Incidental granulomatous inflammation of the uterus.
Background. Granulomas of the uterine corpus have been reported in a variety of pathologic conditions but are relatively rare findings in routine histopathologic material.
Methods. This retrospective clinicopathologic study reviewed patients diagnosed with uterine granulomas between 1980 and 1999 in a tertiary referral center.
Results. The study group was comprised of 11 women, ranging in age from 37 to 90 years. All patients had histologically confirmed, non-necrotizing granulomas. The most common symptom prompting biopsy or hysterectomy was abnormal bleeding. Several concomittant histopathologies were noted. Eight of 11 patients had a known history of uterine instrumentation. None of the patients had clinical evidence of sarcoidosis Sarcoidosis Definition
Sarcoidosis is a disease which can affect many organs within the body. It causes the development of granulomas. Granulomas are masses resembling little tumors. They are made up of clumps of cells from the immune system. or systemic infection, and stains for microorganisms were negative in all cases. Polarizable po·lar·ize
v. po·lar·ized, po·lar·iz·ing, po·lar·iz·es
1. To induce polarization in; impart polarity to.
2. To cause to concentrate about two conflicting or contrasting positions. or foreign materials were not seen.
Conclusions. Well-formed, non-necrotizing granulomas are an infrequent finding in the uterus. A history of instrumentation may explain the presence of granulomas in a subset of patients.
GRANULOMATOUS INFLAMMATION of the uterus is a relatively uncommon finding that previously has been attributed to a variety of conditions, including infection, sarcoidosis, foreign-body reactions, and surgical procedures. Our institution's experience with incidentally-found uterine granulomatous inflammation is reviewed here. The clinicopathologic features of these cases are described, and an attempt is made to define their etiologies.
METHODS AND MATERIALS
We searched the surgical pathology files at the Cleveland Clinic and found 11 cases of granulomatous inflammation involving the uterus diagnosed between 1980 and 1999. Each case was identified and confirmed by review of all microscopic slides. Routine histologic sections were generated from paraffin-embedded and formalin-fixed tissue, cut 4 microns thick and stained with hematoxylin-eosin. All sections containing granulomas were polarized A one-way direction of a signal or the molecules within a material pointing in one direction. and examined for evidence of foreign material. In all cases, stains for fungal (Gomori methenamine methenamine /meth·en·amine/ (meth?en-am´in) an antibacterial used in urinary tract infections; administered as the hippurate and mandelate salts.
n. silver stain) and mycobacterial mycobacterial
emanating from or pertaining to mycobacterium.
may be caused by Mycobacterium tuberculosis (see cutaneous tuberculosis), M. organisms (Ziehl-Neelsen stain) were done. Concomitant uterine pathologies were noted.
The medical record was reviewed in each case to obtain information regarding patient age, menopausal status, history of uterine instrumentation, surgical procedures performed, and follow-up information. Particular attention was paid to whether the patient had a systemic disease to explain the presence of granulomas in the uterus and whether the diagnosis of granulomatous inflammation of the uterus had any documented clinical impact on treatment or further laboratory testing of the patient.
Eleven women with incidental findings of granulomas involving the uterus comprised the study group. At the time of diagnosis, the patients ranged in age from 37 to 90 years (mean 53 years, median 49 years); 6 patients were premenopausal pre·me·no·paus·al
Of or relating to the years or the stage of life immediately before the onset of menopause.
premenopausal adjective and 5 were perimenopausal perimenopausal adjective Referring to a period of a ♀'s life–age 45 to 55-ish–in which menstrual periods become irregular; perimenopause is immediately before, during and after menopause. See Menopause. or postmenopausal post·men·o·paus·al
Of or occurring in the time following menopause.
postmenopausal Change of life Gynecology adjective Referring to the time in ♀ when menstrual periods stop for ≥ 1 yr . The most common clinical symptom prompting biopsy and/or surgery was uterine bleeding (n = 8); 1 of these 8 patients had a history of concomitant pelvic pain and another had a history of vaginal discharge. Of the remaining 3 patients, 1 presented with uterine prolapse, 1 with a pelvic mass, and the third with infertility. Eight of 11 patients had a known history of uterine instrumentation, which initially consisted of dilatation with curettage curettage /cu·ret·tage/ (ku?re-tahzh´) [Fr.] the cleansing of a diseased surface, as with a curet.
medical curettage in 4 patients, endometrial biopsies in 2 patients, hysterosalpingogram in 1 patient, and hysteroscopy in 1 patient. Four of these patients had more than one episode of instrumentation. One patient had an intrauterine device (IUD IUD Definition
An IUD is an intrauterine device made of plastic and/or copper that is inserted into the womb (uterus) by way of the vaginal canal. One type releases a hormone (progesterone), and is replaced each year. ) in place for 11 years before surgery.
