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Reason for improper simple hysterectomy in invasive cervical cancer in Northeast India


 Department of Gynaecologic Oncology, Dr. B. Borooah Cancer Institute, Guwahati, Assam, India

Date of Submission24-Jul-2020
Date of Decision09-Sep-2020
Date of Acceptance21-Dec-2020
Date of Web Publication18-Aug-2021

Correspondence Address:
Haelom Liegise,
East Block Burma Camp, Near Phom Church, Dimapur - 972 112, Nagaland
India
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/jcrt.JCRT_1005_20

 > Abstract 


Objective: The objective of the study was to determine the reasons for improper simple hysterectomy in the presence of invasive cervical cancer in Northeast India.
Materials and Methods: The medical records of 52 patients who had undergone improper simple hysterectomy in the presence of invasive cervical cancer and were referred to a tertiary regional cancer Institute at Guwahati, Assam, between January 2015 and December 2019 were reviewed.
Results: Most of the patients presented with abnormal vaginal bleeding (40.4%). The failure to perform cervical cytology before the operation was quite high at 48.1% (25 patients). Interestingly, normal cytologic smear could still be found in 15.4% (8 patients) despite the presence of invasive cervical cancer. Failure to perform preoperative Papanicolaou smear, incomplete evaluation of cervical intraepithelial neoplasia (CIN) on cervical biopsy, and negative Papanicolaou smear accounted for 75% of the patients undergoing inappropriate simple hysterectomy. The most common indications for inappropriate operation were abnormal vaginal bleeding (40.4%) and CIN (19.2%). The reasons for inappropriate simple hysterectomy included lack of preoperative cervical cytology (48.1%), false-negative cervical cytology (15.4%), incomplete evaluation of cervical dysplasia or microinvasion on biopsy (11.5%). failure to perform indicated conization( 5.8%), emergency hysterectomy (3.8%), errors in colposcopic examination (3.8%), incomplete evaluation of an abnormal cervical cytology (3.8%), failure to review slide (3.8%) and failure to biopsy a gross cervica lesion (3.8%).
Conclusion: Most improper simple hysterectomy resulted from deviation from guideline for cervical cancer detection protocols. Improper simple hysterectomy in the presence of invasive cervical cancer can be avoided if one sticks to the diagnostic guideline for patients with an abnormal cervical cytology.

Keywords: Cervical cancer, cervical cytology, improper simple hysterectomy



How to cite this URL:
Liegise H, Barmon D, Baruah U, Begum D, Kataki AC, Chhangte Z. Reason for improper simple hysterectomy in invasive cervical cancer in Northeast India. J Can Res Ther [Epub ahead of print] [cited 2021 Nov 28]. Available from: https://www.cancerjournal.net/preprintarticle.asp?id=324030




 > Introduction Top


Cervical cancer is ranked as the fourth most frequently diagnosed cancer and the fourth leading cause of cancer death in women worldwide. Cervical cancer is a major public health problem, being the second most common cancer among Indian women. India contributes to one-quarter of the global burden with 96,922 incident cases and 60,078 deaths in 2018.[1] The age-standardized incidence and mortality rates in India (ASR) are 14.7/100,000 and 9.2/100,000 women, respectively.[1] There are regional variations in ASR, from 24.3/100,000 in Aizawl to 5.6/100,000 in Dibrugarh district.[2] In lower and middle-income countries including India, cancer patients have a poor prognosis because of late diagnosis and cases already grown to advanced stages, low cancer awareness, and skewed cancer care facilities.[3] The 5-year relative survival rate for cancer cervix in India continues to be low, approximately 46% (range 34%–60%), predominantly because of late detection.[4]

Cervical cancer ranks second in incidence and mortality behind breast cancer and the performance of inadequate hysterectomy is not uncommon owing to the lack of proper investigative evaluations and/or a lack of expertise in primary care hospitals.[5] Early age at first sexual intercourse, poor sexual hygiene, multiple sexual partners, and frequent childbirth are some of the few reproductive risk factors for cervical cancer.[6] Burden of infection-related cancers is high in developing countries due to limited infection prevention practices. According to report provided by Catalan Institute of Oncology Information Centre on human papillomavirus (HPV)-related cancers in India 2018, the crude incidence rate of HPV-related cervical cancer in India is 14·9%.[7] In cervical cancer, 83·2% of females have HPV-16/HPV-18 detected, highlighting its importance in the development of cervical cancer.[7]

Most cases occur in less developed countries where no effective screening systems are available. Despite clinically accepted guidelines, a considerable proportion of patients with early-stage cervical cancer IA2 to IIA are still subjected to inadequate surgery when inadvertently treated by simple hysterectomy.[8] It is widely agreed that adherence to screening guidelines and careful patient management may help to minimize the number of suboptimal, simple hysterectomies carried out in cervical cancer. Therefore, when invasive cervical cancer is found after simple hysterectomy, further treatment is necessary; salvage radiotherapy[9] or radical parametrectomy has been performed.[10]

This study was undertaken to analyze the events preceding improper simple hysterectomy of invasive cervical cancer so that preventive measures might be suggested.


