Pathology of the equine salpinx - Pferdeheilkunde Equine Medicine

Pathology of the equine salpinx - Pferdeheilkunde Equine Medicine

Pferdeheilkunde15 (1999)6 (November/Dezember)
560-567
Pathologyof the equinesalpinx
KerstinMedenbachl, Heike Aupperlel, Doris Schoonl, M.M. Wittenbrinkzand H.-A. Schoonl
I lnstitutfür Veterinär-Pathologie,
UniversitätLeipzig,Deutschland;2 lnstitutfür Veterinär-Bakteriologie,
UniversitätZürich,Schwerz
Summary
Equineutennetubeswereevaluated
(n=100)
macroscopically
andmicroscopically
(n=76).l\.4acroscopic
lesionsoccurredas infundibular
adhesionsandinfundibular
cysts.Microscopically,
themostcommonfindings
wereintraepithelial
cystswithintheampulla,
slight,multfocalepithelial
andsubepithelial
infiltration
withlymphoc!'tes
andtheoccurrence
junction.
of collagen
masses
withinthelum€noftheampullary-isthmic
In the majority
of the uterinetubesepithelial
cellsshowedan extraordinary
coexpression
of desminandc!,tokeratin.
Thepathological
significanceof thiscoexpression
is questionable
andmightbe attributed
to the physiologic
hormonal
activityduringcycleandpregnancy
respectivelV.
Forthe frst timechlamydial
antigenwasdemonstrated
in the equinesalpinxby meansof an immunohistologic
technique.
In liveof twenty
maresa positive
psittaci-antibody
stainingfor Chlamydia
wasevidentin someepithelial
cellsof the isthmusandto a lesserextentin thoseof
theampulla.
Thesemaresshoweda multifocal
c!'toplasmic
eosinophilia
of theuterinetubeepithelium
anda slightto moderate
endometrosis
of the endometrium.
In two maresdetectionof chlamydial
antigenwasassociated
witha slightchronicsalpingitis
and in two othermares
witha slightchronicendometritis.
Keywords:
equine,salpingitis,
chlamydia,
desmin,immunohistology
Pathologie der equinen Salpinx
Eileitervon Stuten wurden makroskopisch(n=100)und mikroskopisch(n=76)untersucht.Als makroskopischeVeränderungenlageninfundibuläreAdhäsionenund infundibuläreZysten vor. Die häufigstenmikroskopischenBefundewaren intraepitheliale
Zysten, multifokaleInfiltrationenvon Lymphozytensowie luminalvorkommendekollageneMassenim Bereichdes Übergangsvon der Ampullarn den lsthmus.
Bei der immunhistologischen
Untersuchungzeigtendie Epithelzellen
der meistenEileiterepithelien
eine außergewöhnliche
Koexpressionvon
Desminund Z,'tokeratin.Die BedeutungdieserKoexpressionist fraglich,ursächlichkönntenphysiologischeVeränderungendes Hormonstatus im Verlaufdes Zyklusbeziehungsweise
der Graviditätverantwortlichsein.
Mit Hilfeimmunhistologischer
Verfahrenwurde erstmaljgChlamydien-Antigen
in der equinenSalpinxnachgewiesen.In fünf von zwanziguntersuchtenStuten konnteChlamydien-Antigen
in den Epithelzellen
des lsthmusund in einemgeringeremMaß in der Ampulladargestelltwerden. DieseStuten zeigteneine multifokalezytoplasmatische
Eosinophiliedes Eileiterepithels
und eine gering- bis mittelgradigeEndometrose
des Endometrlums.Der Nachweisvon Clamydien-Antigen
war bei zwei Stuten mit einergeringgradigenchronisch€nSalpingitisund bei zwei
weiterenStuten mit einergerlnggradigen
chronischenEndometritisverbunden.
Schlüsselwörter:
Pferd,Salpingitis,Chlamydien,Desmin,lmmunhistologie
Introduction
The mammalianuterinetube servesas a conduit from the
ovary to the uterus providinga satisfactoryenvironmentfor
final maturationof the oocyte, sperm transport, sperm capacitation,fertilisation
and earlyembryonicdevelopment.
D u e to t he uniquec on d i ti o n so f th e e q u i n es a l p i n xthe
, environmentof the uterinetube is a known intrinsicfactor of
possiblecausesfor embryonicloss in mares.These conditions are a prolongedpassageof the equineembryo,resulting in a more advancedstage of developmentof the embryo, retentionof unferlilisedoocytes and the selectivepassage of embryos (Ball, 19BB).
