The Association between Oral Contraceptive Pills and Subtypes of Ovarian Cancer: A Systematic Review and Meta-Analysis
Abstract
Introduction: Limited studies have been conducted on the effect of oral contraceptive pills on the subgroups of ovarian cancer, so we decided that conduct a systematic review and meta-analysis to investigate the effect of preventive pills on ovarian cancer subgroups.
methods: Scopus, PubMed, Web of Science and EMBASE were searched to identify studies on the association between OCPs and subtypes of ovarian cancer from January 1, 2000, through February 5, 2023. The pooled relative risk (RR) and odds ratio (OR) were used to measure this relationship.
Results: A total of 48 studies were included. In the association between ever-use compared with never-use of OCPs and ovarian cancer risk, the pooled RR in cohort studies was 0.69 [95% CI: 0.61, 0.78], and the pooled OR of the case-control studies was 0.64 [95% CI: 0.59, 0.69]. For the relationship between OCPs and subtypes of ovarian cancer, there is a significant inverse relationship between OCPs and serous 0.72 [95% CI: 0.23, 0.82] and endometrioid 0.74 [95% CI: 0.64, 0.86], but no association between OCPs and clear cell 0.84 [95% CI: 0.60, 1.16] and mucinous 0.80 [95% CI: 0.63, 1.01].
Conclusions: This study shows a statistically significant inverse relationship between ever-use compared to never-use of OCPs and ovarian cancer risk. Also shows a statistically significant inverse relationship between serous and endometrioid cancer and OCPs, but no association between OCPs and clear cell and mucinous.
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2.Chiaffarino F, Pelucchi C, Parazzini F, Negri E, Franceschi S ,Talamini R, et al. Reproductive and hormonal factors and ovarian cancer. Annals of Oncology. 2001; 12:337-41.
3.Hemmingsen CH, Kjaer SK, Bennetsen AKK, Dehlendorff C, Baandrup L. The association of reproductive factors with risk of non-epithelial ovarian cancer and comparison with serous ovarian cancer. Gynecologic oncology. 2021; 162:469-74.
4.Cook LS, Pestak CR, Leung AC, Steed H, Nation J, Swenerton K, et al. Combined oral contraceptive use before the first birth and epithelial ovarian cancer risk. British journal of cancer. 2017; 116:265-9.
5.Delort L, Kwiatkowski F, Chalabi N, Satih S, Bignon YJ, Bernard-Gallon DJ. Central Adiposity as a Major Risk Factor of Ovarian Cancer. Anticancer research. 2009; 29:5229-34.
6.Dorjgochoo T, Shu XO, Li HL, Qian HZ, Yang G, Cai H, et al. Use of oral contraceptives, intrauterine devices and tubal sterilization and cancer risk in a large prospective study, from 1996 to 2006. International journal of cancer. 2009; 124:2442-9.
7.Faber MT, Jensen A, Frederiksen K ,Glud E, Høgdall E, Høgdall C, et al. Oral contraceptive use and impact of cumulative intake of estrogen and progestin on risk of ovarian cancer. Cancer causes & control : CCC. 2013; 24:2197-206.
8.Ferris JS, Daly MB, Buys SS, Genkinger JM, Liao Y, Terry MB. Oral contraceptive and reproductive risk factors for ovarian cancer within sisters in the breast cancer family registry. British journal of cancer. 2014; 110:1074-80.
9.Gay GMW, Lim JSP, Chay WY, Chow KY, Tan MH, Lim WY. Reproductive factors, adiposity, breastfeeding and their associations with ovarian cancer in an Asian cohort. Cancer Causes & Control. 2015; 26:1561-73.
10.Gazibara T, Filipović A, Kesić V, Kisiĉ-Tepavcević D, Pekmezović T. Risk factors for epithelial ovarian cancer in the female population of Belgrade, Serbia: a case-control study. Vojnosanitetski pregled. 2013; 70:1097- 102.
11.Greggi S, Parazzini F, Paratore MP, Chatenoud L, Legge F, Mancuso S, La Vecchia C. Risk factors for ovarian cancer in central Italy. Gynecologic oncology. .79:50-4 ;2000
12.Greer JB, Modugno F, Allen GO, Ness RB. Androgenic progestins in oral contraceptives and the risk of epithelial ovarian cancer. Obstetrics and gynecology. 2005; 105:731-40.
