|Year : 2021 | Volume
| Issue : 3 | Page : 85-91
Histomorphological spectrum of incidentally detected fallopian tube lesions in patients operated for various clinical conditions and detection of precursor lesion by applying sectioning and extensively examining the fimbriated end sampling protocol
Neha Singh1, Ipsita Dhal1, Aneesha Mohanpuria2, Swati Saxena2
1 Department of Pathology, Homi Bhabha Cancer Hospital, Varanasi, Uttar Pradesh, India
2 Consultant Pathologist, Oncquest Laboratory, New Delhi, India
|Date of Submission||05-Feb-2021|
|Date of Decision||02-May-2021|
|Date of Acceptance||21-Sep-2021|
|Date of Web Publication||14-Dec-2021|
Department of Pathology, Homi Bhabha Cancer Hospital, Varanasi, Uttar Pradesh
Source of Support: None, Conflict of Interest: None
Background: Fallopian tube specimens are studied either in conjunction with ovaries, uterus, and cervix or alone. However, there is less knowledge about the spectrum of histopathological changes in these specimens due to paucity of data. Aim: This study aims to describe the spectrum of histopathological changes with frequency observed in the resected fallopian tube specimens, especially to detect the malignant precursor lesions and malignancy rate. Materials and Methods: Four hundred and ninety-four patients of resected fallopian tubes either separately or along with other female genital tract organs were retrospectively reviewed for histopathological findings. Hematoxylin- and eosin-stained histopathology slides were retrieved and re-examined. The distal fimbriated end was longitudinally sectioned for examination of fimbrial epithelium. The “sectioning and extensively examining the fimbriated end” (SEE-FIM) sampling protocol was used. Results: Out of 494 resected specimens, 247 patients (50%) had some kind of fallopian tube pathology. Fibrosis was the most common lesion observed in 59 cases followed by hematosalpinx (33 cases). Primary neoplasm was seen in 3 (0.6%) of specimens and all were of serous adenocarcinoma histology. Whereas, secondary malignancies were seen in 2 cases (0.4%), with primary being ovary. Four cases of serous tubal intraepithelial carcinoma (STIC) (0.8%) were detected using SEE-FIM protocol. Conclusion: A thorough histopathological examination including SEE-FIM protocols should be followed for detection of various fallopian tube lesions, which will eventually help in appropriate patient workup and treatment. Early detection of precursor lesions such as STIC and prompt treatment intervention may help in the prevention of ovarian malignancies.
Keywords: Fallopian tube lesions, histopathological study, malignancies, serous tubal intraepithelial carcinoma
|How to cite this article:|
Singh N, Dhal I, Mohanpuria A, Saxena S. Histomorphological spectrum of incidentally detected fallopian tube lesions in patients operated for various clinical conditions and detection of precursor lesion by applying sectioning and extensively examining the fimbriated end sampling protocol. Oncol J India 2021;5:85-91
|How to cite this URL:|
Singh N, Dhal I, Mohanpuria A, Saxena S. Histomorphological spectrum of incidentally detected fallopian tube lesions in patients operated for various clinical conditions and detection of precursor lesion by applying sectioning and extensively examining the fimbriated end sampling protocol. Oncol J India [serial online] 2021 [cited 2022 Jan 21];5:85-91. Available from: https://www.ojionline.org/text.asp?2021/5/3/85/332513
| Introduction|| |
Fallopian tubes, named after Gabriele Falloppio, are a pair of complex structures connecting the ovary to the uterus, hence are involved in crucial aspects of reproduction and normal pregnancy., It is one of the most common specimens studied, either in conjunction with ovaries, uterus, and cervix or simply on its own. As a result, it has been observed that these 10-cm tubular structures are a seat of a wide variety of lesions ranging from inflammatory to malignant, all of which may significantly alter the reproductive health of a female while a few may have an impact on the mortality., Inflammation of the fallopian tubes, one of the most common findings, may lead to infertility, while ectopic pregnancy may be responsible for a high mortality and morbidity rates. Malignancy of the tubes either as primary or secondaries from other organs is a rare diagnosis.