There is extensiveliteratureon the pathologyof the equine
endometriumrelatingto reduced fertility,but in only very
few studies has the influenceof alterationsof the eouine
salpinxbeen examined.
Pathologicallesionsof the uterinetube play an important
role in other domesticanimalssuch as cows (Kessyet al.,
19BS)and sows (Wilsonet al., 1949). Tube-associatedinfertilityin women is frequentlycaused by Chlamydia-in-
560
duced salpingitis.
A similaretiologyof equinesalpingitishas
not yet been reported.
The object of this study was
- to characterisepathologicalfindingsof the equineuterine
tube by lightmicroscopy,supporledby immunohistological examination,
- to determinethe presenceof chlamydialantigen in the
equinesalpinxby immunohistological
techniqueand
- to evaluatepossible relationsbetween inflammatoryprocessesof the uterinetubes and the endometrium,
The uterinetube of the mare, usually20 to 30 cm in length
and 1.5 to 3.0 mm i n di ameter,can be di sti nguishedin
three parts:the infundibulum,
the ampullaand the isthmus
runninginto the uterus (fhrelfall,1995).
The epitheliumof the mucosaconsistsof two cell types: ciliatedand non-ciliatedcells (Fig. 1). The ciliatedcells play
an importantrole in the transportof the oocyte,while most
of the non-ciliatedepithelialcells represent secretory cells
producingand releasingproteinsas well as glycoproteins
'15
Pferdeheilkunde
Kersttn Medenbach eI al.
into the lumen.A third residentcell type,the peg cell,is
variantof the secretorycell
likelyto be a morphologic
(Liebichet al., 1999).
cycle stage was ascertainedby examinationof the ovaries
and the uterinetubes were first evaluatedfor gross abnormalitiesand lesions,
One half of the uterinetubes of 76 mares was removed by
into
longitudinal
sectionfrom the transitionof the infundibulum
a part
the ampullato the tip of the uterinehorn.Additionally,
of the corpus uteriwas excised.The specimenswere routinely embeddedin paraffin.The sectionswere stained,usingheperiodicacid-Schiff(PAS)-alcianblue-,
toluimatoxilin-eosin-,
staining.
red- and Papanicolaou
dineblue-,picro-sirius
The endometriawere classifiedin categoriesaccordingto
Kenney and Doig (1986).
studies,the tissueswere stainedfor
For immunohistolcgical
CD 3, lgA, lgG and lgM and for the intermediatefilaments
desmin,cytokeratinand vimentinby using the peroxidasenique,
anti-peroxidase-tech
The specimenswere investigatedby enzymehistochemistry
mare,luteal for CLAE (chloracetatesterase).
Fig.1: Normalmucosaof the ampulla,13-year-old
phase:The epitheliumconsistof ciliatedand secretory The uterinetubes of 20 mares were stainedfor the expresarefoundbetweenthe epitheli- sion of chlamydialantigenusinga Chlamydiapsittaci-specicells,singlelymphocytes
stain,
al cellsor in the laminapropria.(PAS-alcianblue
fic monoclonalantibodv,
magnification
125x).
13jährige
Stute,GelbMukosaderAmpulla,
Unveränderte
undsebestehtausZilienzellen
körperphase:
DasEpithel
liegenzwischen Results
Lymphozyten
kretorische
Zellen,einzelne
propria.(PAS-Alcianden Epithelzellen
oderin der Lamrna
125x)
Vergrößerung
Fxpression of intermed iate filaments
blau-Färbung,
Material and methods
From summer 1996 to winter 1998 a total of 100 genital
tracts from mares of differentage and breed was collected
at the Instituteof VeterinaryPathology of the Leipzig University and at slaughterhousesand fixed in formalin.The
Stromal cells and vascularendotheliaare stained positive
for vimentin. The unstriated muscles and the smooth
muscle cells of the vesselsshow an expressionof desmin
and to a lesserextentof vimentin.
Epithelialcells exhibit expressionof cytokeratinand in most
of the mares unexpectedlya coexpressionof desmin is revealed.In these cases desminappearsto be presentespeciallywithinthe ciliatedcells(Fig.2).
The stainingfor desmin in the ampulla,compared with the
isthmus,is more remarkable,variesin intensityand occurs
as smallspots eitherin the basalor the apicalcytoplasm.
In only two of the 26 mares examined is the epithelialexpressionof desmin undetectable,Both mares are found in
oestrus,in the absenceof other parameterssuch as age or
pathologicalalterations.In seven mares some epithelial
cellsof the ampullawith a very slightstainingare observed.