13.Haem E, Heydari ST, Zare N, Lankarani KB, Barooti E, Sharif F. Ovarian cancer risk factors in a defined population using rare event logistic regression. Middle East Journal of Cancer. 2015; 6:1-9.
14.Hannaford PC, Selvaraj S, Elliott AM, Angus V, Iversen L, Lee AJ. Cancer risk among users of oral contraceptives :cohort data from the Royal College of General Practitioner’s oral contraception study. BMJ (Clinical research ed). 2007; 335:651.
15.Heinemann LAJ, Lewis MA, Kühl-Habich D, Braendle W, Moehner S, Raff T. Use of Oral Contraceptives and Risk of Cancer of the Uterine Corpus or Ovary. Two Case-Control Studies. Geburtshilfe und Frauenheilkunde. 2003; 63:1018-26.
16.Huusom LD, Frederiksen K, Høgdall EVS, Glud E, Christensen L, Høgdall CK, et al. Association of reproductive factors, oral contraceptive use and selected lifestyle factors with the risk of ovarian borderline tumors: A Danish case-control study. Cancer Causes and Control. 2006; 17:821-9.
17.Iversen L, Fielding S, Lidegaard Ø, Mørch LS, Skovlund CW, Hannaford PC. Association between contemporary hormonal contraception and ovarian cancer in women of reproductive age in Denmark: prospective, nationwide cohort study. BMJ (Clinical research ed). 2018; 362:k3609.
18.Jordan SJ, Green AC, Whiteman DC, Moore SP, Bain CJ, Gertig DM, Webb PM. Serous ovarian, fallopian tube and primary peritoneal cancers: A comparative epidemiological analysis. International journal of cancer. 2008; 122:1598-603. 19.Karlsson T, Johansson T, Höglund J, Ek WE, Johansson Å. Time-dependent effects of oral contraceptive use on breast, ovarian and endometrial cancers. Cancer research. 2020.
20.Kumle M, Weiderpass E, Braaten T, Adami HO, Lund E. Risk for invasive and borderline epithelial ovarian neoplasias following use of hormonal contraceptives: the Norwegian Swedish Women’s Lifestyle and Health Cohort Study. British journal of cancer. 2004; 90:1386- 91.
21.Le DC, Kubo T, Fujino Y, Sokal DC, Vach TH, Pham TM, Matsuda S. Reproductive factors in relation to ovarian cancer: a case-control study in Northern Vietnam. Contraception. 2012; 86:494-9.
22.Li K, Hüsing A, Fortner RT, Tjønneland A, Hansen L, Dossus L, et al. An epidemiologic risk prediction model for ovarian cancer in Europe: The EPIC study. British journal of cancer. 2015; 112:1257-65.
23.Lurie G, Wilkens LR, Thompson PJ, McDuffie KE, Carney ME, Terada KY, Goodman MT. Combined oral contraceptive use and epithelial ovarian cancer risk - Time-related effects. Epidemiology (Cambridge, Mass). 2008; 19:237-43.
24.Modugno F, Ness RB, Wheeler JE. Reproductive risk factors for epithelial ovarian cancer according to histologic type and invasiveness. Annals of epidemiology. 2001; 11:568-74.
25.Moorman PG, Alberg AJ, Bandera EV, Barnholtz- Sloan J, Bondy M, Cote ML, et al. Reproductive factors and ovarian cancer risk in African-American women. Annals of epidemiology. 2016; 26:654-62.
26.Moorman PG, Calingaert B, Palmieri RT, Iversen ES, Bentley RC, Halabi S, et al. Hormonal risk factors for ovarian cancer in premenopausal and postmenopausal women. American journal of epidemiology. 2008; 167:1059-69.
27.Ness RB, Dodge RC, Edwards RP, Baker JA, Moysich KB. Contraception methods, beyond oral contraceptives and tubal ligation, and risk of ovarian cancer. Annals of epidemiology. 2011; 21:188-96.
28.Ness RB, Grisso JA, Klapper J ,Schlesselman JJ, Silberzweig S, Vergona R, et al. Risk of ovarian cancer in relation to estrogen and progestin dose and use characteristics of oral contraceptives. American journal of epidemiology. 2000; 152:233-41.
