FERTILITY AND STERILITY Copyright 1978 The American Fertility Society Vol. 30, No. 1, July 1978 Printed in U.S.A. SALPINGITIS IN OVARIAN ENDOMETRIOSIS BERNARD CZERNOBILSKY, M.D.*t ALAN SILVERSTEIN, M.D. Departments of Pathology and Obstetrics and Gynecology, Magee-Women's Hospital, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania 15213 A histologic study of 87 cases of ovarian endometriosis with salpingectomy revealed 29 cases (33%) in which the removed fallopian tubes showed chronic salpingitis. Tubal obstruction could be demonstrated in only one of these patients. Tubo-ovarian adhesions were found in 15 patients (17%) and in only 7 of these in association with salpingitis. Although the patients in the present series did not consult their physicians because of infertility, but rather for other symptoms related to pelvic endometriosis, the finding of chronic salpingitis in 33% of the cases suggests that salpingitis may play a role in the infertility associated with endometriosis, possibly through altered tubal secretion. Fertil Steril 30:45, 1978 The relationship of infertility to pelvic endometriosis has been well established.'-4 Although the exact mechanism of the infertility in many of these cases remains unknown, the relatively good surgical results following a variety of procedures, including lysis of tubal adhesions and correction of obstruction, indicate that these lesions constitute a definite cause of infertility in a number of patients. 3 5 In spite of the attention given to the fallopian tubes in an attempt to elucidate the mechanisms of infertility in endometriosis, the occurrence of salpingitis and its possible role in the infertility of these patients have not been investigated. The purpose of this paper is to establish the incidence of salpingitis in patients with ovarian endometriosis and to speculate on its possible relationship to infertility. Received February 7, 1978; accepted March 14, 1978. *Visiting Associate Professor of Pathology on sabbatical leave from the Department of Pathology, Kaplan Hospital, Rehovot, Israel, affiliated with the Medical School of the Hebrew University and Hadassah, Jerusalem, Israel. treprint requests: Bernard Czernobilsky, M.D., Magee Women's Hospital, Forbes Avenue and Halket Street, Pittsburgh, Pa. 15213. 45 MATERIALS AND METHODS The slides of 87 cases of histologically proven ovarian endometriosis demonstrating both epithelial and stromal elements in which one or both fallopian tubes were removed were reviewed. The material was fixed in 10% buffered formalin and stained with hematoxylin and eosin. In selected cases the fallopian tubes were also stained with Mallory's iron stain for hemosiderin. The clinical records were studied with special emphasis on the fertility status of these patients. RESULTS Of the 87 patients, 83 were white and 4 were black. The patients' ages ranged from 25 to 68 with a mean of 41.1 years. Unilateral tubaoophorectomy was performed in 45 patients and bilateral salpingo-oophorectomy in 42 patients. Histologic examination revealed unilateral ovarian endometriosis in 63 patients and bilateral ovarian endometriosis in 24 patients. In 29 patients histologic examination revealed the presence of salpingitis which was chronic in 26 patients and acute and chronic in 3 patients
. 46 CZERNOBILSKY AND SILVERSTEIN July 1978 FIG. 1. Chronic salpingitis characterized by diffuse infiltration of swollen plicae by round cells (hematoxylin-eosin, x 113). (Figs. 1 to 3). The lesion was diffuse in 20 patients and focal in 9 patients. Chronic salpingitis was characterized by stromal edema and infiltration by lymphocytes, plasma cells, and round cells, whereas in the acute and chronic cases, polymorphonuclear neutrophils were prominent in addition to the round-cell infiltrate. In eight of the cases the epithelium lining the oviduct showed a variety offocal degenerative changes such as lack of both ciliated and secretory cells, nuclear pleomorphism, stratification, atypism, and reduction of cellular size with the appearance of low cuboidal to flat cells. Hemosiderin-laden macrophages were present within the tubal stroma in four patients and foamy macrophages in two patients with chronic salpingitis. One case showed hydrosalpinx and one follicular salpingitis with tubal obstruction in addition to the chronic inflammation. Endometriosis was observed within the tubal wall but not communicating with the lumen in two instances. The salpingitis was unilateral in 25 patients and bilateral in 4 patients. In six patients with unilateral salpingitis and in one with bilateral salpingitis, tubo-ovarian adhesions were demonstrated on pathologic examination. Eight patients had tubo-ovarian adhesions in the absence of salpingitis (Table 1). All of the patients with salpingitis were white. Their ages ranged from 25 to 51 with a mean of 39.2 years, whereas the ages of the patients without salpingitis ranged from 26 to 68 with a mean of 41.5 years. Information concerning gravidity and number of pregnancies was available in only 79 of the 87 patients. Among 53 patients without salpingitis, 8 (15%) were nulliparous. There were 5 (19%) nulliparous patients among the 26 with salpingitis. The mean value for gravidity and parity was 2 in patients both with and without salpingitis. DISCUSSION One of the most significant aspects of this investigation was the coexistence of salpingitis in 33% of patients with ovarian endometriosis. On the other hand, pathologic examination revealed tubo-ovarian adhesions in only 17% of the patients, and in more than half of these the adhe-