The epitheliumof 13 mares is stained slight to moderate
and the epitheliumof four maresis stronglystainedfor desmin revealingtwo pregnancies,
Pathology
l nfundi bul ar
adhesi ons
In nearlyhalf of the mares examined,thin fibresof conneclinkingfimbriaeand
tive tissueare found, mostly bilaterally,
UnveränderteMukosa der Ampulla, 3jährige, tragende
ovary,The adhesionsare observedas thin strands of fibround in den glatStute (3. Monat):In epithelialenZilienzellen
us tissue,sometimesassociatedwith blood clots, between
ten Muskelzellen
der Gefäßeist eine intrazytoplasmatische
infundibulumand ovary, mesovarium,mesosalpinxor the
nachweisbar.
Die
sekretorischen
Expressionvon Desmin
uterus(Fig.3). In no case howeveris the infundibulumobDesmin,NorZellenreagierennegativ.(lmmunohistologie,
125 x)
Gerätevergrößerung
marski-lnterlerenz-Kontrast,
structedbv the adhesions.
'15
Pferdeheilkunde
56'1
salPinx
of theequine
Pathology
lnfundibular cysfs
More than one third of the mares (n=37)has cysts, obserin the fimbriatedportionof the uterine
ved macroscopically
(n=23)and bilatetube (fig,4). The cysts occur unilaterally
ra l l y(n = 14) .
cyst with a diameterof '1.0x 1'3 x 0.9
Fig.4: An infundibular
cm is locatedat the fimbriae(fixedin formalin;the uterioPened).
netube is partiallY
befindetsich eine
des Infundibulums
An den Fimbrien
.1,3x 0,9 cm (in
von 1,0x
Zystemit einemDurchmesser
partiell
Eileiter)'
erÖffneter
fixiert,
Formalin
tissue
Thinfibresof connective
adhesions:
Fig.3: Infundibular
to the Liand the mesosalpinx
linkingthe infundibulum
gamentum
ovariiProPrium.
ZwischenInfundibulum,
des Infundibulums:
Adhäsionen
ovariipropriumbefinden
und Ligamentum
Mesosalpinx
sichdünneBindegewebsfäden.
The diameterof the predominantlysmallcysts variesfrom a
few millimetresup to one centimetre,only very few are larger than two centimetres.The uterinetubes concernedeither show a singlecyst (n=32)or a seriesof two to four adjacentfrequentlysmallcysts (n=19).
Their luminacontain a transparentfluid,The epithelialcells
of the cysts are flattened or cuboidal with hyperchromattc
elongatedor round nuclei,The appearanceof some epithelialceltsliningthe cystic lumen is similarto those of the uterine tube. Some cells have few short cilia on their sudace,
whereasothersresemblesecretorycells.
lntraepithelial cysts
cysts are found frequentlyin the ampullabut
Intraepithelial
not in the isthmus.The cysts are most often locatedwithin
the epitheliumalongthe sidesand the basesof the mucosal
folds.Theirdiametervariesfrom 1Oto 100 micrometerand
the type of cell liningdiffers.Some of them are flattenedwith
to the luminalspace,
slendernucleiand orientperpendicular
cilia proothers are cuboid with round nuclei.Occasionally
ject into the cystic lumen.Some cysts containmatertalthat
(Fig.5).
is stainedlightbluewith PAS-alcianblue
cysts. In 9 mareson13 of 66 mares have no intraepithelial
cysts in the total of the
ly one or two single intraepithelial
longitudinalsection are detectable.
cysts is found in
The marked presence of intraepithelial
(n--44\
into
three degrees:
and classified
most of the mares
(n=30),
per
mm
5
up to fivecysts
sl i g h t( + )
(n=11) and
per
mm
5
(++)
cysts
six to fifteen
moderate
per
mm (n=3)'
5
(+++)
fifteen
cysts
than
more
severe
is obsercysts
intraepithelial
of
appearance
the
Frequently
(n=7).
unilaterally
(n=35)
less
often
and
ved bilaterdly
562
The epithelialexpressionof desminis most intensein those
mares classifiedas moderate(++) or severe(+++) with recysts.
gard to the intraepithelial
mares of known age with mode13
of
It is strikingthat five
(+++)
of intraepithelialcysts are
degree
(++)
or severe
rate
the
mares are youngerthan
of
years
Two
thirds
old.
three
pregnant.