None of the patients had a previous diagnosis of granulomas involving the uterus. There was no history of sarcoidosis or systemic infection with mycobacterial or fungal organisms.
Table 1 summarizes the clinicopathologic features of all 11 patients. They all had at least 1 identifiable granuloma granuloma /gran·u·lo·ma/ (gran?u-lo´mah) pl. granulomas, granulo´mata an imprecise term for (1) any small nodular delimited aggregation of mononuclear inflammatory cells, or (2) such a collection of modified macrophages of the uterus, involving the endometrium endometrium /en·do·me·tri·um/ (-me´tre-um) pl. endome´tria the mucous membrane lining the uterus.
n. pl. in 9 patients, the myometrium myometrium /myo·me·tri·um/ (-me´tre-um) the tunica muscularis of the uterus.myome´trial
The muscular wall of the uterus. in 1 patient, and the cervix in 1 patient (Figure). Four patients had more than one granuloma identified. One patient, who had pelvic lymph node exploration done at the time of hysterectomy for endometrial endometrial /en·do·me·tri·al/ (en?do-me´tre-il) pertaining to the endometrium.
n relating to the end-ometrium or cavity of the uterus. adenocarcinoma, was found to have non-necrotizing granulomas in several pelvic lymph nodes. In all cases, the granulomatous inflammation was non-necrotizing. There was no polarizable material or evidence of foreign bodies noted in any of the cases. All granulomas were stained for mycobacteria mycobacteria
members of the genus Mycobacterium.
see opportunist (atypical) mycobacteria (below).
see opportunist (atypical) mycobacteria (below). using Ziehl-Neelsen stain, and for fungi using Gomori methenamine silver stain; no organisms were identified in any of the specimens.
Surgical procedures included hysterectomy (either total abdominal or total vaginal) in 6 patients, endometrial biopsies in 4 patients, and endometrial curettage in 1 patient. Concomitant histopathologic findings included acute and chronic cervicitis cervicitis
Inflammation of the cervix of the uterus, caused by infection or irritation. It is most common during the years of menstruation. Cervicitis can be acute or chronic and may worsen during pregnancy. It does not cause pain but may lead to polyps. in 4 patients, squamous meta plasia of the endometrium in 3 patients, leiomyomata of the uterus in 3 patients, complex hyperplasia with or without atypia of the endometrium in 2 patients, endometrial adenocarcinoma in 2 patients, endometritis endometritis /en·do·me·tri·tis/ (-me-tri´tis) inflammation of the endometrium.
puerperal endometritis that following childbirth. in 2 patients, and atypical polypoid polypoid /pol·yp·oid/ (pol´i-poid) resembling a polyp.
Resembling a polyp.
resembling a polyp. adenomyoma in 1 patient, benign endometrial polyps in 1 patient, and adenomyosis adenomyosis /ad·e·no·my·o·sis/ (-mi-o´sis) benign ingrowth of the endometrium into the uterine musculature, sometimes with hypertrophy of the latter; if the lesion forms a circumscribed tumorlike nodule, it is called adenomyoma. in 1 patient. One patient had no significant concomitant pathologic findings in the endometrial biopsy specimen. Postoperative follow-up ranged from 1 to 5 years. There was no evidence of treatment or further laboratory testing because of the finding of granulomatous inflammation. None of the patients were later diagnosed with sarcoid sarcoid /sar·coid/ (sahr´koid)
2. a sarcoma-like tumor.
Of or resembling flesh.
1. , tuberculosis, or other systemic diseases that might have caused granulomas. One patient had rebiopsy for endometrial hyperplasia, and 1 patient had a subsequent hysteroscopy done as a follow-up for squamous metaplasia of the endometrium.
