The Role of Micronutrients in Human Papillomavirus Infection, Cervical Dysplasia, and Neoplasm
Abstract
:1. Introduction
2. Materials and Methods
2.1. Study Design and Search Strategy
2.2. Inclusion Criteria
2.3. Study Selection
2.4. Data Extraction and Data Synthesis
3. Results
3.1. Calcium
3.2. Zinc
3.3. Iron
3.4. Selenium
3.5. Folate and Vitamin B12
3.6. Carotenoids
3.7. Vitamin A
3.8. Vitamin C
3.9. Vitamin D
3.10. Vitamin E
3.11. Vitamin K
4. Limitations of the Study
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Egawa, N.; Egawa, K.; Griffin, H.M.; Doorbar, J. Human Papillomaviruses; Epithelial Tropisms, and the Development of Neoplasia. Viruses 2015, 7, 3863–3890. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Garutti, P.; Montori, S.; Bazzan, E.; Tarabbia, C. Gender differences in the epidemiology and prevention of human papillomavirus (HPV) and HPV-related diseases. Ital. J. Gend.-Specif. Med. 2018, 4, 152–156. [Google Scholar] [CrossRef]
- Momenimovahed, Z.; Mazidimoradi, A.; Maroofi, P.; Allahqoli, L.; Salehiniya, H.; Alkatout, I. Global, regional and national burden, incidence, and mortality of cervical cancer. Cancer Rep. 2023, 6, e1756. [Google Scholar] [CrossRef]
- Dijkstra, M.G.; Snijders, P.J.F.; Arbyn, M.; Rijkaart, D.C.; Berkhof, J.; Meijer, C.J.L.M. Cervical cancer screening: On the way to a shift from cytology to full molecular screening. Ann. Oncol. 2014, 25, 927–935. [Google Scholar] [CrossRef] [PubMed]
- Giuliano, A.R.; Nyitray, A.G.; Kreimer, A.R.; Pierce Campbell, C.M.; Goodman, M.T.; Sudenga, S.L.; Monsonego, J.; Franceschi, S. EUROGIN 2014 roadmap: Differences in human papillomavirus infection natural history, transmission and human papillomavirus-related cancer incidence by gender and anatomic site of infection. Int. J. Cancer 2015, 136, 2752–2760. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Castellsagué, X. Natural history and epidemiology of HPV infection and cervical cancer. Gynecol. Oncol. 2008, 110, S4–S7. [Google Scholar] [CrossRef] [PubMed]
- de Sanjosé, S.; Brotons, M.; Pavón, M.A. The natural history of human papillomavirus infection. Best Pract. Res. Clin. Obstet. Gynaecol. 2018, 47, 2–13. [Google Scholar] [CrossRef]
- Karimi-Zarchi, M.; Allahqoli, L.; Nehmati, A.; Kashi, A.M.; Taghipour-Zahir, S.; Alkatout, I. Can the prophylactic quadrivalent HPV vaccine be used as a therapeutic agent in women with CIN? A randomized trial. BMC Public Health 2020, 20, 274. [Google Scholar] [CrossRef]
- Kechagias, K.S.; Kalliala, I.; Bowden, S.J.; Athanasiou, A.; Paraskevaidi, M.; Paraskevaidis, E.; Dillner, J.; Nieminen, P.; Strander, B.; Sasieni, P.; et al. Role of human papillomavirus (HPV) vaccination on HPV infection and recurrence of HPV related disease after local surgical treatment: Systematic review and meta-analysis. BMJ 2022, 378, e070135. [Google Scholar] [CrossRef]
- Papadimitriou, N.; Markozannes, G.; Kanellopoulou, A.; Critselis, E.; Alhardan, S.; Karafousia, V.; Kasimis, J.C.; Katsaraki, C.; Papadopoulou, A.; Zografou, M.; et al. An umbrella review of the evidence associating diet and cancer risk at 11 anatomical sites. Nat. Commun. 2021, 12, 4579. [Google Scholar] [CrossRef]
- Shenkin, A.; Cuerda, C.; Berger, M.M. About micronutrient shortage and definition of deficiency. Nutr. Clin. Pract. 2022, 37, 966–967. [Google Scholar] [CrossRef] [PubMed]
- Shenkin, A. The key role of micronutrients. Clin. Nutr. 2006, 25, 1–13. [Google Scholar] [CrossRef] [PubMed]
