Supravaginal hysterectomy in Curaçao prevalence and impact on screening for cervical cancer.

4184 hysterectomies were performed between 2003 and 2013, resulting in an incidence of 6.0 hysterectomies per 1000 women (95% CI 5.9–6.2). The main reason for hysterectomy was uterine leiomyomas, in 3082 cases (73.7%) ( Table 1 ). Table 1 Number and reasons for hysterectomy between 2003 and 2013 on Curaçao. Table 1. Hysterectomy Mean age and range Subtotal hysterectomy n (%) Mean age and range Uterus leiomyomatosis CIN/cervical ca. Endometrium ca./Uterus sarcoma Ovarium ca. Other causes 2003 348 46.7 (27–79) 8 (2.3) 42.5 (36–49) 273 8 7 3 49 2004 412 47.0 (25–85) 6 (1.5) 42.2 (34–50) 320 10 8 1 67 2005 360 46.8 (24–86) 16 (4.4) 46.3 (32–63) 241 14 9 0 80 2006 346 46.4 (22–77) 9 (2.6) 44.0 (30–76) 228 17 12 2 78 2007 419 46.9 (28–85) 10 (2.4) 43.7 (30–56) 304 10 14 0 81 2008 357 47.0 (27–83) 9 (2.5) 48.7 (40–72) 244 13 13 0 78 2009 393 47.1 (30–83) 12 (3.1) 44.0 (34–63) 317 16 17 5 26 2010 396 47.6 (23–85) 17 (4.3) 47.0 (23–66) 295 14 15 4 51 2011 387 48.7 (26–87) 16 (4.1) 47.9 (35–85) 280 13 16 2 60 2012 387 48.1 (26–80) 8 (2.1) 42.3 (35–49) 297 7 22 1 52 2013 379 48.3 (20–86) 12 (3.2) 45.6 (30–53) 283 13 15 4 52 Total 4184 47.3 (20–87) 123 (2.9) 44.9 (23–85) 3082 135 148 22 674 CIN = Cervical intraepithelial neoplasia; cervical ca. = cervical cancer. *The row with “other causes” represents the reasons for hysterectomy performed because of postpartum complications, endometriosis or other surgical indications where pathology report showed no abnormalities. Number and reasons for hysterectomy between 2003 and 2013 on Curaçao. CIN = Cervical intraepithelial neoplasia; cervical ca. = cervical cancer. *The row with “other causes” represents the reasons for hysterectomy performed because of postpartum complications, endometriosis or other surgical indications where pathology report showed no abnormalities. In 3.2% of the cases the reason for hysterectomy was the presence of a (pre)malignant lesion of the cervix. From the performed hysterectomies, 123 (2.9%) were supravaginal ( Table 1 ). The mean age in women with supravaginal hysterectomy was 44.9 (range 23–85). One hundred and sixty-one cervical cancer cases were diagnosed between 2003 and 2013 on Curaçao, yielding an incidence of 23.3 per 100,000 women (95% CI 19.9–27.1). No case of cervical cancer in the retained cervix was reported for 2003–2013. Six hundred hysterectomised women, mean age 58.4 year (range 39–77), completed the questionnaire ( Table 2 ). Table 2 Participant's characteristics and reasons for uterus extirpation of 600 hysterectomised women in Curaçao who completed the questionnaire. Table 2. n = 600 % Reason for hysterectomy Uterus myomatosis 357 59.5 Endometriosis 24 4.0 Complication at delivery 8 1.3 Other 176 29.4 no answer 35 5.8 

 Age when hysterectomy was performed 19–45 341 56.8 46–73 199 33.2 No answer 60 10.0 

 Year in which hysterectomy was performed 291 48.5 No answer 109 18.2 

 Awareness of intact cervix post-hysterectomy Intact 168 28.0 Not intact 75 12.5 Unawareness 332 55.3 no answer 25 4.2 

 Date of last Pap-smear < 3 years before this questionnaire 68 11.3 3–5 years before this questionnaire 73 12.2 5–10 years before this questionnaire 99 16.5 Prior hysterectomy 306 51.0 Don't remember 22 3.7 No answer 32 5.3 