young
is
years,
mare
one
eight
pregnant
mare(thirdmonth):Intrae3-year-old,
Fig.5: Ampulla,
pithelialcystsare locatedat the basesof the mucosal
folds, their luminacontainlight blue stainedmaterial'
62.5x)
(PAS-alcianblue
stainmagnification
Stute(3.Monat):Intraepitheliatragende
Ampulla,
3jährige,
lokalile Zystensind an der Basisder Schleimhautfalten
Materiblaugefärbtes
leuchtend
siert,ihrLumenbeinhaltet
62,5x)
GerätevergrÖßerung
al.(PAS-AIcianblau-Färbung,
of epithelialcells
Degeneration
In five mares a cytoplasmiceosinophiliaaffectingseveral
groups of epithelialcells identifiedby HE stainingis remarkable. These epithelialcells show an alteration of the
structureas well.They are increasedin Size,rouneOithelial
ded, with a small round hyperchromaticnucleusand a vacuolated cytoplasm giving the cells a foamy appearance
(Fig. 6). The cytoplasm of these epitheliais stained light
green-greyand their nucleidark grey in the Papanicolaou
stai n.
15
Pferdeheilkunde
Kerstin Medenbach eI al.
The epitheliumfrequentlyseemsto be stratified.Only in one
mare is cytoplasmiceosinophilianot associatedwith alterations of the epithelialstructure.
basal epitheliaand a comparablenumber of cells are scattered throughoutthe laminapropria,These small and oval
or round cells with dark nucleiand scanty hypochromatic
cytoplasmare stained positivefor CD 3 surface antigen,
those cellsas T lymphocytes(Fig.B).
therebycharacterising
Inflammatoryprocessesat the entranceof the ampullaare
n=12,
obvi ousi n one thi rd of the mares (n= 27, uni l atera l:
bilateral:n=15). Most of these mares (n=16)show a slight
with lymphocytesin the ammultifocalor diffuseinfiltration
pullarmucosasometimesassociatedwith plasmacells,hyoeraemiaor oedema of the mucosa. Plasmacells expressing lgA are the most common cell type in the laminapropria. Occasionallyplasma cells of lgG and rarely of lgM
subtype are identified.Moderateto severe salpingitiswith
infiltration
of lymphocyteswas found lessoften (n=6).
of
mare:Cytoplasmic
eosinophilia
Fig.6: Ampulla,21-year-old
epithelial
cells.(H.-E.stain,magnification
degenerated
62. 5x )
Eosinophilie
Ampulla,21jährige
Stute:Zytoplasmatische
(H.-E.-Färbung,
GeräteEpithelzellen.
der degenerierten
vergrößerung
62,5x)
Collagenmasses
ln half of the mares uterinetubes are found to containeosiThe masnophilicmassesof varyingsize,mostlyunilaterally,
junctionconsisting
ses are locatednearthe ampullary-isthmic
of swirlingbundlesof fibres.They are not connectedto the
epitheliumand frequentlydistendthe lumen,The bundlesof
fibresare stainedred with picro-siriusred (Fig.7) and blueThese results stronglysuggest
violet with PAS-alcianblue.
that the massesconsistof collaoenfibres,
Fig.8:
Normal mucosa of the ampulla, 3-year-old, pregnant
mare (thirdmonth):T lymphocytes(brown)in the epitheCD 3
lium and in the laminapropria.(lmmunohistology,
magnisurface antigen, Nomarski-interference-contrast,
fication62.5 x)
UnveränderteMukosa der Ampulla, 3jährige,tragende
Stute (3. Monat):T-Lymphozyten(braun)im Epithelund
CD 3 Oberin der Lamina propria. (lmmunhistologie,
Geräteflächenantrgen,Nomarski-lnterferenz-Kontrast,
62,5 x ).
vergrößerung
In rare cases (n=5) a moderate to severe infiltration with
neutrophilic granulocytes is observed and interpreted as indicative for an exudative salpingitis (Fig.9). In three cases
some eosinophilic granulocytes are detectable in the lamina
Fig. 7:
junction, 1B-year-oldmare: Collagen
Ampullary-isthmic
masses are located within the lumen and consist of swirling bundles of fibres. There is no attachmentto the
(Picro-Sirius
Red stain,magnification
31.25 x)
epithelium.
Übergangder Ampulla in den lsthmus, 18jährigeStute:
KollageneMassen sind im Lumen lokalisiertund bestehen aus wirbeligen Faserbündeln,die nicht mit dem
Epithel verbunden sind. (Pikrosirius-rotFärbung, Verg rößeru ng3 1,2 5 x )
S alping itis
ln the amoulla as well as in the isthmus of the unaffected
uterine tubes a few lymphoid cells are located between the
15
Pferdeheilkunde
propna.
