Hum. Reprod. Advance Access originally published online on September 7, 2006
Human Reproduction 2007 22(1):272-274; doi:10.1093/humrep/del352
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Endometriosis involving the ileocaecal junction with regional lymph node involvement in the baboon—striking pathological finding identical between the human and the baboon: A Case Report
1 Department of Obstetrics, Gynecology and Women’s Health, Division of Reproductive and Perinatal Research, University of Missouri, Columbia, MO and 2 Veterinary Resources, Southwest National Primate Research Center, Southwest Foundation for Biomedical Research, San Antonio, TX, USA
3 To whom correspondence should be addressed at: Division of Research, N625 HSC, One Hospital Drive, Columbia, MO 65212, USA. E-mail: barrierb{at}health.missouri.edu
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Abstract |
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The baboon is an established model for endometriosis research. This report describes the occurrence of spontaneous endometriosis involving the ileocaecal junction and associated regional lymph nodes in the baboon. All endometriotic foci lacked the nuclear atypia, abnormal mitotic activity and altered nuclear-to-cytoplasmic ratio typical of malignancy. These findings are identical to reports in the human in which ileocaecal and colonic endometriosis is associated with endometriosis in pericolonic and mesenteric lymph nodes. The similarity between baboon and human colonic endometriosis in both location and pathology is striking and lends further evidence supporting the validity of the baboon as a model for human endometriosis.
Key words: baboon/bowel/colon/endometriosis/lymph node
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Introduction |
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Endometriosis is a potentially painful condition in women in which endometrium is found inside the peritoneal cavity, adherent to or penetrating the mesothelial surface of the body wall or pelvic/abdominal organs in a gravity-dependent manner. Pelvic endometriosis occurs in
6–10% of the general female population; in women with pelvic pain or infertility, its frequency may be as high as 50% (Houston et al., 1988
; Eskenazi and Warner, 1997; Cramer and Missmer, 2002). Endometriosis is less commonly encountered in the ovaries or rectovaginal septum and infrequently found to involve the colon or appendix. Lymph node involvement of endometriosis is also rarely reported, and it most often coexists with endometriosis of the bowel (Cameron et al., 1995; Insabato and Pettinato, 1996; Sheikh et al., 2005; Thomakos et al., 2006).
The baboon is an established model for endometriosis research (D’Hooghe, 1997; Fazleabas et al., 2002). It has monthly menstrual cycles, spontaneous menses and pelvic anatomy similar to the human and develops spontaneous endometriosis with a prevalence that increases with duration of captivity. After more than 2 years in captivity, the prevalence of biopsy-proven endometriosis is as high as 27% (D’Hooghe et al., 1996a). In established multigenerational breeding colonies, the prevalence has been reported as high as 60% in infertile animals (Barrier et al., 2004). Also in large, established colonies, many cases of severe disease are encountered at the time of necropsy (Dick et al., 2003).
Endometriosis of the para-aortic lymph nodes has been reported once before in Papio doguera, although it was mentioned as a side-note in this third ever reported case of endometriosis in the baboon (Folse and Stout, 1978). The present case is the first description of ileocaecal endometriosis with regional lymph node involvement and bears a striking resemblance to a recent human case report (Sheikh et al., 2005). With aid in interpretation by a large body of developing literature describing endometriosis in the baboon, such pathological similarity serves to reinforce the validity of the baboon as a model for understanding human endometriosis.
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Case Report |
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We report on a 25-year-old female baboon dam who was born on 28 December 1984 at the Southwest Foundation for Biomedical Research in San Antonio, TX, USA. She had been placed in breeding at age 4 and achieved pregnancy at 9 years of age, an abnormally long duration of time with no pregnancy. On 27 July 1994, she delivered a live born female infant by vaginal delivery. Her offspring was fertile and bore her four grandchildren between 1999 and 2001. After this, the dam never again achieved a pregnancy. Over her lifetime following her pregnancy, she was exposed to at least three fertile males—the first for 28 months and the two remaining males each for 1 week—for a total documented duration of exposure of 28.5 months. She was also exposed to males without proven fertility for an additional 21 months. It is possible that additional undocumented exposures to fertile males occurred, but records may not be complete. The reason that this is suspected is that the baboons are rarely kept in individual cages, and in the group setting, a male is usually present with a harem. We can only account for 49 months of this animal’s life exposure to males through available documentation, and it is improbable that the remaining 17 years of this baboon’s life were spent apart from a harem.
On 26 October 2005, the elderly dam appeared pale, moving slowly in her outside cage, with abdominal bloating and a crusty nasal discharge. She was sedated and examined, and a palpable lower abdominal mass was appreciated. Blood urea nitrogen was 79 mg/dl, and creatinine was 5.2 mg/dl. She was diagnosed with acute renal failure and sepsis and was euthanized, as per clinical protocol. All animal handling was performed in accordance with stringent Southwest Foundation for Biomedical Research Institutional Animal Care and Use Committee guidelines.