- Alpha-Tocopherol, Beta Carotene Cancer Prevention Study Group. The Effect of Vitamin E and Beta Carotene on the Incidence of Lung Cancer and Other Cancers in Male Smokers. N. Engl. J. Med. 1994, 330, 1029–1035. [Google Scholar] [CrossRef]
- Tomita, L.; Longatto-Filho, A.; Costa, M.C.; Andreoli, M.A.A.; Villa, L.L.; Franco, E.; Cardoso, M.A. Diet and serum micronutrients in relation to cervical neoplasia and cancer among low-income Brazilian women. Int. J. Cancer 2010, 126, 703–714. [Google Scholar] [CrossRef] [PubMed]
- Myung, S.-K.; Ju, W.; Kim, S.-C.; Kim, H.; for the Korean Meta-Analysis (KORMA) Study Group. Vitamin or antioxidant intake (or serum level) and risk of cervical neoplasm: A meta-analysis. BJOG Int. J. Obstet. Gynaecol. 2011, 118, 1285–1291. [Google Scholar] [CrossRef] [PubMed]
- Cao, D.; Shen, K.; Li, Z.; Xu, Y.; Wu, D. Association between vitamin C Intake and the risk of cervical neoplasia: A meta-analysis. Nutr. Cancer 2016, 68, 48–57. [Google Scholar] [CrossRef]
- Anghileri, L.J. Magnesium, calcium and cancer. Magnes. Res. 2009, 22, 247–255. [Google Scholar] [CrossRef] [Green Version]
- Ermak, G.; Davies, K.J. Calcium and oxidative stress: From cell signaling to cell death. Mol. Immunol. 2002, 38, 713–721. [Google Scholar] [CrossRef]
- Zemel, M.B.; Sun, X. Dietary Calcium and Dairy Products Modulate Oxidative and Inflammatory Stress in Mice and Humans. J. Nutr. 2008, 138, 1047–1052. [Google Scholar] [CrossRef] [Green Version]
- Itoh, M.; Oh-Ishi, S.; Hatao, H.; Leeuwenburgh, C.; Selman, C.; Ohno, H.; Kizaki, T.; Nakamura, H.; Matsuoka, T. Effects of dietary calcium restriction and acute exercise on the antioxidant enzyme system and oxidative stress in rat diaphragm. Am. J. Physiol. Integr. Comp. Physiol. 2004, 287, R33–R38. [Google Scholar] [CrossRef] [Green Version]
- Bruckbauer, A.; Zemel, M.B. Dietary Calcium and Dairy Modulation of Oxidative Stress and Mortality in aP2-Agouti and Wild-type Mice. Nutrients 2009, 1, 50–70. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Sherman, L.; Schlegel, R. Serum- and calcium-induced differentiation of human keratinocytes is inhibited by the E6 oncoprotein of human papillomavirus type 16. J. Virol. 1996, 70, 3269–3279. [Google Scholar] [CrossRef] [Green Version]
- Tsutsumi, K.; Iwatake, H.; Kuwabara, D.; Hyodo, A.; Kobayashi, T.; Koizuka, I.; Kato, I. Effects of Calcium on HPV16 Gene Transcription in Cultured Laryngeal Epithelial Cells. Nippon. Jibiinkoka Gakkai Kaiho 2000, 103, 727–733. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Sengupta, A.; Mallick, R.; Dutta, S.R.; Sarkar, R. Serum calcium level in patients with carcinoma of the cervix in relation to menstrual status. Eur. J. Gynaecol. Oncol. 1989, 10, 153–155. [Google Scholar]
- Hwang, J.H.; Kim, M.K.; Lee, J.K. Dietary Supplements Reduce the Risk of Cervical Intraepithelial Neoplasia. Int. J. Gynecol. Cancer 2010, 20, 398–403. [Google Scholar] [CrossRef] [PubMed]
- Liu, T.; Soong, S.J.; Wilson, N.P.; Craig, C.B.; Cole, P.; Macaluso, M.; Butterworth, C.E. A case control study of nutritional factors and cervical dysplasia. Cancer Epidemiol. Biomark. Prev. 1993, 2, 525–530. [Google Scholar]
- He, A.-J.; Chen, C.; Jia, M.; Fan, R.-Q. Dietary Calcium Intake and HPV Infection Status Among American Women: A Secondary Analysis from National Health and Nutrition Examination Survey (NHANES) Data Set of 2003–2016. Experiment 2020, 26, e921571. [Google Scholar] [CrossRef]
- Michalczyk, K.; Cymbaluk-Płoska, A. The Role of Zinc and Copper in Gynecological Malignancies. Nutrients 2020, 12, 3732. [Google Scholar] [CrossRef]