Table 2 summarizes a list of etiologies reported in the literature to be associated with granulomatous inflammation in the uterus. Infectious etiologies are commonly-reported causes of granulomatous inflammation in any organ system. Uterine involvement by tuberculosis is well documented, (1-5); it involves the endometrium and/or the cervix rather than the myometrium in most cases. (1) Mycobacterial infections, particularly tuberculosis, classically result in the formation of necrotizing necrotizing /nec·ro·tiz·ing/ (nek´ro-tiz?ing) causing necrosis.
Causing the death of a specific area of tissue. Human bites frequently cause necrotizing infections. granulomas; however, non-necrotizing granulomas can certainly be encountered in patients infected with Mycobacterium tuberculosis. All of the granulomas in the current study were non-necrotizing. It has been hypothesized that tuberculous tuberculous /tu·ber·cu·lous/ (too-ber´ku-lus) pertaining to or affected with tuberculosis; caused by Mycobacterium tuberculosis.
1. granulomas in the endometrium are sometimes not necrotic because of the turnover rate of these tissues as part of the normal menstrual cycle. (6,7) In nonendometrial tissue or in postmenopausal women, however, this would not be a factor and some evidence of caseous necrosis might be expected. Ziehl-Neelsen stains failed to show evidence of mycobacterial organisms in any of the cases in the current series. While this does not preclude the possibility of a mycobacterial infection, none of the patients showed systemic signs or symptoms of such an infection before examination of the uterine tissue or after surgery.
In addition to mycobacterial organisms, other infectious processes have been infrequently reported to be associated with the development of granulomatous inflammation in the uterus. (7-12) Some of these were parasitic diseases, such as schistosomiasis schistosomiasis (shĭs`təsōmī`əsĭs), bilharziasis, or snail fever, parasitic disease caused by blood flukes, trematode worms of the genus Schistosoma. or Enterobius vermicularis (pinworm pinworm, roundworm, Enterobius vermicularis, worldwide in distribution and the most common source of worm infestation of humans in the United States. Children are more commonly infested than adults. ) infection. (10-12) Rare examples of fungal infection, such as coccidiomycosis, have also been reported to be associated with granulomatous granulomatous /gran·u·lom·a·tous/ (-lom´ah-tus) containing granulomas.
Resembling a tumor made of granular material. endometritis. (9)
Evaluation of granulomatous inflammation should include staining for fungal organisms (eg, with Gomori methenamine silver stain), in addition to staining for mycobacterial organisms. Interestingly, rare cases of granulomatous uterine inflammation have also been attributed to viral infections. Frank et al (8) reported a case with multiple non-necrotizing granulomas in an endometrial curettage specimen, presumed to be viral in etiology No cytomegalovirus (CMV) inclusions were identified by light microscopic evaluation in that specimen; however, CMV inclusions were noted in an endocervical curettage specimen, and the organism was ultimately shown by polymerase chain reaction polymerase chain reaction (pŏl`ĭmərās') (PCR), laboratory process in which a particular DNA segment from a mixture of DNA chains is rapidly replicated, producing a large, readily analyzed sample of a piece of DNA; the process is in DNA DNA: see nucleic acid.
or deoxyribonucleic acid
One of two types of nucleic acid (the other is RNA); a complex organic compound found in all living cells and many viruses. It is the chemical substance of genes. extracted from paraffin-embedded endometrial tissue. (8) Although not a pattern of tissue pathology typically associated with CMV, previous reports of granulomatous inflammation associated with CMV infection in other organ systems have been documented in the literature. (8) Christie and Krieger (7) reported a case of necrotizing granu lomatous inflammation of the uterine cervix, which they attributed to chlamydial infection. (7) There was no evidence of organisms, either by histologic examination or by additional ancillary staining, in any of the cases in the current series.
Sarcoidosis is a systemic granulomatous disorder that has been previously reported to involve the uterus, (13-17) but involvement of the female genital tract by sarcoidosis is relatively rare. Exclusion of other causes for the inflammation, especially infectious etiologies, is warranted in patients with granlulomatous inflammation of the uterus and without a known history of sarcoidosis. Sarcoidal involvement of the uterus may include both endometrium and myometrium, in contrast to the relative rarity of myometrial involvement by tuberculosis. Menzin et al (17) even reported evidence of granulomas in a titerme leiomyoma of a patient with sarcoidosis. Clinical presentations of uterine sarcoidosis appear to be myriad and nonspecific nonspecific /non·spe·cif·ic/ (non?spi-sif´ik)
1. not due to any single known cause.
2. not directed against a particular agent, but rather having a general effect.