Neither slight nor moderate mononuclearinfiltrationsare
associated with mucosal damage as observed by light
microscopy,Severeinfiltrationof lymphocytesand neutrophilicgranulocyteshowevercausesdestructionof epithelial
cel l s.
The unaffectedisthmus,comparedto the ampulla,shows a
loweramountof T lymphocytes(CD 3 positivecells),Inflammation of the isthmusis diagnosedin 12 mares characterisedby a slight(n=9)or moderate(n=3)diffuseor multifocal
infiltration
of lymphocytes.Plasmacellsare rarelydetectable.
In only one mare are neutrophilicgranulocytesidentified,
granulocytes
are absentfl-ab.1).
whereaseosinophilic
20 of 76 mares investigatedshow a slight(n=6),moderate
(n='10)or severe(n=4)endometritis.In 17 of these cases a
563
Pathologyof the equinesalpinx
mononuclear endometritis is diagnosed and
mares an acute exudativepurulent endometritis
t ?,
the apical and to a lesser extent in the central or the basal
cytoplasmof the epithelialcells (Fig.10).A non-specificreaction can be excluded because these reaction products
are not found in the negativecontrols.All positivefive mares show a multifocal,slight to severedegenerationof ciliated and secretory cells with cytoplasmic eosinophilia.The
positivestainingis only detectablein severalintact epithelial
cells and the degeneratedeosinophiricceils, The epithelial
cells involvedhave largeand hypochromaticnucleisometimes showingindentations.
The stainingfor chlamydialantigen is more intense in the epithelialcells of the isthmus
comparedto those of the ampulla.
Exsudative
Ampullitis,
6 MonatealtesFohlen:Infiltration
von neutrophilen
Granulozyten
(rot)in der Mukosa.(En_
zym-Histochemie,
CLAEChloracetatesterase,
Verqröße_
rung62,5x)
In one half of these mares with endometritis(n=10)a syn_
chronous inflammationof the uterine tubes is observed.
salpingitisis evident in 2 of 6 mares (33vo)with slight, 4 of
10 mares (4)o/o)with moderate and 4 of 4 mares (100%)
with signsof a severemononuclearendometritis.
ln 17 oI 27 maressalpingitis
withoutendometritis
is diagnosed,17of 23 mares (75%)with salpingitisare youngerthan
10 years, whereas g of 15 mares (60%) with endometritis
are olderthan .10years.
Tab. 1: Distributionof differentinflammatory
cells comparing
ampulla,
isthmusandendometrium
(totalnumberof maresinvestigated:
n=76).
lsthmus,
21jährige
Stute:Chlamydien-Antigen
(braun)
ist
vorwiegendim apikalenZytoplasmader Epithelzellen
darstellbar.
(lmmunhistologie,
chlamydiapsittaci-spezifischermonoklonaler
Antikörper,
Vergrößerung
l23 x)
In only three of these mares is a slight increaseof lymVergleichder Verteirung
verschiedener
Entzündungszerlen in Ampulla,lsthmusund Endometrium
(Gesamtzahl phocytes and a few plasma cells of the lgA subtype observed. In two of the maresonly,the mucosaof the uterinetuuntersuchter
Stuten:n=76).
bes appearsto be markedlychangedand a slightinfiltration
Ampufla lsthmus Endometrium
of mononuclearinflammatorycells and moderate to severe
degenerationof epithelialcells is evident.
Infiltrationwith
slight
to
9
7
In the endometriumof all of the five mares a slight to modelymphocytes, moderateto
rate
endometrosisis observed, slight to moderate endoplasmacells
severe
b
10
metritisis diagnosedin only two cases. All mares are claslnfiltrationwith
slight
1
sified in the category ll b and those with known age (n=4)
neutrophilic
moderateto
are olderthan 15 vears,
granulocytes
Ä
severe
Infiltrationwith
eosinophilic
granulocytes
No infiltration
slight
moderateto
z
Discussion
Q O \ / ATA
A
49
o4
56
lmmunohistological
stainingfor chlamydialantigen
In five of twenty mares investigatedpositive staining for
chlamydialantigenis evidentand occurs as small spots in
564
The examinationof the equine uterine tube revealsa high
incidence of macroscopic and microscopic lesions. The
presentstudy finds infundibularadhesionsto be the most
common macroscopiclesionsin the mare, in agreement
with Henry and Vandeplassche(1981) and Saltiel et al.
(1980).In accordancewith our results Henry and Vandeplassche(1981)diagnoseno case of infundibularobstrucPferdeheilkunde
15
KerstinMedenbach
eI al.
tion. The origin of the infundibularadhesionsis unknown
but the authors suggest that frequent attacks of colic and
peritonealinflammatoryprocesses lead to the adhesions.