- York, D.M.; Darden, T.A.; Pedersen, L.G.; Anderson, M.W. Molecular modeling studies suggest that zinc ions inhibit HIV-1 protease by binding at catalytic aspartates. Environ. Health Perspect. 1993, 101, 246–250. [Google Scholar] [CrossRef]
- Yuasa, K.; Naganuma, A.; Sato, K.; Ikeda, M.; Kato, N.; Takagi, H.; Mori, M. Zinc is a negative regulator of hepatitis C virus RNA replication. Liver Int. 2006, 26, 1111–1118. [Google Scholar] [CrossRef]
- Feng, P.; Li, T.-L.; Guan, Z.-X.; Franklin, R.B.; Costello, L.C. Direct effect of zinc on mitochondrial apoptogenesis in prostate cells. Prostate 2002, 52, 311–318. [Google Scholar] [CrossRef] [Green Version]
- Bae, S.N.; Lee, Y.S.; Kim, M.Y.; Kim, J.D.; Park, L.O. Antiproliferative and apoptotic effects of zinc–citrate compound (CIZAR®) on human epithelial ovarian cancer cell line, OVCAR-3. Gynecol. Oncol. 2006, 103, 127–136. [Google Scholar] [CrossRef] [PubMed]
- Park, K.-S.; Ahn, Y.; Kim, J.-A.; Yun, M.-S.; Seong, B.L.; Choi, K.-Y. Extracellular zinc stimulates ERK-dependent activation of p21Cip/WAF1 and inhibits proliferation of colorectal cancer cells. Br. J. Pharmacol. 2002, 137, 597–607. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Grail, A.; Norval, M. Copper and Zinc Levels in Serum from Patients with Abnormalities of the Uterine Cervix. Acta Obstet. Gynecol. Scand. 1986, 65, 443–447. [Google Scholar] [CrossRef] [PubMed]
- Naidu, M.S.K.; Suryakar, A.N.; Swami, S.C.; Katkam, R.V.; Kumbar, K.M. Oxidative stress and antioxidant status in cervical cancer patients. Indian J. Clin. Biochem. 2007, 22, 140–144. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Cunzhi, H.; Jiexian, J.; Xianwen, Z.; Jingang, G.; Shumin, Z.; Lili, D. Serum and Tissue Levels of Six Trace Elements and Copper/Zinc Ratio in Patients with Cervical Cancer and Uterine Myoma. Biol. Trace Elem. Res. 2003, 94, 113–122. [Google Scholar] [CrossRef] [PubMed]
- Chen, C.A.; Hwang, J.L.; Kuo, T.L.; Hsieh, C.Y.; Huang, S.C. Serum copper and zinc levels in patients with cervical cancer. J. Formos. Med. Assoc. 1990, 89, 677–682. [Google Scholar]
- Kim, J.H.; Bae, S.N.; Lee, C.W.; Song, M.J.; Lee, S.J.; Yoon, J.H.; Lee, K.H.; Hur, S.Y.; Park, T.C.; Park, J.S. A pilot study to investigate the treatment of cervical human papillomavirus infection with zinc-citrate compound (CIZAR®). Gynecol. Oncol. 2011, 122, 303–306. [Google Scholar] [CrossRef]
- Barchitta, M.; Maugeri, A.; Quattrocchi, A.; Agrifoglio, O.; Scalisi, A.; Agodi, A. The Association of Dietary Patterns with High-Risk Human Papillomavirus Infection and Cervical Cancer: A Cross-Sectional Study in Italy. Nutrients 2018, 10, 469. [Google Scholar] [CrossRef] [Green Version]
- Xiao, D.; Li, W.; Zhang, W.-H.; Wen, Z.; Dai, B.; Mo, W.; Qiu, S.; Yang, L. Dietary Zinc, Copper, and Selenium Intake and High-Risk Human Papillomavirus Infection among American Women: Data from NHANES 2011–2016. Nutr. Cancer 2022, 74, 1958–1967. [Google Scholar] [CrossRef]
- Ayatollahi, H.; Rajabi, E.; Yekta, Z.; Jalali, Z. Efficacy of Oral Zinc Sulfate Supplementation on Clearance of Cervical Human Papillomavirus (HPV); A Randomized Controlled Clinical Trial. Asian Pac. J. Cancer Prev. 2022, 23, 1285–1290. [Google Scholar] [CrossRef] [PubMed]
- Torti, S.V.; Manz, D.H.; Paul, B.T.; Blanchette-Farra, N.; Torti, F.M. Iron and Cancer. Annu. Rev. Nutr. 2018, 38, 97–125. [Google Scholar] [CrossRef]
- Ito, H.; Takagi, Y.; Ando, Y.; Kubo, A.; Hashimoto, S.; Tsutsui, F.; Kurihara, S. Serum Ferritin Levels in Patients with Cervical Cancer. Obstet. Gynecol. 1980, 55, 358–362. [Google Scholar] [CrossRef] [PubMed]