 Reason why a Pap-smear is done according to the participant Early detection of any cancer in the genital tract 134 22.3 Early detection of cervical cancer 79 13.2 Detection of vaginal infection 143 23.8 Don't know the reason why a Pap-smear is done 143 23.9 no answer 101 16.8 Participant's characteristics and reasons for uterus extirpation of 600 hysterectomised women in Curaçao who completed the questionnaire. Mean age on which hysterectomy of the 562 (87.6%) participants had been performed was 43.2 years (range 19–60 years). Leiomyomatosis (59.5%) was the most common reason for a hysterectomy. This finding is in agreement with the most common reason to perform a hysterectomy as found in PALGA (73.7%). Three hundred and thirty two (55.3%) women were not aware of their cervical status post hysterectomy and 25 (4.2%) of the participants did not answer the question. Three hundred and six women had their last pap smear before the hysterectomy indicating that they had not attended for cervical-screening after the operation. Only 13.2% of the participants gave the correct answer for the reason why Pap smears are performed indicating that the majority of the interviewed women are unaware of the importance of screening ( Table 2 ).

We performed a retrospective review of all hysterectomies done on Curaçao between 2003 and 2013. In addition all new cases of cervical cancer per year were collected. We used the PALGA system, which is the nationwide database containing all pathology reports from Curaçao and the Netherlands. In both datasets, we looked for the diagnosis of cervical cancer in the cervical stump and whether previously a supravaginal hysterectomy had been performed. Also, additional information about the year of surgery, type of surgical-technique and other patient data such as age and reason for hysterectomy were collected. All data were collected anonymously. The Nation Statistics Department [Curaçao Bureau Statistiek (CBS)] provided the number of inhabitants living on Curaçao from 2003 to 2013. For the incidence calculation, we included the at-risk population, which consisted of all women ≥ 15 years in 2003–2013 (n = 692,304). Finally, 600 hysterectomised women were included in the questionnaire survey. The participants were generally women who had a history of hysterectomy and were attending the breast cancer-screening programme or information sessions organised by the prevention centre. The questionnaire was answered anonymously and included multiple-choice questions regarding awareness of retained cervix (RC), reason for hysterectomy, screenings after hysterectomy, current age and age at the time of hysterectomy. The materials were handled very attentive considering the participants' privacy. Prior to participation with the questionnaire survey, each participant received detailed information about the study objectives and an informed consent was signed. Moreover, a marketing campaign was conducted by making use of posters, information sessions, educational programmes on television, radio and on the Facebook page of Fundashon Prevenshon (FP). The study was approved by the Institutional Review Board of the medical ethics committee of Fundashon Prevenshon, Curaçao, (IRB board's approval number 0002/14).

