DOI:10.2214/AJR.07.3183
AJR 2008; 190:W278-W282
© American Roentgen Ray Society
Bilateral Hydrosalpinx in Adolescent Girls with Hirschsprung's Disease: Association of Two Rare Conditions
Laura Merlini1,
Mehrak Anooshiravani1,
Barbara Peiry2,
Giorgio La Scala2 and
Sylviane Hanquinet1
1 Unit of Pediatric Radiology, University Hospital, HUG 6, Willy-Donzé,
1205 Geneva, Switzerland.
2 Clinic of Pediatric Surgery, University Hospital, Geneva, Switzerland.
Received September 19, 2007;
accepted after revision November 28, 2007.
WEB
This is a Web exclusive article.
Address correspondence to L. Merlini
(laura.merlini{at}hcuge.ch).
Abstract
OBJECTIVE. The purpose of our study was to illustrate three cases of
bilateral hydrosalpinx in postpubertal girls operated on for Hirschsprung's
disease and to discuss the possible cause: iatrogenic or congenital. We
identified bilateral hydrosalpinx in three postpubertal sexually inactive
girls with Hirschsprung's disease treated, respectively by Duhamel, Soave
pull-through, and Martin procedures. No history of surgical complications or
pelvic inflammation had been reported.
CONCLUSION. Hirschsprung's disease is rare in girls and bilateral
hydrosalpinx is also extremely uncommon in sexually inactive adolescents. We
think there may be a possible common cause: either a postsurgical complication
or a congenital defect of the autonomous innervation in the context of a
neurocristopathy. Because of the rarity of both conditions, the association is
unlikely to be coincidental. The cause of this association is unclear and
further studies are required to find its prevalence and to estimate the
possible impact on fertility.
Keywords: Hirschsprung's disease • hydrosalpinx • neurocristopathy • surgical complication
Introduction
This article reports on three sexually inactive adolescent girls with
Hirschsprung's disease who underwent surgical treatment at a young age and who
developed bilateral hydrosalpinx in the postpubertal period. Both conditions,
Hirschsprung's disease and bilateral hydrosalpinx, are rare in girls; this
association is therefore unlikely to be a coincidence. We discuss two
potential hypotheses for this finding, a postsurgical complication or a newly
described associated abnormality of Hirschprung's disease in the context of a
neurocristopathy.
Cases
Case 1
A 12-year-old girl presented with a 2-day history of acute right pelvic
pain. Segmentary colon Hirschsprung's disease had been diagnosed when she was
5 years old on the basis of long-standing constipation. A Duhamel-type
pull-through procedure (Fig.
1A) was performed at that stage. No postoperative abdominal
complication was reported. Menarche was 3 months before admission. She was not
sexually active. Abdominal sonography showed signs of appendicitis and no
peritoneal fluid; the uterus and ovaries were normal, but a fluid-filled
tubular structure with folds in the left adnexal region
(Fig. 1B) and a more-complex
mass on the right side were observed (Figs.
1C and
1D). These findings were
confirmed by laparoscopy that was performed for appendectomy. The
postoperative course was uneventful. The patient was lost at follow-up.
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Fig. 1A —12-year-old girl with rectosigmoid Hirschsprung's disease
treated by Duhamel procedure. Drawing shows healthy bowel in green and
unhealthy bowel in red. Blue line indicates bladder catheter.
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Fig. 1B —12-year-old girl with rectosigmoid Hirschsprung's disease
treated by Duhamel procedure. Pelvic sagittal sonogram shows fluid-filled
tubular structure with folds on left side (internal echoes due to
reverberation artifacts).
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Fig. 1C —12-year-old girl with rectosigmoid Hirschsprung's disease
treated by Duhamel procedure. Parasagittal sonograms show complex
heterogeneous mass on right side with beaked appearance (D).
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Fig. 1D —12-year-old girl with rectosigmoid Hirschsprung's disease
treated by Duhamel procedure. Parasagittal sonograms show complex
heterogeneous mass on right side with beaked appearance (D).