- Siegel, E.M.; Patel, N.; Lu, B.; Lee, J.-H.; Nyitray, A.G.; Huang, X.; Villa, L.L.; Franco, E.L.; Giuliano, A.R. Circulating Biomarkers of Iron Storage and Clearance of Incident Human Papillomavirus Infection. Cancer Epidemiol. Biomark. Prev. 2012, 21, 859–865. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Labunskyy, V.M.; Hatfield, D.L.; Gladyshev, V.N. Selenoproteins: Molecular Pathways and Physiological Roles. Physiol. Rev. 2014, 94, 739–777. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Patrick, L. Selenium biochemistry and cancer: A review of the literature. Altern. Med. Rev. 2004, 9, 239–258. [Google Scholar]
- Guillin, O.M.; Vindry, C.; Ohlmann, T.; Chavatte, L. Selenium, Selenoproteins and Viral Infection. Nutrients 2019, 11, 2101. [Google Scholar] [CrossRef] [Green Version]
- Sundström, H. Annual variation of serum selenium in patients with gynaecological cancer during 1978–1983 in Finland, a low selenium area. Int. J. Vitam. Nutr. Res. 1985, 55, 433–438. [Google Scholar]
- Subramanyam, D.; Subbaiah, K.V.; Rajendra, W.; Lokanatha, V. Serum selenium concentration and antioxidant activity in cervical cancer patients before and after treatment. Exp. Oncol. 2013, 35, 97–100. [Google Scholar]
- Obhielo, E.; Ezeanochie, M.; Okonkwo, A.; Gharoro, E. The Relationship between the Serum Level of Selenium and Cervical Intraepithelial Neoplasia: A Comparative Study in a Population of Nigerian Women. Asian Pac. J. Cancer Prev. 2019, 20, 1433–1436. [Google Scholar] [CrossRef] [Green Version]
- Karamali, M.; Nourgostar, S.; Zamani, A.; Vahedpoor, Z.; Asemi, Z. The favourable effects of long-term selenium supplementation on regression of cervical tissues and metabolic profiles of patients with cervical intraepithelial neoplasia: A randomised, double-blind, placebo-controlled trial. Br. J. Nutr. 2015, 114, 2039–2045. [Google Scholar] [CrossRef] [Green Version]
- Abike, F.; Engin, A.B.; Dunder, I.; Tapisiz, O.L.; Aslan, C.; Kutluay, L. Human papilloma virus persistence and neopterin, folate and homocysteine levels in cervical dysplasias. Arch. Gynecol. Obstet. 2011, 284, 209–214. [Google Scholar] [CrossRef]
- Popescu, N.; DiPaolo, J.; Amsbaugh, S. Integration sites of human papillomavirus 18 DNA sequences on HeLa cell chromosomes. Cytogenet. Genome Res. 1987, 44, 58–62. [Google Scholar] [CrossRef]
- Hernandez, B.Y.; McDuffie, K.; Wilkens, L.R.; Kamemoto, L.; Goodman, M.T. Diet and premalignant lesions of the cervix: Evidence of a protective role for folate, riboflavin, thiamin, and vitamin B12. Cancer Causes Control 2003, 14, 859–870. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wang, J.T.; Ma, X.C.; Cheng, Y.Y.; Ding, L.; Zhou, Q. A case-control study on the association between folate and cervical cancer. Zhonghua Liu Xing Bing Xue Za Zhi 2006, 27, 424–427. [Google Scholar] [PubMed]
- Wang, Z.; Yang, A.; Yang, J.; Zhao, W.; Wang, Z.; Wang, W.; Wang, J.; Song, J.; Li, L.; Lv, W.; et al. Dietary nutrient intake related to higher grade cervical intraepithelial neoplasia risk: A Chinese population-based study. Nutr. Metab. 2020, 17, 100. [Google Scholar] [CrossRef]
- Zhao, W.; Hao, M.; Wang, Y.; Feng, N.; Wang, Z.; Wang, W.; Wang, J.; Ding, L. Association between folate status and cervical intraepithelial neoplasia. Eur. J. Clin. Nutr. 2016, 70, 837–842. [Google Scholar] [CrossRef] [Green Version]