Fallopian tubes earlier thought to be significant vastly in the reproductive health of a female, are now being rigorously being studied as a foundation of ovarian carcinoma, especially high-grade serous carcinoma (HGSC). Hence, prophylactic salpingo-oophorectomy procedures have increased as a part of ovarian cancer screening protocol which subsequently, led to increased vigilance and search of precursor lesions in the fallopian tubes, eventually leading to the discovery of serous tubal intraepithelial carcinoma (STIC) as a precursor lesion.
There is a paucity of literature documenting the changes in the fallopian tubes removed for a particular reason. Hence, the present retrospective study aims at describing the spectrum of histopathological changes noted in the surgically resected specimens of fallopian tube and to detect precursor lesions by applying SEE-FIM protocol.
| Materials and Methods|| |
This retrospective study was conducted over a period of 12 months, from September 2018 to September 2019. A total of 494 surgically resected samples of fallopian tubes were received either as salpingectomies or a part of pan hysterectomies or tubo-ovarian masses were studied.
Hematoxylin- and eosin-stained histopathology slides were retrieved. The clinical forms were reviewed for age, clinical presentation, and gross features of the specimens. The histopathology slides were re-examined for detailed description of the histological patterns of different fallopian tube lesions. The protocol for sectioning and extensively examining the fimbriated end (SEE-FIM) of the fallopian tubes was followed in order to ensure optimal histological evaluation. As per the protocol, infundibulum and fimbriae of the fallopian tube were removed from the rest of the tube and were longitudinally sectioned with eventually leading to exposure of the tubal plicae. Furthermore, transverse cuts were made at the isthmus and the ampulla.,, The slides prepared from all the sections after staining with Hematoxylin and eosin were studied by 2 of our pathologists for careful diagnosis.
Data obtained were analyzed using IBM, Statistical Package for the Social Sciences, IBM Corp. Released 2011. IBM SPSS Statistics for Windows, Version 20.0. Armonk, NY: IBM Corp, USA for Windows. Measures of central tendency and variation were calculated for numerical variables while frequency and proportions were calculated for categorical variables.
| Results|| |
A total of 494 patients with surgically resected fallopian tube specimens were obtained for different clinical reasons during the study period and were submitted for histomorphological analysis. Two hundred and forty-seven patients (50%) had some spectrum of pathological findings and the rest were within normal limits [Figure 1]a.
The age range of the study population varies from 25 to 80 years, with a mean age of 48.8 years. The clinical symptoms of the patients included a brief history of abnormal uterine bleed (274 cases), mass abdomen (50 cases), and pain abdomen (104 cases). Sixty-six cases had no significant history at all. Consequently, all the patients had undergone various procedures such as bilateral and/or unilateral salpingo-oophorectomy, hysterectomy with salpingo-oophorectomy, or a simple tubal ligation.
The nature of the surgeries depended on the site of the pathology of the primary disease such as uterus, cervix, ovary, or the fallopian tubes itself. Hysterectomy with bilateral salpingo-oophorectomy (264 cases; 53.4%) was the most common procedure followed by bilateral salpingo-oophorectomy (82 cases; 16.6%) [Table 1]. The parity of the patients ranged from 1 to 5, with the parity of two being the most common group undergoing surgery. Maximum surgeries were performed in the age group of 31–40 years (120 cases) followed by 41–50 years age group (106 cases) which included predominantly bilateral salpingo-oophorectomy in the former (52/120 cases) and hysterectomy with salpingo-oophorectomy in the latter (86/106 cases) [Table 1].