29.Ness RB, Grisso JA, Vergona R, Klapper J, Morgan M, Wheeler JE. Oral contraceptives, other methods of contraception, and risk reduction for ovarian cancer. Epidemiology (Cambridge, Mass). 2001; 12:307-12.
30.Pasalich M, Su D, Binns CW, Lee AH. Reproductive factors for ovarian cancer in southern Chinese women. Journal of gynecologic oncology. 2013; 24:135-40.
31.Parazzini F, Chatenoud L, Chiantera V, Benzi G, Surace M, La Vecchia C. Population attributable risk for ovarian cancer. European Journal of Cancer. 2000; 36:520-4.
32.Parazzini F, Chiaffarino F, Negri E, Surace M, Benzi G, Franceschi S, et al. Risk factors for different histological types of ovarian cancer. International Journal of Gynecological Cancer. 2004; 14:431-6.
33.Pelucchi C, Galeone C, Talamini R, Bosetti C, Montella M, Negri E, et al. Lifetime ovulatory cycles and ovarian cancer risk in 2 Italian case-control studies. American journal of obstetrics and gynecology. 2007; 196:83.e1-.e7.
34.Purdie DM, Siskind V, Bain CJ, Webb PM, Green AC. Reproduction-related risk factors for mucinous and nonmucinous epithelial ovarian cancer. American journal of epidemiology. 2001; 153:860-4.
35.Rosenblatt KA, Gao DL, Ray RM, Nelson ZC, Wernli KJ, Li WJ, Thomas DB. Oral contraceptives and the risk of all cancers combined and site-specific cancers in Shanghai. Cancer Causes & Control. 2009; 20:27-34.
36.Rosner BA, Colditz GA, Webb PM, Hankinson SE. Mathematical models of ovarian cancer incidence. Epidemiology (Cambridge, Mass). 2005; 16:508-15.
37.Royar J, Becher H, Chang-Claude J .Low-dose oral contraceptives: protective effect on ovarian cancer risk. International journal of cancer. 2001; 95:370-4.
38.Siskind V, Green A, Bain C, Purdie D. Beyond ovulation: oral contraceptives and epithelial ovarian cancer. Epidemiology (Cambridge, Mass). 2000; 11:106- 10. 39.Soegaard M, Jensen A, Høgdall E, Christensen L, Høgdall C, Blaakaer J, Kjaer SK. Different risk factor profiles for mucinous and nonmucinous ovarian cancer: results from the Danish MALOVA study. Cancer epidemiology, biomarkers & prevention : a publication of the American Association for Cancer Research, cosponsored by the American Society of Preventive Oncology. 2007; 16:1160-6.
40.Wilailak S, Vipupinyo C, Suraseranivong V, Chotivanich K, Kietpeerakool C, Tanapat Y, et al .Depot medroxyprogesterone acetate and epithelial ovarian cancer: a multicentre case–control study. BJOG: An International Journal of Obstetrics & Gynaecology. 2012; 119:672-7.
41.Tavani A, Ricci E, La Vecchia C, Surace M, Benzi G, Parazzini F, Franceschi S. Influence of menstrual and reproductive factors on ovarian cancer risk in women with and without family history of breast or ovarian cancer. International journal of epidemiology. 2000; 29:799-802.
42.Tsilidis KK, Allen NE, Key TJ, Dossus L, Lukanova A, Bakken K, et al. Oral contraceptive use and reproductive factors and risk of ovarian cancer in the European Prospective Investigation into Cancer and Nutrition. British journal of cancer. 2011; 105:1436-42.
43.Tung KH, Goodman MT, Wu AH, McDuffie K, Wilkens LR, Kolonel LN, et al. Reproductive factors and epithelial ovarian cancer risk by histologic type: A multiethnic case-control study. American journal of epidemiology. 2003; 158:629-38.
44.Urban M, Banks E, Egger S, Canfell K, O’Connell D, Beral V ,Sitas F. Injectable and oral contraceptive use and cancers of the breast, cervix, ovary, and endometrium in black South African women: case-control study. PLoS medicine. 2012; 9:e1001182.
45.Vessey M, Painter R. Oral contraceptive use and cancer. Findings in a large cohort study, 1968-2004. British journal of cancer. 2006; 95:385-9.