- Piyathilake, C.J.; Macaluso, M.; Alvarez, R.D.; Bell, W.C.; Heimburger, D.C.; Partridge, E.E. Lower Risk of Cervical Intraepithelial Neoplasia in Women with High Plasma Folate and Sufficient Vitamin B12 in the Post-Folic Acid Fortification Era. Cancer Prev. Res. 2009, 2, 658–664. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Piyathilake, C.J.; Henao, O.L.; Macaluso, M.; Cornwell, P.E.; Meleth, S.; Heimburger, D.C.; Partridge, E.E. Folate Is Associated with the Natural History of High-Risk Human Papillomaviruses. Cancer Res. 2004, 64, 8788–8793. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Piyathilake, C.J.; Macaluso, M.; Chambers, M.M.; Badiga, S.; Siddiqui, N.R.; Bell, W.C.; Edberg, J.C.; Partridge, E.E.; Alvarez, R.D.; Johanning, G.L. Folate and Vitamin B12 May Play a Critical Role in Lowering the HPV 16 Methylation–Associated Risk of Developing Higher Grades of CIN. Cancer Prev. Res. 2014, 7, 1128–1137. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ragasudha, P.N.; Thulaseedharan, J.V.; Wesley, R.; Jayaprakash, P.G.; Lalitha, P.; Pillai, M.R. A Case-Control Nutrigenomic Study on the Synergistic Activity of Folate and Vitamin B12 in Cervical Cancer Progression. Nutr. Cancer 2012, 64, 550–558. [Google Scholar] [CrossRef]
- Kwanbunjan, K.; Saengkar, P.; Cheeramakara, C.; Tangjitgamol, S.; Chitcharoenrung, K. Vitamin B12 status of Thai women with neoplasia of the cervix uteri. Southeast Asian J. Trop. Med. Public Health 2006, 37 (Suppl. S3), 178–183. [Google Scholar] [PubMed]
- Alberg, A.J.; Selhub, J.; Shah, K.V.; Viscidi, R.P.; Comstock, G.W.; Helzlsouer, K.J. The risk of cervical cancer in relation to serum concentrations of folate, vitamin B12, and homocysteine. Cancer Epidemiol. Biomark. Prev. 2000, 9, 761–764. [Google Scholar]
- Li, Q.; Ding, L.; Jing, N.; Liu, C.; Yang, Z.; Chen, F.; Hou, L.; Wang, J. Folate deficiency and aberrant DNA methylation and expression of FHIT gene were associated with cervical pathogenesis. Oncol. Lett. 2018, 15, 1963–1972. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bai, L.-X.; Wang, J.-T.; Ding, L.; Jiang, S.-W.; Kang, H.-J.; Gao, C.-F.; Chen, X.; Chen, C.; Zhou, Q. Folate Deficiency and FHIT Hypermethylation and HPV 16 Infection Promote Cervical Cancerization. Asian Pac. J. Cancer Prev. 2014, 15, 9313–9317. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Asemi, Z.; Vahedpoor, Z.; Jamilian, M.; Bahmani, F.; Esmaillzadeh, A. Effects of long-term folate supplementation on metabolic status and regression of cervical intraepithelial neoplasia: A randomized, double-blind, placebo-controlled trial. Nutrition 2016, 32, 681–686. [Google Scholar] [CrossRef]
- Sabihi, S.; Vahedpoor, Z.; Saraf-Bank, S.; Nourian, M. Effects of folate supplementation on recurrence and metabolic status of cervical intraepithelial neoplasia grade 2/3 in overweight and obese women: A randomized double-blind placebo-controlled trial. Eur. J. Clin. Nutr. 2022, 76, 666–670. [Google Scholar] [CrossRef]
- Batieha, A.M.; Armenian, H.K.; Norkus, E.P.; Morris, J.S.; Spate, V.E.; Comstock, G.W. Serum micronutrients and the subsequent risk of cervical cancer in a population-based nested case-control study. Cancer Epidemiol. Biomark. Prev. 1993, 2, 335–339. [Google Scholar]
- Harris, R.W.; Forman, D.; Doll, R.; Vessey, M.P.; Wald, N.J. Cancer of the cervix uteri and vitamin A. Br. J. Cancer 1986, 53, 653–659. [Google Scholar] [CrossRef] [Green Version]
- Palan, P.R.; Mikhail, M.S.; Goldberg, G.L.; Basu, J.; Runowicz, C.D.; Romney, S.L. Plasma levels of beta-carotene, lycopene, canthaxanthin, retinol, and alpha- and tau-tocopherol in cervical intraepithelial neoplasia and cancer. Clin. Cancer Res. 1996, 2, 181–185. [Google Scholar]