Of the specimens received, uterus was the primary clinical indication in 46% (n = 227) of cases, followed by ovary in 34.8% (n = 172), infertility in 13.4% (n = 66), cervix in 4% (n = 20), and fallopian tubes in only 1.8% (n = 9) of cases [Table 2]. The uterine lesions leading to resection varied from fibroid (103 cases) to UTROSCT (2 cases). Ovarian lesions included a predominantly neoplastic spectrum (90 cases) and followed by nonneoplastic spectrum (82 cases). Cervical intraepithelial neoplasia Grade III and squamous cell carcinomas constitute the cervical lesions. Ectopic pregnancy and high grade serous carcinoma (HGSC) were the only two fallopian tube lesions in our study which were the primary cause of surgical excision. For the primary site of malignancy contributes as surgical specimens, 20 cases are endometrial carcinoma, 62 cases are ovarian malignancies (HGSC: 42 cases; mucinous cystadenocarcinoma: 10 cases; and germ cell tumor: 10 cases), 10 cases are cervical squamous cell carcinoma, and 3 cases are HGSC of fallopian tube.
Even though the fallopian tube pathologies did not reveal a specific clinical finding, it was observed that the most common finding noted was that of abnormal uterine bleeding, which was seen most commonly with fallopian tube fibrosis and hematosalpinx. Fallopian tube lesions were seen most commonly in patients with parity of two, however, the most common finding of fibrosis (28 cases) was seen in patients with a parity of 3.
The fallopian tube lesions were mostly observed in the age group of 31–40 years. The findings observed in the fallopian tubes examined during the routine procedures were broadly divided as stromal in 212 cases and epithelial lesions in 35 cases [Figure 1]b, [Figure 2], [Figure 3], [Figure 4], [Figure 5]. Epithelial findings were seen predominantly in the age group of 51–60 years of age while the stromal findings were most commonly detected in the age group of 31–40 years of age. Epithelial lesions were distributed as vacuolization in 12 cases, epithelial tufting in 11 cases [Figure 3]d, STIC in 4 cases [Figure 2]a, mucinous metaplasia in 5 cases [Figure 4]b, and HGSC in 3 cases [Figure 4]d and [Table 3]. The most common stromal finding was of inflammation which included the most common finding of fibrosis (59 cases) [Figure 2]c followed by hematosalpinx (33 cases) [Figure 1]b, while tuberculosis granuloma was seen in two cases, pyosalpingitis in a single case, acute salpingitis in 5 cases [Figure 1]d, and chronic salpingitis in 19 cases [Figure 2]d. Pigmentosis tubae, another aspect of chronic inflammation, was noted in 9 cases [Figure 4]c. Walthard cell nests [Figure 1]c and [Figure 5]b and Wolffian duct remnants were seen in 5 cases each. Twenty cases of paratubal cysts were also recorded along with 14 inclusion cysts [Figure 1]d and [Figure 5]b. Ectopic pregnancy was seen in a total of 6 cases. Other entities we noted were suture granuloma in 1 case, along with nonspecific findings such as calcification in 2 cases [Figure 5]a, cholesterol clefts in 1 case [Figure 3]c, and foamy histiocytes in 2 cases [Figure 2]d.
|Figure 1: (a) Normal fallopian tube, (b) Hemosiderin laden macrophages in the submucosa with lumen filled with acute suppurative exudates, (c) Fallopian tube with Walthard cell nest, (d) Acute salpingitis with inclusion cyst|
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|Figure 2: (a) Serous tubal intraepithelial carcinoma, (b) Fallopian tube with increased capillary proliferation in the submucosa, (c) Sclerosis of the fallopian tube stroma, (d) Xanthogranulomatous salpingitis|
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|Figure 3: (a) Fallopian tube epithelium with increased peg cells with clear cytoplasm, (b) Cholesterol granuloma formation, (c) Cholesterol clefts, and (d) Increased stratification of the tubal epithelium|
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|Figure 4: (a) Metastatic deposit in the tubal wall, (b) Intestinalization of the tubal epithelium with goblet cells, (c) Pigment in the tubal lining, (d) Tubal serous adenocarcinoma|
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|Figure 5: (a) Psammomatous calcification, and (b) Walthard cell nest with inclusion cyst|
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The metastatic carcinoma [Figure 4]a was seen in a total of 2 cases, both of which were known cases of HGSC in the ovary. Precursor lesion of the fallopian tube as STIC [Figure 2]a was noted in 4 cases (0.8%) while the primary fallopian tube malignancy as HGSC [Figure 4]d was seen in 3 cases (0.6%).