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Case 2
An 11-year-old girl underwent abdominal sonography for annual follow-up of
Wilms' tumor. Menarche had occurred 2 months earlier. Immediately after birth,
segmentary rectosigmoid Hirschsprung's disease had been diagnosed. Left
colostomy was performed when she was 5 days old followed by a Soave-type
pull-through procedure (Fig.
2A) at 7 months old. She continued to suffer from persistent
soiling, and sphincterotomy by posterior access was performed when she was 7
years old. Chronic constipation and soiling were nevertheless still reported.
She was diagnosed with Wilms' tumor of the right kidney at 9 years old. Right
nephrectomy and regional and retroperitoneal lymphadenectomy were performed,
followed by radiation therapy (10.5 Gy on the right flank but not on the
pelvis) and chemotherapy (vincristine, dactinomycin, and doxorubicin).
Multiple follow-up sonographic examinations during childhood did not show any
genital organ ano malies. No intestinal obstruction was reported despite
multiple surgical procedures and irradiation. Pelvic sonography showed no
genitourinary abnormalities, and fluid-filled tubular structures folded on
themselves to form a C or an S shape (Fig.
2B), consistent with hydrosalpinx. MRI including sagittal
T2-weighted images (Fig. 2C)
showed plicae, or folds, that are typical of hydrosalpinx. T1-weighted
contrast-enhanced images (Fig.
2D) showed enhancement of the tubal walls, ruling out complete
tubal torsion. Moreover, absence of hyperintensity of tubal contents on
T1-weighted imaging, ruled out hematosalpinx. Sonographic examination 9 months
later confirmed bilateral hydro salpinx. Oral contraceptive medication was
prescribed to improve dysmenorrhea. Five months later, sonographic examination
showed a reduction in dilatation of the fallopian tubes.
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Fig. 2A —11-year-old girl with rectosigmoid Hirschsprung's disease
treated by Soave procedure. Drawing shows ganglionated bowel in green and
aganglionated bowel in red. Blue line indicates bladder catheter.
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Fig. 2B —11-year-old girl with rectosigmoid Hirschsprung's disease
treated by Soave procedure. Pelvic axial plane sonogram shows fallopian tubes
as fluid-filled tubular structures folded on themselves.
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Case 3
Pelvic sonography was performed on a 16-year-old girl before surgery for
nonobstructive cribriform hymen to rule out associated genital malformations.
A Martin procedure for total colonic Hirschsprung's disease diagnosed at birth
(Fig. 3A) was performed when
she was 1 year old. A paraanal abscess had complicated the postsurgical
period. Sphincterotomy for insufficient opening of the anal sphincter was
performed when she was 4 years old. No obstructions or subacute obstructions
were reported. Onset of menarche occurred 12 months before the diagnosis of
hydrosalpinx. Menstrual cycles were painless and regular. Sonography showed
bilateral paraovarian heterogeneous masses with cystic components and no
evidence of folds (Figs. 3B
and 3C). The ovaries and
uterus were normal. MRI was performed. Coronal T2-weighted sequences showed
dilated fallopian tubes with a folded appearance
(Fig. 3D), typical findings of
hydrosalpinx. Contrast-enhanced T1-weighted sequences showed enhancement of
the tubal walls. Oral contraceptive medication was prescribed. One year later,
bilateral hydrosalpinges disappeared.
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Fig. 3A —16-year-old girl with total colonic Hirschsprung's disease
treated by Lester Martin procedure. Drawing shows aganglionated bowel in red
and common channel with side-to-side ileocolic and ileorectal anastomosis to
normal bowel in green. Blue line indicates bladder catheter.
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Fig. 3B —16-year-old girl with total colonic Hirschsprung's disease
treated by Lester Martin procedure. Axial (B) and sagittal (C)
sonograms show bilateral paraovarian complex masses. Sagittal image (C)
shows fluid in tubes (internal echoes result from reverberation artifacts)
with no clear folds inside.