The number of hysterectomies (6.0 per 1000 women) performed on Curaçao is high and supravaginal hysterectomy occurred in 2.9% of hysterectomised women. The majority of the participants (55.3%) were unaware of their cervical status post-hysterectomy and do not understand the reason why Pap-smears are being performed (86.8%). No cases of cancer of the cervical stump were found during our analysis. The reason to leave an intact cervix was not written in the pathology reports. Moreover we were unable to look in surgery reports, which limits our interpretation. A limitation of our study is that a number of women on Curaçao seek medical assistance abroad and consequently the here presented data may not be complete. The Caribbean region, mainly consists of an Afro and Latin population and is known for a high incidence and high mortality rate of cervical cancer. ( Murillo et al., 2008 ) Cervical cancer in the Afro female population is higher compared to the Caucasian female population. ( Moorman et al., 2013 , Beavis et al., 2017 ) A recent publication in the U.S. also reports a higher mortality rate of cervical cancer under (old) African American women. ( Beavis et al., 2017 ) Furthermore, hysterectomy rate for the African Americans is 10.1 while for the white Americans this was 4.7 ( Beavis et al., 2017 ) indicating a higher prevalence in the ethnic group from Afro descendants. Despite the high incidence of cervical cancer (23.3%) our study showed a low awareness of the need for cervical screening under the population on Curaçao. This unawareness that results in misinterpretations, maybe based on differences in social and cultural background, and may explain why women do not respond to the call for cervical cancer screening. Further investigation to the underlying factors is needed. More hysterectomies are performed in the Afro female population because of the high prevalence of leiomyomatosis. ( Moorman et al., 2013 ) In the Americas, mainly under the African and Hispanic population, the thought exists that the cervix may influence coitus favourably. However, studies have shown no evidence for this phenomenon. ( Hellström et al., 2011 , Roovers et al., 2003 , El-Toukhy et al., 2004 ) In addition in some cases, women do not want their cervix removed because of the threat of the partner breaking up the relationship after hysterectomy. ( Richter et al., 2000 , Groff et al., 2000 ) This may influence a woman's decision in preferring a supravaginal hysterectomy. Collectively these considerations suggest that psychological arguments play a role in the decision to perform a supravaginal hysterectomy. In Europe, most publications comparing total versus supravaginal hysterectomy describe the differences in physical adverse effects post-surgery. The studies that compare the effect of total and supravaginal hysterectomy on psychological and sexual satisfaction show no significant difference between the two procedures. ( Ellström Engh et al., 2010 , Risa et al., 2006 ) Given the social and cultural differences, a different approach to raise awareness for cervical screening in the women of Curaçao is required. We found no cervical carcinoma cases in the cervical stump. One important reason is that several inhabitants seek medical consultation outside Curaçao. Since proper or structured data registration is lacking in most of the Caribbean region we cannot evaluate the size of this problem. However given the prevalence of an intact cervix after hysterectomy (2.9%) and the published risk of cervical carcinoma in the cervical stump (3–9% of cervical cancer cases in the world) ( Hellström et al., 2001 , Hellström et al., 2011 ; Cléber et al., 2004 , Wahba et al., 2015 ) we aim to inform women still to continue with cervical screening after a supravaginal hysterectomy. This information must be clear to both, patient and health providers in charge of screening. Another limitation of the study is that the 600 women who filled in the questionnaire were not randomly selected from the women who underwent hysterectomy between 2003 and 2013. Despite this limitation we have the impression that the results of the questionnaire give a reasonable impression about the awareness of cervical cancer in Curaçao. The questionnaire finding that leiomyomatosis is the most important reason for hysterectomy is corroborated by the data from the national data registry system PALGA and further supports our impression. Lack of understanding of the impact of an intact cervix after hysterectomy and the necessity for Pap-smear in general are reasons why women don’t respond to cervical cancer screening invitations. As part of the strategy to achieve the eradication of cervical cancer, ( Bosch et al., 2013 ) information campaigns on these topics are necessary.

Cervical cancer is the 4th most prevalent female cancer in the world ( Instituto Catalán de Oncología [ICO], 2015 ) and in the Caribbean region it is the second most common cancer in women. ( Martin et al., 2013 ) Studies have stated that this cancer can be eradicated. ( Bosch, 2012 ) However, important reasons for why this preventable cancer cannot yet be eradicated, are the low uptake of HPV vaccination programmes, lack of proper implementation of screening programmes on the global level and/or the high numbers of none responders to the screening programme. ( Bruni et al., 2016 , de San José et al., 2012 ) The need to investigate reasons why women do not attend for cervical cancer screening and especially after having undergone a hysterectomy, was identified as part of the process for the preparation for the HPV research on Curaçao. When women were approached to participate with a pilot screening, many refused to participate because of their history of hysterectomy. When asked for the type of hysterectomy procedure and follow up actions, most of them were unaware whether their cervix had been preserved or not. Therefore they never attended for cervical cancer screening anymore because they assumed that this was not necessary. Hysterectomy is one of the most common surgeries performed worldwide ( Moorman et al., 2013 , Garry, 2005 ) and different surgical techniques are used for this procedure. Supravaginal hysterectomy is one of the surgical modalities in which the surgeon removes the uterus but leaves the cervix in place. Some studies refer that it can be considered less morbid than total hysterectomy. ( Zouhair et al., 2012 ) This surgical procedure may be performed for women when the reason for hysterectomy is a benign disorder. Women should continue screening for cervical cancer when a supravaginal hysterectomy has been performed. If they are not well informed about the procedure, misunderstanding and misinterpretations about continuing with cervical cancer screening will occur. Cancer of the preserved cervical stump contributes to 3–9% of cervical cancer cases in the world. ( Hellström et al., 2001 , Hellström et al., 2011 , Cléber et al., 2004 , Wahba et al., 2015 ) The present study was set up with the aim to obtain insight in the proportion of supravaginal hysterectomies in women from Curaçao, and to investigate the level of awareness of the need of continuing cervical cancer screening in case of a preserved cervix.