46.Wu AH, Pearce CL, Lee AW, Tseng CC, Jotwani A, Patel P, Pike MC. Timing of births and oral contraceptive use influences ovarian cancer risk. International journal of cancer. 2017; 141:2392-9.
47.Yang HP, Trabert B, Murphy MA, Sherman ME, Sampson JN, Brinton LA, et al. Ovarian cancer risk factors by histologic subtypes in the NIH-AARP diet and health study. International journal of cancer. 2012; 131:938-48.
48.Zhang M ,Lee AH, Binns CW. Reproductive and dietary risk factors for epithelial ovarian cancer in China. Gynecologic oncology. 2004; 92:320-6.
2.Chiaffarino F, Pelucchi C, Parazzini F, Negri E, Franceschi S ,Talamini R, et al. Reproductive and hormonal factors and ovarian cancer. Annals of Oncology. 2001; 12:337-41.
3.Hemmingsen CH, Kjaer SK, Bennetsen AKK, Dehlendorff C, Baandrup L. The association of reproductive factors with risk of non-epithelial ovarian cancer and comparison with serous ovarian cancer. Gynecologic oncology. 2021; 162:469-74.
4.Cook LS, Pestak CR, Leung AC, Steed H, Nation J, Swenerton K, et al. Combined oral contraceptive use before the first birth and epithelial ovarian cancer risk. British journal of cancer. 2017; 116:265-9.
5.Delort L, Kwiatkowski F, Chalabi N, Satih S, Bignon YJ, Bernard-Gallon DJ. Central Adiposity as a Major Risk Factor of Ovarian Cancer. Anticancer research. 2009; 29:5229-34.
6.Dorjgochoo T, Shu XO, Li HL, Qian HZ, Yang G, Cai H, et al. Use of oral contraceptives, intrauterine devices and tubal sterilization and cancer risk in a large prospective study, from 1996 to 2006. International journal of cancer. 2009; 124:2442-9.
7.Faber MT, Jensen A, Frederiksen K ,Glud E, Høgdall E, Høgdall C, et al. Oral contraceptive use and impact of cumulative intake of estrogen and progestin on risk of ovarian cancer. Cancer causes & control : CCC. 2013; 24:2197-206.
8.Ferris JS, Daly MB, Buys SS, Genkinger JM, Liao Y, Terry MB. Oral contraceptive and reproductive risk factors for ovarian cancer within sisters in the breast cancer family registry. British journal of cancer. 2014; 110:1074-80.
9.Gay GMW, Lim JSP, Chay WY, Chow KY, Tan MH, Lim WY. Reproductive factors, adiposity, breastfeeding and their associations with ovarian cancer in an Asian cohort. Cancer Causes & Control. 2015; 26:1561-73.
10.Gazibara T, Filipović A, Kesić V, Kisiĉ-Tepavcević D, Pekmezović T. Risk factors for epithelial ovarian cancer in the female population of Belgrade, Serbia: a case-control study. Vojnosanitetski pregled. 2013; 70:1097- 102.
11.Greggi S, Parazzini F, Paratore MP, Chatenoud L, Legge F, Mancuso S, La Vecchia C. Risk factors for ovarian cancer in central Italy. Gynecologic oncology. .79:50-4 ;2000
12.Greer JB, Modugno F, Allen GO, Ness RB. Androgenic progestins in oral contraceptives and the risk of epithelial ovarian cancer. Obstetrics and gynecology. 2005; 105:731-40.
13.Haem E, Heydari ST, Zare N, Lankarani KB, Barooti E, Sharif F. Ovarian cancer risk factors in a defined population using rare event logistic regression. Middle East Journal of Cancer. 2015; 6:1-9.
14.Hannaford PC, Selvaraj S, Elliott AM, Angus V, Iversen L, Lee AJ. Cancer risk among users of oral contraceptives :cohort data from the Royal College of General Practitioner’s oral contraception study. BMJ (Clinical research ed). 2007; 335:651.
15.Heinemann LAJ, Lewis MA, Kühl-Habich D, Braendle W, Moehner S, Raff T. Use of Oral Contraceptives and Risk of Cancer of the Uterine Corpus or Ovary. Two Case-Control Studies. Geburtshilfe und Frauenheilkunde. 2003; 63:1018-26.