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Fig. 3C —16-year-old girl with total colonic Hirschsprung's disease
treated by Lester Martin procedure. Axial (B) and sagittal (C)
sonograms show bilateral paraovarian complex masses. Sagittal image (C)
shows fluid in tubes (internal echoes result from reverberation artifacts)
with no clear folds inside.
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Discussion
Hydrosalpinx develops due to a blocked, dilated, fluid-filled fallopian
tube. Sonography, showing fallopian tubes as fluid-filled tubular structures
folded on themselves to form a C or S shape, with longitudinal folds and
separated from the ovaries, is consistent with hydrosalpinx and helps to
distinguish it from a septated ovarian cystic mass that is usually round
[1] (Figs.
1B and
2B). When the elongated nature
of these folds is not recognized, they may be mistaken for mural nodules of an
ovarian cystic mass (Fig. 3B).
In this case, MRI helps distinguishing between a hydrosalpinx and a cystic
ovarian mass (Fig. 3D).
T1-weighted images are also useful to rule out endometrioma, which can be a
cause of hydrosalpinx (hyperintense lesions on T1-weighted images)
[2]. Gadolinium uptake can be
useful in symptomatic patients to differentiate simple hydrosalpinx from
torsion with infarction [2]
(Fig. 2D).
The differential diagnosis also includes peritoneal inclusion cyst,
paraovarian cyst, loculated ascites, and fallopian tube neoplasm. The aspect
of folds may help distinguish between peritoneal adhesions and hydrosalpinx,
given that in adhesions they would cross the entire width of a fluid
collection whereas in hydrosalpinx they cross partially. Paraovarian cysts are
different because they usually appear as single or multiple cysts separate
from the ovary with no septa or folds. In loculated ascites (pseudocysts)
there are no walls because contours are formed by surrounding anatomic
structures. This may be well shown by contrast-enhanced T1-weighted images
[3]. Tubal tumors in
adolescents are exceedingly rare and imaging procedures (sonography and MRI)
are helpful to depict solid components and vascularization.
Bilateral hydrosalpinx is extremely rare in adolescents without
inflammatory disease. The only case report we could find in the literature was
due to endometriosis [4]. A
further case was presented by C. Durand et al. at the 2000 annual congress of
the French Society of Pediatric Radiology in which they report on bilateral
hydrosalpinges as a postoperative complication in a 17-year-old girl with
bladder extrophy.
In our patients, pelvic inflammatory disease was ruled out because the
patients were not sexually active and because they each lacked clinical signs
and symptoms of active infection. One of our patients (case 2) received
radiation therapy on the right flank for Wilms' tumor. The pelvis was not
included in the field of radiation. To our knowledge, there have been no
reported cases of bilateral hydrosalpinges secondary to complications of
radiation therapy. A cause of hydrosalpinx in adults and probably in
adolescents is endometriosis. This hypothesis was ruled out by laparoscopy in
one case and by MRI, which showed no signs of hematosalpinx, in the two
others.
These are the first reports to our knowledge of bilateral hy drosalpinges
in postpubertal girls who were treated for Hirschsprung's disease during early
infancy. Hirschsprung's disease is rare in girls, occurring in one in 20,000.
We believe that, because of the rarity of these two conditions, our findings
are unlikely to be coincidental. Thus we speculate that there is a possible
common cause.
It may be speculated that bilateral hydrosalpinges is a complication of
Hirschsprung's disease surgery. The hypothesis of postsurgical adhesions
cannot be ruled out, but this seems rather unlikely because of the lack of
further, more common, manifestations such as bowel obstruction.
Innervation of the fallopian tubes consists of sympathetic and
parasympathetic nerves originating from the mesenteric plexus and from the
renal plexus. Furthermore, the uterovaginalis plexus from the hypogastric
inferior plexus, which originates from the sacral cord, also innervates the
fallopian tubes. It is well known that loss of adrenergic innervation induces
hydrosalpinx, as shown in the rabbit
[5]. Thus, postsurgical
impairment of fallopian tube adrenergic nerves may explain our findings.