Vol. 30, No.1 SALPINGITIS IN OVARIAN ENDOMETRIOSIS 47 FIG. 2. Higher magnification of chronic salpingitis showing marked abnormalities of the lining epithelium, such as lack of normal distribution of ciliated and secretory cells (hematoxylin-eosin, x 125). sions were not associated with salpingitis. These findings suggest that salpingitis is much more frequently associated with ovarian endometriosis than has been hitherto considered. Our results also indicate that salpingitis is not necessarily associated with tubo-ovarian adhesions; as a matter of fact, in 72% of the instances of salpingitis no adhesions were demonstrated on pathologic examination. It should be pointed out that the patients in this study did not consult their physicians for infertility, but rather for a variety of symptoms related to pelvic endometriosis which eventually led to ablation of the ovaries and tubes. Thus, the data concerning infertility, either primary or secondary, must be considered incomplete. However, review of the medical records revealed that 16.4% of the patients in this series were nulliparous. The figure was higher in the group of patients with salpingitis as compared with those without salpingitis, but the difference was not statistically significant. Furthermore, the mean figures for gravidity and parity were the same in patients with and without salpingitis. Thus, although our results fail to show a higher frequency of infertility in patients with salpingitis than in those without salpingitis-and this most likely because of the nature of this series-it is probable that chronic salpingitis constitutes a supplementary cause of infertility in patients with ovarian endometriosis. The presence of salpingitis may also explain some of the failures of surgical treatment in correcting infertility in these patients. Infertility in the presence of chronic salpingitis is usually attributed to an associated tubal obstruction. 6 In the absence of obstruction, as prevailed in all but one of the present cases, other mechanisms must be implicated. It is now well known that factors other than oviductal obstruction, such as altered tubal secretion, contribute to infertility. 7 8 Chronic stromal inflammation of the endosalpinx may very well influence the morphology of overlying epithelial cells as evidenced in eight of our cases. This effect in turn might
48 CZERNOBILSKY AND SILVERSTEIN July 1978 FIG. 3. Details of the epithelium in chronic salpingitis demonstrating markedly diminished numbers of ciliated and secretory cells, areas of multilayered cells, and nuclear atypism (hematoxylin-eosin, x286). manifest itself in changes in the chemical composition of the oviduct secretion which is the product of these epithelial cells. The etiology of chronic salpingitis in ovarian endometriosis remains unknown. It can be postulated that if, as has been suggested, regurgitation of endometrium through the fallopian tubes takes place, 9 this aberrant tissue could act as an irritant and produce inflammatory changes. It is unlikely, however, that this possible mechanism is a significant factor in ovarian endometriosis. Endometriosis seems to develop mainly through metaplasia of the multipotential ovarian germinal epithelium, which is of celomic origin and thus capable of producing Mullerian structures. 10 11 Endometriosis of the oviduct cannot be implicated as a cause of chronic salpingitis because it occurred only twice in our series and in each case was situated in the tubal wall and did not communicate with the lumen of the oviduct. In conclusion, the observation in this study, that 33% of patients with ovarian endometriosis also had histologic evidence of chronic salpingitis not necessarily associated with tubal adhesions, Salpingitis TABLE 1. Salpingitis and Tubo-Ovarian Adhesions in 87 Patients with Ovarian Endometriosis Unilateral ovarian endometriosis 17 patients (3 with adhesions) Unilateral salpingitis Bilaterial ovarian endometriosis Bilateral salpingitis Total 8 patients 4 Patients 29 Patients (3 with adhesions) (1 with adhesions) (7 with adhesions) Unilateral adhesions Bilateral adhesions Tubo-ovarian adhesions without salpingitis 5 Patients 2 Patients 1 Patient 8 Patients
Vol. 30, No.1 SALPINGITIS IN OVARIAN ENDOMETRIOSIS 49 constitutes a hitherto unrecognized factor which must be considered when pelvic endometriosis is treated, especially in the infertile patient. REFERENCES 1. Kistner RW: Endometriosis and infertility. Obstet Gynecol 2:877, 1959 2. Norwood GE: Sterility and fertility with pelvic endometriosis. Clin Obstet Gynecol 3:456, 1960 3. Kistner RW: Management of endometriosis in the infertile patient. Fertil Steril 26:1151, 1975 4. Weed JC, Holland JB: Endometriosis and infertility: an enigma. Fertil Steril 28:135, 1977 5. Sadigh H, Naples MD, Batt RE: Conservative surgery for endometriosis in the infertile couple. Obstet Gynecol 49:562, 1977 6. Ledger WJ: Inflammations in infertility. In Progress in Infertility, Second Edition, Edited by SJ Behrman, RW Kistner. Boston, Little, Brown, and Co, 1975, p 208 7. David A, Garcia CR, Czernobilsky B: Human hydrosalpinx. Am J Obstet Gynecol 105:400, 1969 8. David A, Serr DM, Czernobilsky B: Chemical composition of human oviduct fluid. Fertil Steril 24:435, 1973 9. Sampson JA: Perforating hemorrhagic (chocolate) cysts of the ovary, their importance and especially their relation to pelvic adenomas of the endometrial type. Arch Surg 3:245, 1921 10. Hertig AT, Gore H: Atlas of Tumor Pathology, Sect IX, Fasc 33: Tumors of Female Sex Organs, Part 3: Tumors of the Ovary and Fallopian Tube. Washington DC, Armed Forces Institute of Pathology, 1961, p 106 11. Czernobilsky B: Primary epithelial tumors of the ovary. In Pathology of the Female Genital Tract, Edited by A Blaustein.. New York, Springer Verlag, 1977, p 475