 > Materials and Methods Top


From January 2015 to December 2019, data of 52 women with invasive cervical cancer found incidentally in the hysterectomy specimens and referred to our institute from all of Northeast India were included in the study. All medical records were reviewed after ethical clearance for clinical characteristics, preoperative cytology, pathology, and other investigations as well as the indications for simple hysterectomy. Preoperative information including the cytologic study was also obtained from the records of the referring physicians (general surgery/gynecologist). All patients received clinical staging investigation including thorough physical examination, chest X-ray, and intravenous pyelogram. Cystoscopy, proctosigmoidoscopy, barium enema, and computed tomography scan of the abdomen were undertaken when indicated and deemed necessary.

Presumed clinical stage was assigned according to the FlGO-2009 staging system. Microscopic tumor invasion >3 cm and <5 cm with extension of >7 mm was classified as stage IA2, tumor confined to cervix with negative surgical margins was classified as Stage IB. Patients with tumor at surgical margins and no gross residual tumors were considered to have Stage IIA or IIB disease with histologically proven vaginal or paracervical involvement. Patients with gross residual disease remaining on paracervical areas or hydroureteronephrosis were designated as having Stage IIB or stage IIIB. Bladder or rectal invasion or distant metastasis was classified as Stage IV. The radiotheraphy (RT) treatment consisted of whole pelvic RT with a total dose of 45–50 Gy that was divided into 23–25 applications along with vaginal brachytheraphy. For chemoradiation patients, cisplatin (50 mg/m2) was administered weekly.


 > Results Top


[Table 1] shows the clinicopathological characteristics. The age of 52 patients ranged from 36 to 68 years, with a mean of 52 years. Women with parity ≤2 consisted of 12 (23.1%) patients and 40 (76.9%) patients with parity >2. There were 32 (61.5%) patients with Grade 1 tumor, followed by 14 (26.9%) and 6 (11.5%) patients with Grade 2 and 3, respectively. Tumor wide ≤20 mm included 32 (61.5%) patients and 20 (38.5%) patients with tumor >20 mm. Twelve (23.1%) patients had positive lymphovascular space invasion (LVSI) while remaining 40 (76.9%) had negative LVSI. The interval from simple hysterectomy to the start of treatment ranged from 20 to 540 days with a mean of 60 days. Among 12 patients with interval more than 100 days, eight patients were referred with vaginal bleeding and pelvic mass suggestive of recurrence. The remaining four patients were referred late for unknown reason. Forty-five (86.5%) patients had squamous cell carcinoma, 5 (9.6%) had adenocarcinoma, and 2 (3.8%) had adenosquamous carcinoma. Presumed FIG0 Stage IB cervical cancer was noted in 18 patients (34.6%), Stage IA2 and Stage II in 12 patients (23.1%) each, while Stage III and Stage IV were found in 7 (13.5%) and 3 (5.7%) patients, respectively.
Table 1: Clinicopathological characteristics of the 52 patients

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Most of the patients presented with abnormal vaginal bleeding (40.4%). The failure to perform cervical cytology before the operation was quite high at 48.1% (25 patients) due to the lack of preoperative investigation and pathologist in the rural setup. In addition, normal cytologic smear could still be found in 15.4% (8 patients) despite the presence of invasive cervical cancer. Normal pelvic examination with no gross invasive tumor was observed in 57% of the patients.

[Table 2] shows the indications for simple hysterectomy. Most of the operations were carried out for abnormal vaginal bleeding and cervical intraepithelial neoplasia (CIN). In 21 instances, the diagnosis was abnormal vaginal bleeding. No Papanicolaou smear was performed in 17 (80.9%) women with abnormal vaginal bleeding, while 4 (19.04%) patients had normal cervical cytology. Two of three patients (66.7%) with myoma uteri, two of 5 (40%) patients with endometrial hyperplasia, and two of 3 patients (66.7%) with ovarian tumor did not have Papanicolaou smear before hysterectomy. Out of 52 cases of improper simple hysterectomy, 38 (73.1%) patients had postoperative HPE report; the remaining 14 (26.9%) patients' HPE report was not available/not sent due to lack of basic infrastructure and pathologist in that rural areas.
Table 2: Indications for simple hysterectomy (n=52)