| Discussion|| |
Although fallopian tubes are one of the most common structures reported in surgical gynecological specimens, the spectrum of fallopian tube lesions has been defined infrequently in literature. Hence, the current study was undertaken in a small subset of Indian population to see the variety of fallopian tube lesions detected either incidentally or as a cause of surgery. In our study, fallopian tube with pathological lesions was seen in 50% (247/494) of the patients. The rest 50% of cases were without any pathological lesions. This similar finding was noted in various studies in the past in which more than 50% of the fallopian tubes studied did not reveal a significant pathology.,,
We found 31–40 years of age as the most common age group for various surgical procedures conducted closely followed by 41–50 years of age group. Similarly, Bagwan et al. and Gon et al. in their studies reported a maximum number of cases belonged to 36–45 years' age group. 31–40 years of age was the most common age group for various procedures conducted., However, some studies such as Onyishi et al., and Kujur et al., have reported a slightly older age group as the predominant age group for various surgical procedures.,
Uterine lesions were the common clinical indication (46%) followed by ovarian lesions (34.8%) for the surgical procedures. Similarly, according to Onyishi et al., the contributions of organ-wise gynecological tract lesions promoting surgical procedures are uterine corpus lesions in 66.9% of cases, lesions of the ovary in 24.7%, and cervix lesions in 8.4% of cases. The most common surgery performed was hysterectomy with bilateral salpingo-oophorectomy (53.4%), followed by tubectomies, which was in concordance with other studies.,,
The most common fallopian tube lesion overall turned out to be inflammation which was seen in most of the studies as well.,,,,, Our study showed an overall 27.6% of fallopian tubes with an inflammatory pathology. Among the inflammatory pathology, chronic inflammation or the sequelae of it comprised the bulk of inflammatory lesions,, which was seen most commonly in the reproductive age group. Furthermore, similar to a study by Hunt and Lynn, we noted fibrosis as the most frequent finding among all the inflammatory lesions and in toto, seen in 11.9% of the cases followed by hematosalpinx in 6.6% of the cases, whereas chronic nonspecific salpingitis was seen in only 3.8% of the cases. Acute inflammation was the least common finding noted in our study, seen in 1% of the cases. Gon et al. reported acute salpingitis with an incidence of 0.06%.
Fibrosis was seen most commonly in patients with uterine fibroid followed by uterine prolapse, whereas hematosalpinx was noted in patients with adenomyosis, endometrial carcinoma, endometrial polyp, and cervical carcinoma. Similarly, chronic nonspecific salpingitis was most commonly observed in patients with endometriosis. Tuberculosis, another significant chronic inflammatory pathology in our country, was also noted in the study. The incidence of tuberculosis which was seen as a consequent of primary pulmonary disease or as spread of the disease from the nearby organs has been declining over the past few years. However, we still noted tubercular granuloma in 0.4% of the fallopian tube lesions which was similar to other studies.,, Gon et al. reported fallopian tube tuberculosis with an incidence of 0.19%, and all the cases had concomitant involvement of endometrium. In contrast to the other studies, we did not find a similar pathology in the rest of the female genital tract organs, but found the granuloma in patients with uterine prolapse.