1. , and include recurrent pelvic pain, uterine bleeding, infertility, and persistent vaginal discharge. (16) None of the patients in the current series were known to have sarcoidosis, either before surgery or during the follow-up period.
Rare examples of uterine granulomatous vasculitis Vasculitis Definition
Vasculitis refers to a varied group of disorders which all share a common underlying problem of inflammation of a blood vessel or blood vessels. The inflammation may affect any size blood vessel, anywhere in the body. have also been documented in the literature. Lhote et al (18) reported the case of a 61-year-old woman with a history of fever and weight loss over an 8-year period. Hysterectomy specimen showed evidence of giant-cell arteritis arteritis
Inflammation of the arteries. It occurs in diseases including syphilis, tuberculosis, and lupus erythematosus. Varieties not closely associated with systemic disease or disease of an organ outside the cardiovascular system have been described as temporal arteritis, affecting the ovaries and myometrium. Interestingly, a temporal artery biopsy in the same patient showed evidence of temporal arteritis. Although granulomatous inflammation associated with infectious processes and sarcoidosis may also be vascular in nature, the presence of blood-vessel-associated granulomatous inflammation should at least raise the possibility of a true vasculitic process.
In patients with a history of surgery, foreign material from glove talc or suture may elicit a foreign-body giant-cell reaction. In many of these cases, histologic evidence of the foreign material may be evident by routine light microscopic evaluation, including polarization of the granuloma. An IUD may also elicit a focal foreign-body giant-cell reaction. Davis et al (19) reported foreign-body giant-cell reaction associated with iron-pigment residue from use of Monsel's solution in the uterine cervix at sites of previous biopsies. Independent of foreign material left behind during surgery, there has been association of surgery, particularly diathermy diathermy (dī`əthûr'mē), therapeutic measure used in medicine to generate heat in the body tissues. Electrodes and other instruments are used to transmit electric current to surface structures, thereby increasing the local blood ablation procedures, with granulomatous inflammation. (20-27) In many of these cases, the granulomatous inflammation is associated with evidence of caseous necrosis related to the surgical procedure, as well as hemosiderin-type pigment. Evans et al (21) suggested that perhaps the basis for these lesions is an idiosyncratic id·i·o·syn·cra·sy
n. pl. id·i·o·syn·cra·sies
1. A structural or behavioral characteristic peculiar to an individual or group.
2. A physiological or temperamental peculiarity.
3. reaction to focally-altered collagen ma terial. None of the current cases showed evidence of caseous necrosis associated with the granulomatous inflammation. Eight of the women, however, had a history of uterine instrumentation, which may have accounted for the etiology of their granulomas.
Other unusual causes of granulomatous inflammation in the endometrium have been reported. Radiation therapy has been described as an uncommon cause of granulomas. Rare examples of so-called ceroid granulomas have also been described in the uterus. (28-30) These lesions are marked by presence of granular pigment, which often accumulates within macrophages Macrophages
White blood cells whose job is to destroy invading microorganisms. Listeria monocytogenes avoids being killed and can multiply within the macrophage. . In many cases, this type of granuloma is associated with previous hemorrhage and necrosis, such as is seen in either tumor necrosis or endometriosis. (30) Such granulomas were not identified in any of the cases in this study.
Despite staining for organisms, a search for foreign material, and a review of the medical record, the precise etiology of the granulomas was not known in a number of the patients in the current series. Presumably pre·sum·a·ble
That can be presumed or taken for granted; reasonable as a supposition: presumable causes of the disaster. , in some cases, a history of surgery accounted for the presence of granulomas. Although the pathologic diagnosis of granulomas in these cases does not appear to prompt further evaluation of the patients for potential etiologies, consideration of such workup work·up
n. Abbr. w/u
A thorough medical examination for diagnostic purposes. may be deemed appropriate in certain scenarios.