The migration of Strongylusedentatus seems to be a further cause of infundibularinflammationsresultingin adhesions [/andeplassche and Henry, 7977). Furthermorethe
authors consider that postovulatoryhemorrhagesfrom the
ovulatoryfossa might be responsible.
Comparing the incidence of adhesions in pregnant and
non-pregnantmares Saltielet al. (1.986)cannot ascertaina
marked differencebetween the two groups indicatingthat
these lesionsmay not be detrimentalto fertilityin mares.
One of eight pregnant mares in the present study reveals
bilateralmoderateinfundibular
adhesions,whereasthe fertilityof this mare remainedintact.
The frequentobservationof cysts found in the infundibulum
by the current examinationis supported by the results of
Saltiel et al. (1986) who describe ,,paraovariancysts" in
44o/oof mares. Mc Entee (1990) suggesteda redefinitionof
the term ,,paraovariancyst" - incorrectlydeterminingany
type of cyst located around the ovary - and use of a specific designationfor each type of cyst. The histologicstructure as well as the location of a cyst are important for the
ascertainmentof the origin.Cysts close to the uterinetube
or the ovary are usuallyremnantsof the mesonephricor
paramesonephrictubules or ducts and are common in
most speciesof domestic animals.
These small congenital cysts frequently occur in the
fimbriated portion of the equine salpinx and tend to be
multiple.The presentstudy revealsthree of eight pregnant
mares havingsmall infundibularcysts, therebyprovingthat
infundibularcysts had no effects on fertility. Blue (1984)
describes the presence of a tubo-ovariancyst (9cm in
diameter)of a young thoroughbredmare causingunilateral
obstruction of the uterine tube. This type of cyst is described as a complete fusion of fimbria with the ovary and
is extremelyrare. The aetiologyin the mare remains unkn o wn.
As repofted in the study of Saltielet al. (1986/ intraepithelial
cysts are the most frequent microscopic lesions of the
equinesalpinxin our materialtoo. In cows the intraepithelial
cysts are interpretedas a sequelaof hyperestrogenicsituations (Donaldsen,7969).Mc Entee (1990) observes similar
cysts in the fimbriaand to a lesserextent in the ampullaof
cows on days 9 through to 30 postpartum.
Odor (1991) revealsthe largest number of intraepithelial
cysts in rabbits, especiallyin the isthmus, with estradiol
treatment.The authorsuggeststhat intraepithelial
cysts derive from a fusion of adjacent ciliated vacuoles. Atypical
ciliogenesrsmay be responsiblefor the developmentof
ciliatedvacuoles. Microtubules,microfilamentsand intermediatefilamentsmight be involvedin this processtoo.
The current study reports an atypical immunohistological
coexpressionof the intermediatefilaments desmin and
cytokeratinin the epithelialcells. Smooth muscle cells are
usuallystainedfor desmin,but the coexpressionof desmin
and cytokeratinin the epithelialcells is extraordinary,Wakui
(1994) demonstratesthe coexpressionof differentcytokePferdeheilkunde
15
ratins,vimentinand desmin in the epitheliumof the rete testis in the dog.
It might be possiblethat the ciliatedcellsof the uterinetube
express desmin indicatingmotilitysupport. The variationof
desmin expressionin the epitheliumthereforecan attribute
to differentcycle stages.
Our results reveal a marked exoression of desmin associated with an increaseof intraepithelialcysts, but the flattened cells lining the cysts are rarely stained for desmin.
Thereforeit is doubtfulwhetherdesmin should be interpreted as a markerof epithelialdamage such as abnormalities
of ciliogeniccells.Electronmicroscopywill be necessaryto
understand physiologicalor pathologicalconditions that
leadto the exoressionof desminin the eoithelialcells.
It is questionablewhether pathologicalsignificancecan be
deduced from the frequent occurrence of intraepithelial
cysts in mares, especiallyin those being young or pregnant. lf comparablefindings in rabbits after estradioltreatment and in cows postpartum are considered an atypical
ciliogenesis,
likelyas a resultof hormonalundulation,might
leadto intraepithelial
cysts.
The incidenceof globularmasses reported in the uterine
tubes of mares varies from 2OVolo B7o/o(van Niekerkand
Gerneke, 1966; Liu et al., 1990). The masses, predominantlycharacterisedas collagenfibres by specialstainings,
juncare always located at or near the ampullary-isthmic
(1979)
tion, While Isutsumi et al.
report that the materialis
connected to the epithelium,Liu et al. (1990) find no
attachmentto the epithelialcells.Two opinionsare presented as to the origin of the masses; namelythe ovarianor
peritonealorigin (van Niekerkand Gerneke, 1966; Liu et al,
1990) and the uterinetube mucosal origin (fsutsumi et al.,
1979). In our material we can observe neither collagen
massesattachedto the eoitheliumnor the evidenceof desquamated tubal cells, Therefore we agree with Lru et al.