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[Table 3] summarizes the reasons for inappropriate simple hysterectomies in the presence of invasive cervical cancer. Failure to perform preoperative Papanicolaou smear, incomplete evaluation of patients with CIN on cervical biopsy, and negative Papanicolaou smear accounted for 75% of the patients. Of the 25 patients who did not have cytologic smears performed before the operation, the preoperative diagnoses were abnormal vaginal bleeding (15 patients), myoma uteri (3), ovarian tumor (3), endometrial hyperplasia (2), and prolapse uteri (2). Of the ten patients with CIN on cervical biopsy, neither colposcopy nor conization was carried out in these patients. In eight instances, the preoperative cervical cytology was normal. In two patients, the invasive lesion was in the endocervical canal. Three of five patients with endometrial hyperplasia underwent fractional curettage with negative results. Fractional curettage was not performed in two of the patients with endometrial hyperplasia. Emergency hysterectomies were performed for one case of uterine perforation during fractional curettage, and one case of spontaneous uterine perforation of invasive cervical cancer with endometrial involvement. In one case, the cytology and cervical biopsy showed definitely invasive squamous carcinoma, a simple hysterectomy was performed for reason unknown. One patient with exophytic appearance of cervical cancer at the lower lip was misdiagnosed as cervical myoma without preoperative pathologic evaluation. Diagnostic conization should be carried out if deemed necessary but none of the patients in the study underwent cervical conization although it was indicated to rule out endocervical involvement.
Table 3: Reasons for improper simple hysterecectomy (n=52)

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 > Discussion Top


Over the past few decades, cervical cancer incidence and mortality rates reportedly have been in decline in many populations worldwide. Aside from screening, these declines have been ascribed to factors linked either to increasing average socioeconomic levels or a diminishing risk of persistent infection with high-risk HPV, resulting from improvements in genital hygiene, reduced parity, and a diminishing prevalence of sexually transmitted disease.[4] Total vaginal or abdominal hysterectomy and cervical conization continue to be an effective procedure for carcinoma in situ and microinvasive cervical carcinoma. However, simple hysterectomy has been proven inadequate for invasive carcinoma with FIGO Stage IA2–IIIB disease and results in a poor survival rate.[11]

In our study, abnormal vaginal bleeding was the most common preoperative diagnosis. Failure to perform or check cervical cytology preoperatively is a critical error found in this study as well as in other reports.[2],[12] The findings of this study indicate that most errors are preventable by strictly conforming to the established management guidelines for early detection of cervical cancer, i.e., performing routine Papanicolaou smear and evaluating patients with abnormal cytology by colposcopy if available. In India, there are marked variations in resources for cervical cancer screening; one important problem in Northeast India is that not every hospital is well equipped with colposcopy. Furthermore, the number of gynecologists experienced in colposcopy is also limited. Any abnormal or suspicious areas must be histologically confirmed by biopsy followed by routine endocervical curettage (ECC) if colposcopy is unsatisfactory. Most improper hysterectomy resulted from deviation from triage and management protocols for patients with abnormal Papanicolaou smear; a problem which can be avoided if guidelines are followed religiously.

No preoperative cytology accounted for 48.1% of the reasons for performing an inadvertent hysterectomy. In rural part of northeast India, pap tests are performed predominantly for diagnosis in the presence of problematic symptoms such as abnormal vaginal bleeding and rarely performed in asymptomatic women for routine screening, demonstrating less orientation toward secondary prevention due to limited resources. India is a land of diversity with enormous variations in sociocultural practices, health-care infrastructure, and marked variations in resources for cervical cancer screening.[13] Shortage of trained manpower and infrastructure has limited the establishment of effective, standardized, cytology-based screening program, which is currently used only for opportunistic screening in Northeast part of India. Total and subtotal hysterectomy for locally advanced cervical cancer are not uncommon in India; many cases of cervical carcinoma are treated in peripheral hospitals with total and subtotal hysterectomy even for Stage IIB-IIIB.[8]

False-negative cervical cytology is the third most common reason for inappropriate hysterectomy in this study which accounted for 15.4%. False-negative smears can be due to true-negative results, by virtue of a complete absence of cancer cells on the basis of sampling or background necrosis and inflammation in the presence of underlying invasive cancer[14],[15] or errors in screening and/or interpretation. In Northeast India, an Ayre wooden spatula is generally used to scrape cells from the cervical surface without endocervical sampling, and with this method, endocervical cells are often not present in the smears. Two of eight patients with false-negative smears in this study were postmenopausal women whose invasive lesion was in the endocervical canal. Sampling of the endocervical canal either with a saline-moistened cotton tipped applicator or an endocervical brush has been shown to decrease the false-negative rate.[16],[17]

If gross cervical lesion is visualized, irrespective of the cytology report, a biopsy is mandatory for pathologic evaluation before definite treatment, a procedure not done in two patients (3.8%) in the present study. Patients complaining of abnormal vaginal bleeding should be investigated preoperatively for the source either from the ectocervix, endocervix, or endometrium. For cases in which the ECC reveals an adenocarcinoma without a definitive diagnosis of either endocervix or endometrium origin, one should advance to perform conization, endometrial curettage, or hysteroscopy to solve this problem before hysterectomy. The combination of cervical cytology, colposcopy, endocervical sampling, cervical punch biopsies, and indicated conization is highly effective in preventing improper simple hysterectomy with cervical pathology. Similar reason for improper simple hysterectomy and survival was seen in the study conducted by Srisomboon et al. and Choi et al.