Posterior wall proprioceptive nerves can possibly be injured during blunt
dissection for the creation of a retrorectal–presacral passage for the
surgical pull-through in Duhamel and Martin procedures (cases 1 and 3). In the
Duhamel procedure (Fig. 1A), a
surgical stapler is used to connect posterior ganglionic bowel and anterior
aganglionic bowel with a side-to-side anastomosis in a sagittal plane.
Proprioceptive nerves are preserved in the anterior wall of the rectum but
possibly not in the posterior wall. The anterior pelvic extrarectal nerves to
the bladder are protected.
The Martin procedure (Fig.
3A) was used for total colonic Hirschsprung's disease. It consists
of the construction of an extended common channel, a long side-to-side
anastomosis between the normal ileus and aganglionic colon and rectum. On the
other hand, the risk of injury to fallopian tube innervation is unlikely for
the Soave pull-through procedure because this technique consists of pulling
ganglionated bowel through the aganglionic muscular cuff of the rectum and
leaving the outer wall of the colon and the surrounding structures untouched
(Fig. 2A). However, a small
percentage of patients have persistent functional insufficiency after
different kinds of pull-through surgeries. The most frequent alterations are
intestinal, but extraintestinal complications, such as enuresis
(0.5–9.7%) and alterations of bladder function have also been reported
[6,
7].
Many studies in the literature have raised the hypothesis that most of the
supposed postsurgical complications in Hirschsprung's disease are not
consequences of surgery but rather are due to preexisting pathologic
conditions such as impairment of interstitial cells of Cajal
[8] or intrinsic defects of
smooth muscle cells [9]. Also
supporting the hypothesis of a nonsurgical cause is the fact that there have
been no previous reports of hydrosalpinx in postsurgical cases such as repair
of high imperforate anus in girls.
Hirschsprung's disease is the consequence of defective migration of neural
crest cells to the colonic submucosa and is therefore considered a
neurocristopathy. Neurocristopathies are a group of diverse disorders
resulting from defective growth, differentiation, and migration of the neural
crest cells. These cells have a migration potential that involves them in the
embryogenesis of many distant tissues, such as the adrenal medulla, all
pigmentary cells of the body, and many peripheral and autonomic neural
structures. Many studies have described the numerous conditions associated
with Hirschsprung's disease [9]
due to neural crest cell impairment. Most of them are well-recognized
syndromes (e.g., Down, Goldberg-Shprintzen, and Waardenburg's syndrome); many
others are unusual and diverse combined associations with Hirschsprung's
disease. Autonomic dysfunction has been detected in a relatively high
percentage of children with allegedly isolated Hirschsprung's disease
[10,
11].
Our observations are likely to be a newly reported association with
Hirschsprung's disease. In the literature, there are many experimental studies
about nerve abnormalities outside the gut (i.e., auditory nerves)
[12], for instance, in mice
with neural crest defects
[13]. However, to our
knowledge, fallopian tubes have never been investigated in this context.
Because the role of hydrosalpinx in infertility is well established, we
have investigated data from the literature concerning sexual function and
specifically female fertility after operative procedures for Hirschsprung's
disease. In fact, relevant data are extremely scarce. Only one article reports
on patients with Hirschsprung's disease who were treated with the Swenson
operation: 80 were married and collectively had 146 children, but the study
did not report the percentage of male and female patients
[6]. The Swenson technique is a
pull-through procedure that consists of circumferential dissection of the
rectum from the abdomen with anastomosis of normal bowel to the low rectum,
requiring a significant amount of pelvic and perirectal dissection.