- García-Closas, R.; Castellsagué, X.; Bosch, X.; González, C.A. The role of diet and nutrition in cervical carcinogenesis: A review of recent evidence. Int. J. Cancer 2005, 117, 629–637. [Google Scholar] [CrossRef] [PubMed]
- Niranjana, R.; Gayathri, R.; Mol, S.N.; Sugawara, T.; Hirata, T.; Miyashita, K.; Ganesan, P. Carotenoids modulate the hallmarks of cancer cells. J. Funct. Foods 2015, 18, 968–985. [Google Scholar] [CrossRef]
- Nagata, C.; Shimizu, H.; Yoshikawa, H.; Noda, K.; Nozawa, S.; Yajima, A.; Sekiya, S.; Sugimori, H.; Hirai, Y.; Kanazawa, K.; et al. Serum carotenoids and vitamins and risk of cervical dysplasia from a case–control study in Japan. Br. J. Cancer 1999, 81, 1234–1237. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Peterson, C.; Sedjo, R.L.; Davis, F.G.; Beam, C.A.; Giuliano, A.R. Combined Antioxidant Carotenoids and the Risk of Persistent Human Papillomavirus Infection. Nutr. Cancer 2010, 62, 728–733. [Google Scholar] [CrossRef]
- Sedjo, R.L.; Roe, D.J.; Abrahamsen, M.; Harris, R.B.; Craft, N.; Baldwin, S.; Giuliano, A.R. Vitamin A, carotenoids, and risk of persistent oncogenic human papillomavirus infection. Cancer Epidemiol. Biomark. Prev. 2002, 11, 876–884. [Google Scholar]
- Sedjo, R.L.; Papenfuss, M.R.; Craft, N.E.; Giuliano, A.R. Effect of plasma micronutrients on clearance of oncogenic human papillomavirus (HPV) infection (United States). Cancer Causes Control 2003, 14, 319–326. [Google Scholar] [CrossRef] [PubMed]
- Tomita, L.Y.; Roteli-Martins, C.M.; Villa, L.L.; Franco, E.L.; Cardoso, M.A. Associations of dietary dark-green and deep-yellow vegetables and fruits with cervical intraepithelial neoplasia: Modification by smoking. Br. J. Nutr. 2011, 105, 928–937. [Google Scholar] [CrossRef] [Green Version]
- Kanetsky, P.A.; Gammon, M.D.; Mandelblatt, J.; Zhang, Z.; Ramsey, E.; Dnistrian, A.; Norkus, E.P.; Wright, T.C. Dietary intake and blood levels of lycopene: Association with cervical dysplasia among non-hispanic, black women. Nutr. Cancer 1998, 31, 31–40. [Google Scholar] [CrossRef]
- Van Eenwyk, J.; Davis, F.G.; Bowen, P.E. Dietary and serum carotenoids and cervical intraepithelial neoplasia. Int. J. Cancer 1991, 48, 34–38. [Google Scholar] [CrossRef]
- De Vet, H.C.W.; Knipschild, P.G.; Grol, M.E.C.; Schouten, H.J.A.; Sturmans, F. The Role of Beta-Carotene and Other Dietary Factors in the Aetiology of Cervical Dysplasia: Results of a Case-Control Study. Leuk. Res. 1991, 20, 603–610. [Google Scholar] [CrossRef]
- de Vet, H.C.; Knipschild, P.G.; Willebrand, D.; Schouten, H.J.; Sturmans, F. The effect of beta-carotene on the regression and progression of cervical dysplasia: A clinical experiment. J. Clin. Epidemiol. 1991, 44, 273–283. [Google Scholar] [CrossRef] [PubMed]
- Romney, S.L.; Ho, G.Y.; Palan, P.R.; Basu, J.; Kadish, A.S.; Klein, S.; Mikhail, M.; Hagan, R.; Chang, C.J.; Burk, R.D. Effects of β-Carotene and Other Factors on Outcome of Cervical Dysplasia and Human Papillomavirus Infection. Gynecol. Oncol. 1997, 65, 483–492. [Google Scholar] [CrossRef] [PubMed]
- Fujii, T.; Takatsuka, N.; Nagata, C.; Matsumoto, K.; Oki, A.; Furuta, R.; Maeda, H.; Yasugi, T.; Kawana, K.; Mitsuhashi, A.; et al. Association between carotenoids and outcome of cervical intraepithelial neoplasia: A prospective cohort study. Int. J. Clin. Oncol. 2013, 18, 1091–1101. [Google Scholar] [CrossRef]