 > Conclusion Top


Total and subtotal hysterectomy for occult invasive cervical cancer is not uncommon in Northeast India. As a rule, total hysterectomy is not curative for the management of early invasive carcinoma because the paravaginal and paracervical soft tissue including the upper vagina and pelvic lymph nodes are not removed. For those reasons, supplemental treatment is usually advocated. Implementation of universal screening for cervical cancer irrespective of resources is the need of the hour. The screening effort should be linked with optimum treatment and follow-up. Improper simple hysterectomy in the presence of invasive cervical cancer can be virtually avoided if one sticks to the traditional diagnostic approach for patients with an abnormal cervical cytology. Unfortunately and undoubtedly, some cases of invasive cancer will still be detected after simple hysterectomy despite complete preoperative assessment.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
 > References Top

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Cancer Today-Global Cancer Observatory. Available from: https://gco.iarc.fr/today/home. [Last accessed on 2018 Oct 12].  Back to cited text no. 1
    
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Sreedevi A, Javed R, Dinesh A. Epidemiology of cervical cancer with special focus on India. Int J Women's Health 2015;7:405-14.  Back to cited text no. 2
    
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Sivaram S, Majumdar G, Perin D, Nessa A, Broeders M, Lynge E, et al. Population-based cancer screening programmes in low-income and middle-income countries: regional consultation of the international cancer screening network in India. The Lancet Oncol 2018;19:e113-22.  Back to cited text no. 3
    
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Bruni L, Albero G, Serrano B, Meena M, Gomez D, MunozJ, et al. ICO/IARC Information Centre on HPV and Cancer (HPV Information Centre). Human Papillomavirus and Related Diseases in India. Summary Report; 10 December, 2018. Available from: https://hpvcentre.net/statistics/reports/IND.pdf. [Last accessed on 2019 May 15].  Back to cited text no. 7
    
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Koh HK, Jeon W, Kim HJ, Wu HG, Kim K, Chie EK, et al. Outcome analysis of salvage radiotherapy for occult cervical cancer found after simple hysterectomy. Jpn J Clin Oncol 2013;43:1226-32.  Back to cited text no. 8
    
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Sharma DN, Rath GK, Kumar S, Bhatla N, Gandhi AK, Sharma P. Postoperative radiotherapy following inadvertent simple hysterectomy versus radical hysterectomy for cervical carcinoma. Asian Pac J Cancer Prev 2011;12:1537-41.  Back to cited text no. 9
    
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Sharma DN, Rath GK, Kumar S, Bhatla N, Gandhi AK, Sharma P, et al. Postoperative radiotherapy following inadvertent simple hysterectomy versus radical hysterectomy for cervical carcinoma. Asian Pac J Cancer Prev 2011;12:1537-41.  Back to cited text no. 11
    
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Denny L. Cervical cancer: prevention and treatment. Discov Med 2012;14:125-31.  Back to cited text no. 12
    
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Bhatla N, Puri K, Kriplani A, Iyer VK, Mathur SR, Mani K, et al. Adjunctive testing for cervical cancer screening in low resource settings. Aust N Z J Obstet Gynaecol 2012;52:133-9.  Back to cited text no. 13
    
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Labeit A, Peinemann F, Kedir A. Cervical cancer screening service utilization in UK. Sci Rep 2013;3:2362.  Back to cited text no. 14
    
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WHO. Guidelines for Screening and Treatment of Precancerous Lesions for Cervical Cancer Prevention. Geneva: World Health Organization; 2013.  Back to cited text no. 15
    
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Suh DH, Chung HH, Kim JW, Park NH, Song YS, Kang SB. An occult invasive cervical cancer found after a simple hysterectomy: a 10-year experience in a single institution. Int J Gynecol Cancer 2011;21:1646-53.  Back to cited text no. 16
    
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Bai H, Yuan F, Wang H, Chen J, Cui Q, Shen K. The potential for less radical surgery in women with stage IA2-IB1 cervical cancer. Int J Gynaecol Obstet 2015;130:235-40.  Back to cited text no. 17
    



 
 
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