Xanthogranulomatous salpingitis and oophoritis: a case report and review of the literature.

Reprints: Yulia Gray, MD, Department of Pathology, Roger Williams Medical Center, 825 Chalkstone Ave, Providence, RI 02908. From the Department of Pathology, Rhode Island Hospital and Brown University School of Medicine, Providence, RI (Dr Gray), and Department of Pathology, Roger Williams Medical Center, Providence, RI, and Boston University School of Medicine, Boston, Mass (Dr Libbey). From the Department of Pathology, Rhode Island Hospital and Brown University School of Medicine, Providence, RI (Dr Gray), and Department of Pathology, Roger Williams Medical Center, Providence, RI, and Boston University School of Medicine, Boston, Mass (Dr Libbey). A case of xanthogranulomatous salpingitis and oophoritis in a 47-year-old woman is presented. Xanthogranulomatous inflammation is an uncommon form of chronic inflammation that is destructive to affected organs; it is characterized by the presence of lipid-filled macrophages with admixed lymphocytes, plasma cells, and neutrophils. Only a few cases of xanthogranulomatous salpingitis and oophoritis have been reported to date. The case presented here is associated with Escherichia coli infection, endometriosis, and an intrauterine device. The presence of a large number of lipid-containing macrophages with an admixture of lymphocytes, plasma cells, and neutrophils is characteristic of xanthogranulomatous inflammation. Multinucleated giant cells may be present. Xanthogranulomatous inflammation is a form of chronic inflammation that is destructive to the normal tissue of affected organs.1–4 This is an uncommon process best known to occur in the kidney.4–7 Other organs in which xanthogranulomatous inflammation has been reported are the gallbladder, stomach, anorectal area, bone, urinary bladder, testis, epididymis, vagina, endometrium, ovary, and fallopian tube.1,3,4,8–15 We report a case of xanthogranulomatous salpingitis and oophoritis in a 47-year-old woman. REPORT OF A CASE A 47-year-old woman, married and a mother of one child, presented with a several-month history of intermittent severe sharp abdominal pain localized to the left suprapubic region, which also occurred with intercourse. The onset of these symptoms coincided with an upper respiratory infection with cough, minimal sputum, nausea, anorexia, and multiple loose stools. At that time, she developed a low-grade fever but was subsequently afebrile. The patient was noted to have a Trichomonas infection, and she and her husband were treated with metronidazole. However, her symptoms persisted. She had had an intrauterine device (IUD) for 9 years and experienced an episode of pelvic inflammatory disease after the IUD was first inserted. The patient's medical history was otherwise unremarkable. Her physical examination revealed fullness and tenderness in the left suprapubic region. Laboratory tests showed a hemoglobin level of 119 g/L, a white blood cell count of 8.3 × 109/L with a normal differential, and an erythrocyte sedimentation rate elevated to 91 mm/h. Pelvic ultrasound revealed no masses. A computed tomographic scan of the abdomen disclosed a bilobed mass in the left adnexal region measuring 5 × 4 × 3 cm, which was thought to represent either an inflammatory mass, an ovarian cyst, or an ovarian neoplasm. The IUD was removed. The patient underwent a total abdominal hysterectomy and bilateral salpingo-oophorectomy without complications. During the surgery, it was noted that the left adnexal structures were involved with a 5- to 7-cm mass adherent to the rectum. A small amount of purulent fluid was extruded and cultured. The culture grew Escherichia coli. MATERIALS AND METHODS The specimen was fixed in 10% buffered formalin, processed by routine methods, and stained with hematoxylin-eosin and periodic acid–Schiff, Gram, methenamine silver, acid-fast bacilli, and Steiner stains. PATHOLOGIC FINDINGS The specimen consisted of a uterus with attached cervix and bilateral fallopian tubes and ovaries weighing 110 g. The uterus measured 7.0 × 4.0 × 1.5 cm. The right ovary measured 2.0 × 1.0 × 1.0 cm, and the right fallopian tube was 5.0 × 1.0 cm. The left ovary measured 4.0 × 3.0 × 2.5 cm, and the left fallopian