- Giuliano, A.R.; Siegel, E.M.; Roe, D.J.; Ferreira, S.; Baggio, M.L.; Galan, L.; Duarte-Franco, E.; Villa, L.L.; Rohan, T.E.; Marshall, J.R.; et al. Dietary Intake and Risk of Persistent Human Papillomavirus (HPV) Infection: The Ludwig-McGill HPV Natural History Study. J. Infect. Dis. 2003, 188, 1508–1516. [Google Scholar] [CrossRef] [Green Version]
- Goodman, M.T.; Shvetsov, Y.B.; McDuffie, K.; Wilkens, L.R.; Zhu, X.; Franke, A.A.; Bertram, C.C.; Kessel, B.; Bernice, M.; Sunoo, C.; et al. Hawaii Cohort Study of Serum Micronutrient Concentrations and Clearance of Incident Oncogenic Human Papillomavirus Infection of the Cervix. Cancer Res. 2007, 67, 5987–5996. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Schiff, M.A.; Patterson, R.E.; Baumgartner, R.N.; Masuk, M.; van Asselt-King, L.; Wheeler, C.M.; Becker, T.M. Serum carotenoids and risk of cervical intraepithelial neoplasia in Southwestern American Indian women. Cancer Epidemiol. Biomark. Prev. 2001, 10, 1219–1222. [Google Scholar]
- Potischman, N.; Brinton, L.A.; Stacewicz-Sapuntzakis, M.; Jones, C.J.; De Britton, R.C.; Herrero, R.; Reeves, W.C.; Brenes, M.M.; Tenorio, F.; Gaitan, E. A Case-Control Study of Nutrient Status and Invasive Cervical Cancer: II. Serologic Indicators. Am. J. Epidemiol. 1991, 134, 1347–1355. [Google Scholar] [CrossRef]
- Shimizu, H.; Nagata, C.; Komatsu, S.; Morita, N.; Higashiiwai, H.; Sugahara, N.; Hisamichi, S. Decreased serum retinol levels in women with cervical dysplasia. Br. J. Cancer 1996, 73, 1600–1604. [Google Scholar] [CrossRef] [Green Version]
- Huang, X.; Chen, C.; Zhu, F.; Zhang, Y.; Feng, Q.; Li, J.; Yu, Q.; Zhong, Y.; Luo, S.; Gao, J. Association between Dietary Vitamin A and HPV Infection in American Women: Data from NHANES 2003–2016. BioMed Res. Int. 2020, 2020, 4317610. [Google Scholar] [CrossRef] [Green Version]
- Yeo, A.S.S.; Schiff, M.A.; Montoya, G.; Masuk, M.; van Asselt-King, L.; Becker, T.M. Serum Micronutrients and Cervical Dysplasia inSouthwestern American Indian Women. Nutr. Cancer 2000, 38, 141–150. [Google Scholar] [CrossRef]
- Eleutério, J.J.; Giraldo, P.C.; Gonçalves, A.K.; Eleutério, R.M.N.; Barbosa, R.D.C.C.; Cavalcante, D.I.M. The Risk of High-Grade Squamous Intraepithelial Lesions in Women with Low Serum Levels of Vitamin A. Gynecol. Obstet. Investig. 2014, 78, 235–238. [Google Scholar] [CrossRef] [PubMed]
- Kim, J.; Kim, M.K.; Lee, J.K.; Kim, J.-H.; Son, S.K.; Song, E.-S.; Lee, K.B.; Lee, J.P.; Lee, J.M.; Yun, Y.M. Intakes of Vitamin A, C, and E, and β-Carotene Are Associated with Risk of Cervical Cancer: A Case-Control Study in Korea. Nutr. Cancer 2010, 62, 181–189. [Google Scholar] [CrossRef] [PubMed]
- Ghosh, C.; Baker, J.A.; Moysich, K.B.; Rivera, R.; Brasure, J.R.; McCann, S.E. Dietary Intakes of Selected Nutrients and Food Groups and Risk of Cervical Cancer. Nutr. Cancer 2008, 60, 331–341. [Google Scholar] [CrossRef]
- Zheng, C.; Zheng, Z.; Chen, W. Association between serum vitamin C and HPV infection in American women: A cross-sectional study. BMC Women’s Health 2022, 22, 404. [Google Scholar] [CrossRef] [PubMed]
- Ziegler, R.G.; Jones, C.J.; Brinton, L.A.; Norman, S.A.; Mallin, K.; Levine, R.S.; Lehman, H.F.; Hamman, R.F.; Trumble, A.C.; Rosenthal, J.F.; et al. Diet and the risk of in situ cervical cancer among white women in the United States. Cancer Causes Control 1991, 2, 17–29. [Google Scholar] [CrossRef]
- Brock, K.E.; Mock, P.A.; Berry, G.; MacLennan, R.; Truswell, A.S.; Brinton, L.A. Nutrients in Diet and Plasma and Risk of In Situ Cervical Cancer. Gynecol. Oncol. 1988, 80, 580–585. [Google Scholar] [CrossRef]