(1990) who presume that the collagen derives from the
ovary or the peritonealcavity.
Aquilar et al. (1997) find livingcells within the intraluminal
masses that are predominantly identified as fibroblasts.
Lantz et al. (1998)attributethe collagenmasses with viable
fibroblaststo recent ovulationand conclude that connective
tissue, drawn in the uterinetube at ovulation,is retained
and collagensynthesiscontinuesat leastfor a few days.
The intraluminalaccumulationof large masses of collagen
fibres may potentiallyresult in a complete occlusion,causing retentionof the ova. Furthermorethe collagenmight irritatethe uterinetube musclesor interferewith the waves of
ciliary activity (Liu et al., 1990). The authors suspect that
the age of a mare might influencethe amount of masses
since largermassestend to be presentin the uterinetube
of some older mares.
The retentionof unfertilisedoocytes in the mare is unique
among domestic animals,These ova originatefrom previous normalcycle ovulationand persistin the uterinetube
for several months (Betteridge and Mitchell, 1974). Most
frequentlythe ova are found in the ampullary-isthmicjunction and do not have any attachment to the epithelium.
Horse embryos therefore bypass the unfertilisedoocytes
565
Pathology
of theequine
salprnx
hardly observed. Henry and Vandeplassche (1981) who
and enter the uterus.Freemanet al. (1989a)suggestthat
likewisedescribe an increaseof inflammatoryalterations
horse embryos initiate transport mechanismswithin the
uterinetube by secretinga mediator.Weber et al. (1991) from the isthmusto the infundibulumsuggest that the infundi bul umand the ampul l ami ght be more susceptiblet o
support the hypothesisthat embryonicPGE2is involvedin
inflammationwith regard to their more folded mucosa or
the initiationof uterinetube transoortin the mare.
To determinethe retentionof unfertilised
oocytesit is of adthat the isthmus recoversmore rapidlyfrom inflammation,
vantageto flush the uterinetube and to search for ova in
The authors have no doubt that salpingitiscan originate
investigation
from an endometritisbut they also discuss the possibility
the flushingswherebylightmicroscopic
of parof salpingitisdevelopingdue to an extensionof inflammaaffin slides only occasionallyrevealspositiveresults.This
might be an explanationfor the negativeresultsin our study
tory processesfrom the infundibulumand the peritoneal
cavity,
concerningthe detectionof unfertilisedoocytes.
The intactuterinetube is determinedto be almostfree of inSaltielet al. (1980) diagnose slight inflammatorylesions
filtratinglymphocytesby Vandeplassche
and Henry (1977)
correspondingto the upper segment of the uterine tube
The presentstudy howeverstatesthat HE stainingalone is
and thereforehypothesisethat the lesionsdo not originate
inadeouatefor the detectionof the total numberof mucosal from the uterineportionbut are the resultof disorders,such
melymphocytes.With use of specificrmmunohistological
as non-reproductive
diseasesin the abdominalcavity,octhods for CD 3 lymphocyticsurfaceantigenit is possibleto
curringtowardsthe ovarianportionof the salpinx.In mares,
revealthe existenceof a certainT lymphocytepopulationin
the occlusionby a sphinctermuscle about the uterineostithe epitheliumand the stromaeven under obviouslyphysio- um might preventascendinginfections.
logicalconditions.Some studiesreportthe natureof ,,basal" The positiveimmunohistologicreactionsusing Chlamydia
psittaci-antibodyis demonstratedfor the first time in the
cellsin the epitheliumof the uterinetube. Peters(1986)idenequinesalpinx.The selectivetropism of Chlamydiaspp. to
tifiesthe ,,basal"cellsin humanbeingsas T lymphocytes.
Light focal or diffusemucosal infiltrationof lymphocytesis
cervix and salpinx is suggested as an important circumnot uncommon and also frequentlyobserved by Henry and
stance of chlamydialgenitalinfectionsin severalstudies in
humanbei ngs,
Vandeplassche(1981) and Sa/fielet al. (1986).These lymphocytesmay or may not indicateinflammation.