tube, 7.0 × 0.7 cm. The external surface of the ovaries, fallopian tubes, and part of the uterus was hemorrhagic. Dense tubo-ovarian adhesions appeared bilaterally, more prominent on the left. A maroon cyst was found below the right ovary, measuring 1.5 × 1.2 × 1.0 cm. The cut surface of the right ovary showed a hemorrhagic cyst consistent with corpus luteum. The left ovary adhered to the uterus. The cut surface of the left ovary revealed an abscess, lined by a yellow granular wall and containing yellow cloudy fluid (Figure 1). The cavity of the abscess measured 2.0 × 1.0 × 1.0 cm. A cross section of the left fallopian tube showed an enlarged lumen with yellow papillary structures (Figure 2). There was an increased amount of fibrous and adipose tissue below the left ovary, alongside the uterus. The uterus contained 2 white mural nodules, which were 0.6 and 0.5 cm in greatest dimensions. The endometrium was slightly hemorrhagic, measuring 0.1 cm thick. Histopathologic examination of the fallopian tubes showed infiltration of the lamina propria by histiocytes with abundant hemosiderin-laden cytoplasm with a mixture of inflammatory cells, including lymphocytes, plasma cells, and occasional neutrophils (Figures 3 and 4). There were also chronic inflammatory cells in the muscularis propria, and there was subserosal fibrosis and chronic inflammation with focal adhesions. The lumen contained numerous histiocytes and neutrophils. Many of the histiocytes in the lamina propria appeared to contain abundant lipid material. A similar reaction was present in the left ovary surrounding an abscess cavity containing purulent exudate and surrounded by dense fibrosis and chronic inflammation. There were fibrinous and fibrous adhesions on the ovarian surface. No Michaelis-Gutmann bodies were identified, and stains for microorganisms, including periodic acid–Schiff, methenamine silver, acid-fast bacilli, Gram, and Steiner stains, were negative. A small focus of endometriosis was present in the adipose tissue adherent to the adnexa and uterine wall. No significant inflammation was identified in the endometrium, but the cervix showed chronic inflammation and squamous metaplasia. These findings were diagnostic of xanthogranulomatous salpingo-oophoritis with left ovarian abscess. COMMENT Seven cases of xanthogranulomatous salpingitis, 3 cases of xanthogranulomatous oophoritis, and 4 cases of xanthogranulomatous salpingitis and oophoritis have been reported to date,2,12,13,16–22 some under other diagnoses, such as xanthomatous salpingiosis, tubal xanthomatosis, xanthogranuloma of the ovary, and pelvic inflammatory pseudotumor. They have in common foamy histiocytes, mixed inflammatory infiltrate, and occasional foreign body or Touton giant cells. Several similar reported cases, sufficiently different histologically from xanthogranulomatous salpingitis and oophoritis, are not included in this list. One report described necrotic pseudoxanthomatous nodules of the ovary in patients with ovarian endometriosis.23 In another report, a patient with squamous cell carcinoma of the cervix developed “pigmentosis tubae,” thought to be due to cellular damage caused by radiotherapy and considered to be similar to melanosis coli.24 In another article, the authors suggested their patients had a form of old endometriosis rather than salpingitis.25 Patients with xanthogranulomatous salpingitis and oophoritis in previously reported cases ranged from 23 to 72 years old. Presenting complaints were lower abdominal or suprapubic pain (sometimes unilateral), fever, menorrhagia, or vaginal bleeding. On physical examination, there was adnexal tenderness and a pelvic mass.2,12,13,16–22 The pathogenesis of xanthogranulomatous inflammation remains unclear. Many unrelated disorders may have the same mechanism of foam cell production26; proposed causes are infection, ineffective antibiotic therapy, abnormality in lipid metabolism, endometriosis, and ineffective clearance of bacteria by phagocytes.4,19,21 A combination of factors may be responsible. For example, bleeding and obstruction may predispose to infection13,21; tissue necrosis occurs, followed by the release of cholesterol and other lipids and phagocytosis by macrophages.20 Malakoplakia, a form