TABLE 1 Clinicopathologic Features of Patients With Granulomatous Inflammation of the Uterus Age Presenting Previous Uterine Patient (yrs) Symptom Instrumentation Procedure 1 49 Menorrhagia Yes x 2 Endometrial bx 2 37 Menorrhagia Yes x 6 TAH/BSO 3 38 Menometorrhagia Yes x 3 Endometrial curettage 4 78 Postmenopausal Yes x 1 TAH/BSO bleeding 5 45 Menorrhagia Yes x 1 TAH/BSO 6 39 Infertility Yes x 3 Endometrial bx History of IUD 7 90 Uterine prolapse Yes x 1 TVH 8 43 Pelvic mass No TAH/BSO 9 51 Menometorrhagia No Endometrial bx 10 64 Postmenopausal Yes x 1 Endometrial bx bleeding 11 50 Menorrhagia No TAH/BSO Foreign/ Type of Polarizable No. of AFB & GMS Patient Granuloma Material Granulomas Stains 1 Non-necrotizing None 1 Negative 2 Non-necrotizing None 1 Negative 3 Non-necrotizing None Multiple Negative 4 Non-necrotizing None 1 Negative 5 Non-necrotizing None 1 Negative 6 Non-necrotizing None 2 Negative 7 Non-necrotizing None 1 Negative 8 Non-necrotizing None Multiple Negative 9 Non-necrotizing None 1 Negative 10 Non-necrotizing None 1 Negative 11 Non-necrotizing None 3 Negative Concomitant Patient Pathology 1 Exaggerated proliferative-phase endometrium, complex hyperplasia, squamous metaplasia 2 Acute and chronic inflammation, complex hyperplasia with atypia 3 Atypical polypoid adenomyoma 4 Endometrial adenocarcinoma 5 Endometritis, adenomyosis, leiomyoma 6 None 7 Endometrial polyp, leiomyomata, accute and chronic cervicitis 8 Endometrial adenocarcinoma, acute and chronic cervicitis 9 Exaggerated proliferative-phase endometrium, squamous metaplasia 10 Endometritis 11 Squamous metaplasia, lciomyomata, chronic cervicitis AFB = Acid-fast bacillus GMS = Gomori methenamine silver IUD = intrauterine device, bx = biopsy, TAH/BSO = transabdominal hysterectomy with bilateral salpingo-oophorectomy, TVH = transvaginal hysterectomy TABLE 2 Summary of Possible Etiologies of Uterine Granulomatous Inflammation Infection (mycobacterial, fungal, viral, parasitic) Sarcoid Vasculitis Foreign-body giant-cell reaction (intrauterine device, parasite, foreign material) Ceroid accumulation Radiotherapy Previous instrumentation/surgery (eg, diathermy ablation) Unknown
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1. causing little pain.
2. slow growing.
1. Disinclined to exert oneself; habitually lazy.
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(18.) Lhote F, Mainguene C, Griselle-Wiseler V, et al: Giant cell arteritis giant cell arteritis
See temporal arteritis.
Giant cell arteritis
Also called temporal arteritis. A condition which causes the inflammation of temporal arteries. of the female genital tract with temporal arteritis. Ann Rheum rheum (rldbomacm) any watery or catarrhal discharge.
A watery or thin mucous discharge from the eyes or nose.
any watery or catarrhal discharge. Dis 1992; 51:900-903
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The science concerned with the cytologic and histologic structure of abnormal or diseased tissue.
The study of diseased tissues at a minute (microscopic) level. 1995; 27:541-47
(21.) Evans CS, Goldman RL, Klein HZ, et al: Necrobiotic nec·ro·bi·o·sis
The natural death of cells or tissues through aging, as distinguished from necrosis or pathological death.
nec granulomas of the uterine cervix. a probable postoperative reaction. Am J Surg Pathol 1984; 8:841-844
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(28.) Shintaku M, Sasaki M, Babi Y: Ceroid-containing histiocytic histiocytic
pertaining to histiocytes.
see malignant histiocytosis.
prolymphocyte. granuloma of the endometrium. Histopathology 1991; 18:169-172
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(30.) Ooi K, Riley C, Billson V, et al: Ceroid granulomas in the female genital system. J Clin Pathol 1995; 48:1057-1059
RELATED ARTICLE: KEY POINTS
* Infectious etiologies are commonly reported causes of granulomatous inflammation of the uterus.
* Involvement of the female genital tract by sarcoidosis is a relatively rare occurrence.
* Foreign material from suture or glove talc may elicit a foreign-body giant-cell reaction in patients with a history of surgery.
* Previous surgery may account for the presence of granulomas in some cases.
From the Department of Anatomic Pathology, Cleveland Clinic Foundation, Cleveland, Ohio.
Reprint requests to Richard A. Prayson, MD, Cleveland Clinic Foundation, Department of Anatomic Pathology (L25), 9500 Euclid Ave, Cleveland OH 44195.