16.Huusom LD, Frederiksen K, Høgdall EVS, Glud E, Christensen L, Høgdall CK, et al. Association of reproductive factors, oral contraceptive use and selected lifestyle factors with the risk of ovarian borderline tumors: A Danish case-control study. Cancer Causes and Control. 2006; 17:821-9.
17.Iversen L, Fielding S, Lidegaard Ø, Mørch LS, Skovlund CW, Hannaford PC. Association between contemporary hormonal contraception and ovarian cancer in women of reproductive age in Denmark: prospective, nationwide cohort study. BMJ (Clinical research ed). 2018; 362:k3609.
18.Jordan SJ, Green AC, Whiteman DC, Moore SP, Bain CJ, Gertig DM, Webb PM. Serous ovarian, fallopian tube and primary peritoneal cancers: A comparative epidemiological analysis. International journal of cancer. 2008; 122:1598-603. 19.Karlsson T, Johansson T, Höglund J, Ek WE, Johansson Å. Time-dependent effects of oral contraceptive use on breast, ovarian and endometrial cancers. Cancer research. 2020.
20.Kumle M, Weiderpass E, Braaten T, Adami HO, Lund E. Risk for invasive and borderline epithelial ovarian neoplasias following use of hormonal contraceptives: the Norwegian Swedish Women’s Lifestyle and Health Cohort Study. British journal of cancer. 2004; 90:1386- 91.
21.Le DC, Kubo T, Fujino Y, Sokal DC, Vach TH, Pham TM, Matsuda S. Reproductive factors in relation to ovarian cancer: a case-control study in Northern Vietnam. Contraception. 2012; 86:494-9.
22.Li K, Hüsing A, Fortner RT, Tjønneland A, Hansen L, Dossus L, et al. An epidemiologic risk prediction model for ovarian cancer in Europe: The EPIC study. British journal of cancer. 2015; 112:1257-65.
23.Lurie G, Wilkens LR, Thompson PJ, McDuffie KE, Carney ME, Terada KY, Goodman MT. Combined oral contraceptive use and epithelial ovarian cancer risk - Time-related effects. Epidemiology (Cambridge, Mass). 2008; 19:237-43.
24.Modugno F, Ness RB, Wheeler JE. Reproductive risk factors for epithelial ovarian cancer according to histologic type and invasiveness. Annals of epidemiology. 2001; 11:568-74.
25.Moorman PG, Alberg AJ, Bandera EV, Barnholtz- Sloan J, Bondy M, Cote ML, et al. Reproductive factors and ovarian cancer risk in African-American women. Annals of epidemiology. 2016; 26:654-62.
26.Moorman PG, Calingaert B, Palmieri RT, Iversen ES, Bentley RC, Halabi S, et al. Hormonal risk factors for ovarian cancer in premenopausal and postmenopausal women. American journal of epidemiology. 2008; 167:1059-69.
27.Ness RB, Dodge RC, Edwards RP, Baker JA, Moysich KB. Contraception methods, beyond oral contraceptives and tubal ligation, and risk of ovarian cancer. Annals of epidemiology. 2011; 21:188-96.
28.Ness RB, Grisso JA, Klapper J ,Schlesselman JJ, Silberzweig S, Vergona R, et al. Risk of ovarian cancer in relation to estrogen and progestin dose and use characteristics of oral contraceptives. American journal of epidemiology. 2000; 152:233-41.
29.Ness RB, Grisso JA, Vergona R, Klapper J, Morgan M, Wheeler JE. Oral contraceptives, other methods of contraception, and risk reduction for ovarian cancer. Epidemiology (Cambridge, Mass). 2001; 12:307-12.
30.Pasalich M, Su D, Binns CW, Lee AH. Reproductive factors for ovarian cancer in southern Chinese women. Journal of gynecologic oncology. 2013; 24:135-40.
31.Parazzini F, Chatenoud L, Chiantera V, Benzi G, Surace M, La Vecchia C. Population attributable risk for ovarian cancer. European Journal of Cancer. 2000; 36:520-4.
32.Parazzini F, Chiaffarino F, Negri E, Surace M, Benzi G, Franceschi S, et al. Risk factors for different histological types of ovarian cancer. International Journal of Gynecological Cancer. 2004; 14:431-6.
33.Pelucchi C, Galeone C, Talamini R, Bosetti C, Montella M, Negri E, et al. Lifetime ovulatory cycles and ovarian cancer risk in 2 Italian case-control studies. American journal of obstetrics and gynecology. 2007; 196:83.e1-.e7.