of chronic granulomatous inflammation, can involve a variety of organs, most frequently the urinary tract, but it rarely affects the female genital tract. It is recognized by the presence of calcified cytoplasmic or extracytoplasmic lamellar spherules called Michaelis-Gutmann bodies.27 Because of the presence of foamy histiocytes, malakoplakia should be considered in the differential diagnosis of xanthogranulomatous inflammation. Walther et al28 have suggested that malakoplakia and xanthogranulomatous inflammation may have a common pathogenesis. Malakoplakia is thought to result from a deficit in the ability of phagocytes to kill microorganisms,27,29 possibly due to diminished release of β-glucuronidase and low levels of cyclic guanosine monophosphate.30 Michaelis-Gutmann bodies are thought to arise from phagolysosomes, which contain partly digested bacteria.31 Escherichia coli is commonly implicated. No Michaelis-Gutmann bodies were identified in the present case, thus this is not a case of malakoplakia, but the similarities between xanthogranulomatous inflammation and malakoplakia are worth noting. Xanthogranulomatous salpingitis and oophoritis may have an infectious etiology. In some cases, including the present case, the patients had a history of pelvic inflammatory disease.12,18 In several cases bacteria, including Bacteroides fragilis, E coli, Proteus vulgaris, and Salmonella typhi grew from bacterial cultures.12,13,20,22 Bacteria have also been associated with xanthogranulomatous inflammation in other organs.5,6,7,10,14 Escherichia coli was cultured from ovarian abscess fluid in the present case. Other associations include antibiotic treatment,19,21,22 cervical stenosis,13,20 and endometriosis.21,22 There has been no association of xanthogranulomatous salpingitis and oophoritis with malignancy or radiotherapy, as exists in other organs.11,15 An association does exist between the use of intrauterine contraceptive devices, pelvic inflammatory disease, and unilateral or bilateral tubo-ovarian abscess, one of the most serious complications of pelvic inflammatory disease.32–36 Associated microorganisms include Actinomyces,35 Staphylococcus aureus,32,33,36 Streptococcus (Enterococcus) faecalis,32 E coli,33,36 viridans streptococci, B fragilis, Torulopsis (Candida) glabrata, and group B streptococci.36 It is thought that the colonization of the IUD in the endometrial cavity is followed by the shedding of bacteria through the lumen of the fallopian tube. Ruptured ovarian surface is exposed to bacteria at the time of ovulation. The corpus luteum becomes infected, producing an ovarian abscess.36 The present case is consistent with other reported cases of xanthogranulomatous salpingitis and oophoritis in its presentation, history of infection, and antibiotic treatment. The patient did not have a workup for abnormal lipid metabolism, nor did her history give an indication of any immunodeficiency. Although not found in fallopian tubes or ovaries, endometriosis was present in soft tissue adherent to the uterus and adnexa. Histologic findings were also characteristic of xanthogranulomatous inflammation. This patient had an episode of pelvic inflammatory disease when her IUD was first inserted, 9 years prior to admission. It is possible that the patient's left fallopian tube and ovary became infected with E coli at that time, the infection was partially treated, and subsequent changes resulted in xanthogranulomatous inflammation. Whether it is etiologic or not is uncertain, but to our knowledge, this is the first reported case of xanthogranulomatous oophoritis and salpingitis associated with the use of an IUD. Copyright: College of American Pathologists 2001 Figure 1. Gross appearance of xanthogranulomatous oophoritis. Cut surface of the left ovary shows an abscess with a yellow granular lining containing yellow cloudy fluid.Figure 2. Gross appearance of xanthogranulomatous salpingitis. Cross section of the left fallopian tube shows dilated lumen with enlarged yellow plicae.Figure 3. Tubal plica filled with lipid-containing macrophages (hematoxylin-eosin, original magnification ×25).Figure 4. Lipid-containing macrophages and mixed inflammatory infiltrate (hematoxylin-eosin, original magnification ×100).