There are several limitations to our study. There is no pathologic proof of
the presence of dilated fallopian tubes in our cases of Hirschsprung's
disease. We report only three cases, and more data are required to understand
how common this association might be. However, the results of our observations
may have practical implications because the role of hydrosalpinx in
infertility is well established. In adolescent girls with Hirschsprung's
disease, the possibility of hydrosalpinx should be considered especially in
the setting of unexplained pelvic pain using pelvic sonography as a first-line
technique.
Conclusion
This is the first report to our knowledge of the association of
Hirschsprung's disease and bilateral hydro salpinx. Because of the rarity of
both conditions, their association is unlikely to be coincidental. At present,
the hypothesis that hydrosalpinx is a postsurgical complication that may
manifest only after the onset of tubal fluid production at menarche is the
least likely, above all for the patient who underwent a Soave procedure. Our
observations could be a newly reported association with Hirschsprung's disease
in the context of a neurocristopathy. Long-term studies of adolescent girls
with Hirschsprung's disease are needed to ascertain the prevalence of the
association with hydrosalpinx and its effects on fertility.
Acknowledgments
We thank Martin Tramer for his editorial assistance in the preparation of
the manuscript.
References
- Sacher P, Meuli M. Laparoscopic removal of hydrosalpinx in a girl:
case report. Eur J Pediatr Surg 1997;7
: 239–240[Medline]
- Outwater EK, Siegelman ES, Chiowanich P, Kilger AM, Dunton CJ,
Talerman A. Dilated fallopian tubes: MR imaging characteristics.
Radiology 1998;208
: 463–469[Abstract/Free Full Text]
- Jain KA. Imaging of peritoneal inclusion cysts.
AJR 2000; 174:1559
–1563[Free Full Text]
- Stavroulis AI, Saridogan E, Creighton SM, Cutner AS. Laparoscopic
treatment of endometriosis in teenagers. Eur J Obstet Gynecol
Reprod Biol 2006; 125:248
–250[CrossRef][Medline]
- Donnez J, Caprasse J, Casanas-Roux F, Ferin J, Thomas K. Loss of
adrenergic innervation in induced rabbit hydrosalpinx. Gynecol
Obstet Invest 1986; 21:213
–216[Medline]
- Hoehner JC, Ein SH, Shandling B, Kim PC. Long-term morbidity in
total colonic aganglionosis. J Pediatr Surg1998; 33:961
–965[CrossRef][Medline]
- Boemers TM, Bax NM, van Gool JD. The effect of rectosigmoidectomy
and Duhamel-type pull-through procedure on lower urinary tract function in
children with Hirschsprung's disease. J Pediatr Surg2001; 36:453
–456[CrossRef][Medline]
- Sandgren K, Larsson LT, Ekblad E. Widespread changes in
neurotransmitter expression and number of enteric neurons and interstitial
cells of Cajal in lethal spotted mice: an explanation for persisting
dysmotility after operation for Hirsch sprung's disease? Dig Dis
Sci 2002; 47:1049
–1064[CrossRef][Medline]
- Wedel T, Van Eys GJ, Waltregny D, Glénisson W, Castronovo V,
Vanderwinden JM. Novel smooth muscle markers reveal abnormalities of the
intestinal musculature in severe colorectal motility disorders.
Neurogastroenterol Motil 2006;18
: 526–538[CrossRef][Medline]
- Amiel J, Lyonnet S. Hirschsprung disease, associated syndromes, and
genetics: a review. J Med Genet 2001;38
: 729–739[Abstract/Free Full Text]
- Staiano A, Santoro L, De Marco R, et al. Autonomic dysfunction in
children with Hirschsprung's disease. Dig Dis Sci1999; 44:960
–965[CrossRef][Medline]
- Cheng W, Au DK, Knowles CH, Anand P, Tam PK. Hirschsprung's
disease: a more generalised neuropathy? J Pediatr Surg2001; 36:296
–300[CrossRef][Medline]
- Schrott A, Melichar I, Popelár J, Syka J. Deterioration of
hearing function in mice with neural crest defect. Hear
Res 1990; 46:1
–7[CrossRef][Medline]
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Abstract
Introduction