Tubal ectopic, or presence of gestational sac in the fallopian tubes, most commonly noted in the ampullary region, may arise as a result or as a sequela to inflammation, which is on the rise according to the current scenario., Contrary to the trend, we noted only 1.2% (6 cases) of tubal ectopic which was comparable to the findings of Kukreja and Shetty which was 1.34%. However, we found the tubal ectopic in an older age group than the other studies.,,, These findings were overall considered low when compared to majority of other studies which showed an incidence of at least 10% or more of tubal ectopic.,,,
Infertility may also be a result of chronic inflammation. However, our study did not show a significant fallopian tube pathology in correlation with infertility; in contrast, we found cases of infertility to have spectrum of benign fallopian tube lesions such as presence of cysts followed by hematosalpinx, edema, and Walthard cell nests. The presence of cystic lesions which included inclusion cyst (14 cases) and paratubal cysts (20 cases) was seen in a total of 34 cases, which was considerably higher when compared to most of the studies.,,, Few studies such as Bagwan et al. and Kujur et al., however, had reported even more cases of paratubal cysts., Paratubal cysts have no clinical significance and can be seen in a wide range of conditions. In our study, we saw that the paratubal cysts were seen in a spectrum of cases which varied from uterine prolapse to ovarian follicular cysts and occasional cases of infertility. Inclusion cysts, on the other hand were seen more commonly associated with infertility and a case of ovarian carcinoma.
The presence of ectopic endometriotic tissue at the fallopian tube serosa and/or the epithelium was noted in about 2% of our specimens, which was considerably higher than other studies.,,,,, The presence of endometrial tissue at fallopian tubal serosa was noted in association with ovarian endometriotic cyst in all the cases. Benign epithelial cell clusters of cuboidal to transitional cells clusters seen grossly as gray-yellow nodules are one of the common incidental findings in the fallopian tube, mesovarium, and mesosalpinx. We noted only 1% of such findings, along with similar incidence of Wolffian duct remnants. A similar distribution was noted in other studies.,, Metaplasia of the fallopian tube is an uncommon entity, which was reflected in our study as 1% of the cases, which was seen similarly in a study by Hunt and Lynn. The most common metaplasia noted was mucinous metaplasia.
Fallopian tube malignancies are rare and primary fallopian tube lesions are even rarer. Secondaries to the fallopian tube are more common than the primary malignancy of the tube. For secondaries, ovary, endometrium, and cervix are the common site of the primary followed by appendix, stomach, colon, and breast., The evaluation of such requires a proper history as well as a proper IHC panel as per the suspected sites. The primaries of the fallopian tube are diagnosed rarely and incidentally, which may be as a result of their nonspecific clinical findings and the inability to distinguish them from the other female genital tract malignancies preoperatively. Hence, the proper gross and histopathological examination is essential by the pathologist so as not to miss out the diagnosis.
In addition, the recently proposed theory of carcinoma of fallopian tube suggests the presence of precursor lesions, i.e. STIC. In addition, the updated dualistic model of carcinogenesis by Kurman and Shih suggested that the distal ends of the fallopian tube harboring STIC may be the site of development of type II carcinomas which include HGSC., STIC is benignly recognized as a possible premalignant lesion in pelvic HGSC. Apart from STIC, there are a few lesions which have been noted to occur prior to STIC such as secretory cell outgrowth, p53 signature, and serous tubal intraepithelial lesions.,,, These lesions, however, are difficult to discern on routine examination and require further investigations. STIC on the other has striking histomorphological appearance which includes tubal epithelium displaying nuclear and cellular atypia, nuclear hyperchromasia, molding, prominent nucleoli and epithelial stratification as well as loss of polarity, and loss of ciliated cells. These lesions, like HGSC, show either a strong and diffuse immunostaining or a lack of p53 immunostaining, along with a very high Ki-67 proliferative activity index. In cases where no p53 expression is noted along with low proliferative activity on Ki-67, laminin γ1 staining and its alterations can be used to identify STIC. The significance of STIC lies in the recent studies which point towards its ability to give rise to primary HGSC at the local site (i.e. the fallopian tube) or other pelvic sites after metastases., A few studies have also emphasized the use of STIC in the staging of carcinomas.