34.Purdie DM, Siskind V, Bain CJ, Webb PM, Green AC. Reproduction-related risk factors for mucinous and nonmucinous epithelial ovarian cancer. American journal of epidemiology. 2001; 153:860-4.
35.Rosenblatt KA, Gao DL, Ray RM, Nelson ZC, Wernli KJ, Li WJ, Thomas DB. Oral contraceptives and the risk of all cancers combined and site-specific cancers in Shanghai. Cancer Causes & Control. 2009; 20:27-34.
36.Rosner BA, Colditz GA, Webb PM, Hankinson SE. Mathematical models of ovarian cancer incidence. Epidemiology (Cambridge, Mass). 2005; 16:508-15.
37.Royar J, Becher H, Chang-Claude J .Low-dose oral contraceptives: protective effect on ovarian cancer risk. International journal of cancer. 2001; 95:370-4.
38.Siskind V, Green A, Bain C, Purdie D. Beyond ovulation: oral contraceptives and epithelial ovarian cancer. Epidemiology (Cambridge, Mass). 2000; 11:106- 10. 39.Soegaard M, Jensen A, Høgdall E, Christensen L, Høgdall C, Blaakaer J, Kjaer SK. Different risk factor profiles for mucinous and nonmucinous ovarian cancer: results from the Danish MALOVA study. Cancer epidemiology, biomarkers & prevention : a publication of the American Association for Cancer Research, cosponsored by the American Society of Preventive Oncology. 2007; 16:1160-6.
40.Wilailak S, Vipupinyo C, Suraseranivong V, Chotivanich K, Kietpeerakool C, Tanapat Y, et al .Depot medroxyprogesterone acetate and epithelial ovarian cancer: a multicentre case–control study. BJOG: An International Journal of Obstetrics & Gynaecology. 2012; 119:672-7.
41.Tavani A, Ricci E, La Vecchia C, Surace M, Benzi G, Parazzini F, Franceschi S. Influence of menstrual and reproductive factors on ovarian cancer risk in women with and without family history of breast or ovarian cancer. International journal of epidemiology. 2000; 29:799-802.
42.Tsilidis KK, Allen NE, Key TJ, Dossus L, Lukanova A, Bakken K, et al. Oral contraceptive use and reproductive factors and risk of ovarian cancer in the European Prospective Investigation into Cancer and Nutrition. British journal of cancer. 2011; 105:1436-42.
43.Tung KH, Goodman MT, Wu AH, McDuffie K, Wilkens LR, Kolonel LN, et al. Reproductive factors and epithelial ovarian cancer risk by histologic type: A multiethnic case-control study. American journal of epidemiology. 2003; 158:629-38.
44.Urban M, Banks E, Egger S, Canfell K, O’Connell D, Beral V ,Sitas F. Injectable and oral contraceptive use and cancers of the breast, cervix, ovary, and endometrium in black South African women: case-control study. PLoS medicine. 2012; 9:e1001182.
45.Vessey M, Painter R. Oral contraceptive use and cancer. Findings in a large cohort study, 1968-2004. British journal of cancer. 2006; 95:385-9.
46.Wu AH, Pearce CL, Lee AW, Tseng CC, Jotwani A, Patel P, Pike MC. Timing of births and oral contraceptive use influences ovarian cancer risk. International journal of cancer. 2017; 141:2392-9.
47.Yang HP, Trabert B, Murphy MA, Sherman ME, Sampson JN, Brinton LA, et al. Ovarian cancer risk factors by histologic subtypes in the NIH-AARP diet and health study. International journal of cancer. 2012; 131:938-48.
48.Zhang M ,Lee AH, Binns CW. Reproductive and dietary risk factors for epithelial ovarian cancer in China. Gynecologic oncology. 2004; 92:320-6.
| Files | ||
| Issue | Vol 10 No 3 (2024) | |
| Section | Articles | |
| Keywords | ||
| subtypes of ovarian Cancer, OCPs, Systematic Review, meta-analysis | ||
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How to Cite
1.
Khodamoradi F. The Association between Oral Contraceptive Pills and Subtypes of Ovarian Cancer: A Systematic Review and Meta-Analysis. JBE. 2024;10(3):281-310.
