he gland can mani fest , but also
whet her a rel at i onshi p exists bet ween t he secret i on of
t he gland and f emal e ej acul at i on as a pr oduct of sti-
mul at i on during coitus, of t he so called " G spot ". I n
animals, t he existence of t hat ej acul at i on has not yet
been det ermi ned, al t hough t he presence of a well de-
vel oped gland could have a similar significance. The
di scovery of a pr ost at e of const ant appear ance in the
viscacha f emal e would allow t he use of this ani mal as
an exper i ment al model for studying t he physi ol ogy of
t he gland.
Acknowledgements. The technical work done by Ruben C. Ma-
rio and the personnel of the Estaci6n de Cria de Animales Sil-
vestres (ECAS), Ministerio de Asuntos Agrarios de la Provincia
de Buenos Aires is acknowledged. We would like to thank Tamar
Ferguson for the proofreading of the manuscript. ELP and EJG
are Research Career Members of CONICET (National Scientific
Research Council).
344
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Accept ed February 12, 2002
345