The decisi- Rank and Sanders (1992) investigatethe pathogenesisof
on in a certaincase is arbitrary.Undoubtedlythe infiltration ascending chlamydial infection of the genital tract in
fi ndi ngsare acute or chr oof neutroohilshas to be interoretedas an exudativeinflam- gui neapi gs. P athohi stol ogi cal
nic endometritisand salpingitis.Chlamydiaare reisolated
matoryprocessin the equinesalpinx,
Our results agree with those of Vandeplasscheand Henry
by culture technique in most of the uterinetubes (78%),
(1 9 7 7 )des c r ibings alpin g i tiisn th e m a re a s m i l d n o n -occl u- while only half of the animalsinfected(49%)show pathohisive, infiltrative,
or less often exudative,infundibulitis,
amstologicalchanges.
p u l l i ti sa nd is t hm it is O
The presenceof plasma cells in three of five mares might
. n th e o th e r h a n d s a l p i n g i ti si n the
be a morphol ogi cal
fi ndi ngi ndi cati nga cel l ul ari mmuner escow is characterisedby masses of connectivetissue wrth
ponse followingprimarychlamydialinfectionsas described
extensivecellularinfiltrationreplacingthe mucosa and reby Patton et al. (1989) in the monkey subcutaneouspocket
sultingin a completeobstructionof the lumen(Kessyet al.,
7985).Neithertransluminaladhesionsof mucosa folds nor
model.The authorsobserveearlyepithelialdamagesin the
secretoryand ciliatedcells by vacuolisation.
Chlamydialinobstructionof the lumen is diagnosedin the presentstudy
confirmingthe resultsof Henry and Vandeplassche(1981) clusionsare found in secretorybut not in ciliatedcells.After
tertiary infection especially epithelial eosinophilia,focal
who checked the tubal patency by the injectionof Bouin's
areas of eoithelialdestructionand luminalexudatecorrelasolutionand assume that salpingitisin the mare is not as
ted with mononuclearcell infiltrates
are detectable.
severe,or healsmore readilythan rn cows and sows.
This observationagreeswith the resultsof the currentstudy
Allen et al. (1979) investigatethe usefulnessof two experimentalproceduresfor the diagnosisof occlusionsaffecting revealingeosinophiliaof the epitheliumin associationwith
the equine salpinx.The starch grain test, which is carried the evidenceof chlamydialantigen.Furthermore,infiltration
out by the injectionof a starch suspensiononto the ovary
with lymphocytesis found.
By use of special staining(Papanicolaoustain) it can be
and the subsequentrecoveryof starchfrom the cervix,is a
provensafe and reliablemethod. Each tube can be investi- excludedthat the degenerationof the epitheliumis related
gated separatelyin contrastto the phenolsulphonphthalein to a metaplastickeratinisation.Electronmicroscopicstu(PSP)test, which impliesthe depositionof a dye solutionindies will have to be carriedout to establishwhether cytoplasmiceosinophiliais due to chlamydia-induced
to the uterusand its subseouentidentification
in urineafter
cytoplasperitonealabsorption.
mic degeneration.
The presentstudy finds no predominanceof unilateralor biCytoplasmiceosinophiliain the human uterinetube is delateralsalpingitisand thereforecannot agree with the rescribedas oncocyticmetaplasiaas well and in the case of
sults of Henry and Vandeplassche(1981) who witnessed
associationwith salpingitisand papillarychanges is interpreted as a benign tumour (Saffos, 1980). By contrast, no
more frequentoccurrencesof unilateralsalpingitis.
case of papillarychangesin the equinesalpinxis observed
Compared with the isthmusthe ampulla is most often involved in inflammatoryprocesses, whereas an isthmitis is
in the presentstudy.
566
15
Pferdeheilkunde
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1
6
9
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8
0
6
8
3
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Chlamydia-inducedinfertilityhowever is based on several Rank,R. G. and Sanders,M. M. (1992):Pathogenesis
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. m . J . C l i n .P a t h o l . , 7 4 , 2 3 2 - 2 3 6
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Saltiel,A., Päramo,R,, Murcia,C. and Tolosa,J. (1980):Pathologic
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as well, whereby increasingseverityof the endometritis
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Henry, 1977).The presentstudy reveals'17casesof salpingitis in the absence of endometritissuppoftingthe suggestion that an originof inflammationfrom the proximalportion of the uterinetube is oossibletoo.
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15
Pferdeheilkunde
KerstinMedenbach
Dr. HeikeAupperle
Doris Schoon
Prof. Dr. H.-A. Schoon
In stitut für Veterinär-PathoIoqie
UniversitätLeipzig
An den Tierkliniken33
D 04103 Leipzig
Tel.:0049 341 973 82 77
Fax:0049341 973 82 99
567