Gross evaluation revealed normal muscle mass, normal hydration, adequate adipose tissue and a distended abdomen. On entry into the abdomen, the abdominal viscera and pelvic organs were adhered to one another and to the abdominal wall. A gross photograph of the densely adhered abdominal viscera is seen in Figure 1. There was 60 ml of bloody fluid within the peritoneal cavity, surrounded by a dense coating of diffuse fibrosis and haemorrhage consistent with the presence of a massive pelvic endometrioma. The ovary was not directly involved. A gross photograph of the endometrioma and relationship to pelvic structures is seen in Figure 2. The lining of the pelvic endometrioma was contiguous with a 2 x 2-cm firm mass noted within the bowel wall on the mesenteric side of the ileocaecal junction.
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Microscopic evaluation of the pelvic endometrioma and of the bowel wall nodule stained with hematoxylin and eosin revealed well-differentiated endometrial epithelium and stroma present in each. This nodule predominantly involved the caecum and included a portion of the ileum and proximal colon. The nodule involved adipose tissue, serosa and muscularis of the intestine, but intestinal mucosa was not involved. Three different 0.5-cm to 1-cm mesenteric lymph nodes also contained multiple foci of endometriosis on microscopic examination (see Figure 3). All endometriotic foci lacked the nuclear atypia, abnormal mitotic activity and altered nuclear-to-cytoplasmic ratio typical of malignancy. The mucosa, muscularis and serosa of the ileum were expanded by a marked infiltrate of neutrophils, fewer macrophages and oedema. This enteritis was judged to result from a local effect of endometriotic invasion, and intestinal perforation appears to have resulted in the development of septicaemia as evidenced by the observed peritonitis, pleuritis and meningitis. The dam had no evidence of hydronephrosis or ureteral obstruction.
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Discussion |
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We here report the first identified case of ileocaecal endometriosis with lymph node involvement in the baboon. This case bears striking resemblance to a recently reported case of ileocaecal endometriosis with lymph node involvement in the human (Sheikh et al., 2005
). In both cases, benign endometrial epithelium and stroma were found in the caecal wall and in draining lymph nodes. In neither case was there evidence of malignancy.
Extensive endometriosis in the baboon has been infrequently reported, primarily limited to earlier literature because of the obvious nature of the disease in these cases. These early reports contain a common element of dense pelvic and abdominal adhesions and large pelvic endometriomata containing up to 500 ml of dark bloody fluid (Folse and Stout, 1978; DaRif et al., 1984).
A large body of literature has since developed to describe the behaviour of endometriosis in the baboon—beginning with a 1991 landmark article by Dr D’Hooghe in which spontaneous mild endometriosis was frequently found in captive animals (D’Hooghe et al., 1991). The overwhelming preponderance of this literature is concerned with mild to moderate endometriosis. Absent are data exploring risk factors for the development of extensive endometriosis such as that described in this case report. Although it remains to be proved, risk factors for extensive disease may perhaps be similar to those noted for the development of milder endometriosis, amplified by longer duration of exposure. Such an hypothesis may help to explain why extensive endometriosis is rarely encountered in the baboon, but encountered more frequently in large established breeding centres (Dick et al., 2003).
Common risk factors for endometriosis in baboons include the duration of captivity and hence the number of menstrual cycles uninterrupted by pregnancy (D’Hooghe et al., 1996a); the performance of serial laparoscopy (D’Hooghe et al., 1996b) which monitors the natural progression of the disease and potentially augments this progression by inducing pelvic inflammation (D’Hooghe et al., 1999); and increased prevalence of retrograde menstruation in baboons with endometriosis (D’Hooghe et al., 1996c).
The pathogenesis of endometriosis is still the subject of debate 80 years after Dr Sampson postulated that most endometriosis occurs by direct peritoneal seeding from retrograde menstruation (Sampson, 1927). The presence of endometriosis on the caecal serosa and within the caecal wall in this case suggests a route of direct spread from the pelvic endometrioma consistent with Sampson’s hypothesis. This is further reinforced by the presence of endometriotic foci within regional draining lymph nodes. We hypothesize that the proximity of the caecum to the pelvis is the most likely reason for its involvement in both the baboon and human cases.
The baboon has emerged as an ideal animal model for the study of both naturally occurring and induced endometriosis (D’Hooghe, 1997; Fazleabas et al., 2002). The presence of ileocaecal endometriosis with regional lymph node involvement is identical to similar disease reported in the human, lending further evidence to support the validity of the baboon as a model for human endometriosis.
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References |
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Submitted on June 15, 2006; resubmitted on July 28, 2006; accepted on August 4, 2006.
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