On histomorphological examination, we detected STIC in 4 cases (0.8%), two of which were operated for endometrial hyperplasia and two for fibroid. This finding is slightly higher than the incidence reported in some studies. Samimi et al. in a study on population-based data from 10 523 surgeries including salpingectomy detected STIC in 40 (0.38%) specimens which include 35 cases of STIC having cancer indications and 5 cases with noncancer indications for surgery. Tang et al. reported an overall incidence of 4% of STIC among the 300 surgical specimens operated for different gynecological causes. Meserve et al. in a study detected 80 cases of STIC from 2268 patients at the age of >50 years undergoing bilateral salpingectomies including 78 cases of STIC either from risk reducing salpingo-oophorectomies or cases with HGSC and 2 cases of incidentally detected STICs from cases who had no history of risk for or a diagnosis of HGSC. According to Samimi et al. and Meserve et al., most of the STICs diagnosed among patients being operated for cancer indications. However, in our study, all the 4 cases of STICs are of incidental findings without any cancer indications which contradict the result of the above studies. The finding of STIC was not noted in few of the studies reviewed. This finding of STIC could have been as a result of the usage of SEE-FIM sampling protocol in our study which enabled the incidental detection of such lesions.
Soong et al. have stated a latent window period of 5 years as seen in other studies for progression of STIC to full-blown metastatic HGSC; in addition, the risk of incidentally detected isolated STIC getting transformed into disseminated HGSC is only 5%. Despite knowing the risk of STIC leading to pelvic HGSC, the management is still an area under study, as there is no fixed treatment or surveillance recommendations for such lesions; however, the concept of STIC and tubal origin of HGSC has led to the increasing rate of opportunistic salpingectomies being performed in low-risk populations.,
Primary fallopian tube carcinoma is accounted for 0.14%–1.8% of female genital tract malignancy, and hence is considered a rare malignancy. Similar to the ovarian epithelial tumors, serous adenocarcinomas are the most common primary malignancy of the fallopian tube, which may have arisen as a sequence of the precursor lesion STIC giving rise to a HGSC. The other malignancies include endometrioid, mucinous, clear cell, and transitional cell carcinoma. Similarly, we found only 3 cases of primary carcinoma in our study which accounts for 0.6% of resected specimens. All the 3 cases are of HGSC histology. Gon et al. in their study reported only one case of primary adenocarcinoma which accounts for 0.03% of all the specimens. Although fallopian tube malignancies have been reported in various case series throughout literature ranging from 0% to 5%, they are highly aggressive with high rates of recurrence, especially as retroperitoneal nodes and distant sites.,,,,,,,
In our study, primary HGSC was seen in 3 cases (0.6%) whereas metastatic carcinoma to the fallopian tubes was found in 2 cases (0.4%). This finding was in contradiction with the recent studies conducted where metastatic lesions to the fallopian tube are more common than the primary.,,,,,,,
The present study has some limitations: first, being retrospective nature of the study. Second, this study analyzed spectrum of histopathological changes of the resected specimens in which unilateral salpingo-oophorectomy and tubal ligation specimens were also analyzed. This may affect the incidence of STIC findings as one tube is missing from histopathological examination. Hence, further prospective studies should be conducted, and immunohistochemical examination and common molecular analysis between STIC and presence of malignancy need evaluation.
| Conclusions|| |
Fallopian tube, either sent separately or as a part of other specimens, remains one of the most commonly examined organs; the lesions of which vary predominantly from inflammatory pathology to the lesser common entities like carcinomas. Fallopian tube malignancies are rare entities having nonspecific clinical features along with an aggressive disease course. With the recent knowledge of precursor lesion such as STIC which has potential to transform into pelvic HGSC, it becomes essential to carefully examine the fallopian tubes.
Hence, taking into account the incidentally detected pathologies of the fallopian tube such as STIC and the low rates of clinically detected fallopian tube lesions, the proper grossing protocols (SEE-FIM) should be followed as well as detailed histomorphological examination should be done for detection of these lesions, which will eventually help in appropriate patient workup and treatment. The results of this study imply that extensive sampling and examination of even grossly unremarkable fallopian tube may lead to detection of a vast range of pathology.
We would like to thank the Department of Surgical Pathology, Oncquest Laboratories, New Delhi.
Financial support and sponsorship
Conflicts of interest
There are no conflicts of interest.
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[Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5]
[Table 1], [Table 2], [Table 3]