- Herrero, R.; Potischman, N.; Brinton, L.A.; Reeves, W.C.; Brenes, M.M.; Tenorio, F.; De Britton, R.C.; Gaitan, E. A Case-Control Study of Nutrient Status and Invasive Cervical Cancer: I. Dietary Indicators. Am. J. Epidemiol. 1991, 134, 1335–1346. [Google Scholar] [CrossRef]
- Ghosh, J.; Das, S. Evaluation of vitamin A and C status in normal and malignant conditions and their possible role in cancer prevention. Jpn. J. Cancer Res. 1985, 76, 1174–1178. [Google Scholar]
- Shannon, J.; Thomas, D.B.; Ray, R.M.; Kestin, M.; Koetsawang, A.; Koetsawang, S.; Chitnarong, K.; Kiviat, N.; Kuypers, J. Dietary risk factors for invasive and in-situ cervical carcinomas in Bangkok, Thailand. Cancer Causes Control 2002, 13, 691–699. [Google Scholar] [CrossRef]
- Basu, J.; Palan, P.R.; Vermund, S.H.; Goldberg, G.L.; Burk, R.D.; Romney, S.L. Plasma ascorbic acid and beta-carotene levels in women evaluated for HPV infection, smoking, and cervix dysplasia. Cancer Detect. Prev. 1991, 15, 165–170. [Google Scholar]
- DeLuca, H.F. History of the discovery of vitamin D and its active metabolites. BoneKEy Rep. 2014, 3, 479. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hosono, S.; Matsuo, K.; Kajiyama, H.; Hirose, K.; Suzuki, T.; Kawase, T.; Kidokoro, K.; Nakanishi, T.; Hamajima, N.; Kikkawa, F.; et al. Association between dietary calcium and vitamin D intake and cervical carcinogenesis among Japanese women. Eur. J. Clin. Nutr. 2010, 64, 400–409. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Al-Sofiani, M.E.; Jammah, A.; Racz, M.; Khawaja, R.A.; Hasanato, R.; El-Fawal, H.A.N.; Mousa, S.A.; Mason, D.L. Effect of Vitamin D Supplementation on Glucose Control and Inflammatory Response in Type II Diabetes: A Double Blind, Randomized Clinical Trial. Int. J. Endocrinol. Metab. 2015, 13, e22604. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Vahedpoor, Z.; Jamilian, M.; Bahmani, F.; Aghadavod, E.; Karamali, M.; Kashanian, M.; Asemi, Z. Effects of Long-Term Vitamin D Supplementation on Regression and Metabolic Status of Cervical Intraepithelial Neoplasia: A Randomized, Double-Blind, Placebo-Controlled Trial. Horm. Cancer 2017, 8, 58–67. [Google Scholar] [CrossRef] [PubMed]
- Vahedpoor, Z.; Mahmoodi, S.; Samimi, M.; Gilasi, H.R.; Bahmani, F.; Soltani, A.; Esfahani, M.S.; Asemi, Z. Long-Term Vitamin D Supplementation and the Effects on Recurrence and Metabolic Status of Cervical Intraepithelial Neoplasia Grade 2 or 3: A Randomized, Double-Blind, Placebo-Controlled Trial. Ann. Nutr. Metab. 2018, 72, 151–160. [Google Scholar] [CrossRef] [PubMed]
- Schulte-Uebbing, C.; Schlett, S.; Craiut, I.; Antal, L.; Olah, H. Chronical cervical infections and dysplasia (CIN I, CIN II): Vaginal vitamin D (high dose) treatment. Dermato-Endocrinology 2014, 6, e983684. [Google Scholar] [CrossRef] [Green Version]
- Özgü, E.; Yılmaz, N.; Başer, E.; Güngör, T.; Erkaya, S.; İbrahim Yakut, H. Could 25-OH vitamin D deficiency be a reason for HPV infection persistence in cervical premalignant lesions? J. Exp. Ther. Oncol. 2016, 11, 177–180. [Google Scholar]
- Abraham, A.; Kattoor, A.J.; Saldeen, T.; Mehta, J.L. Vitamin E and its anticancer effects. Crit. Rev. Food Sci. Nutr. 2019, 59, 2831–2838. [Google Scholar] [CrossRef]
- Yang, C.S.; Luo, P.; Zeng, Z.; Wang, H.; Malafa, M.; Suh, N. Vitamin E and cancer prevention: Studies with different forms of tocopherols and tocotrienols. Mol. Carcinog. 2020, 59, 365–389. [Google Scholar] [CrossRef]
- Zhang, Y.-Y.; Lu, L.; Abliz, G.; Mijit, F. Serum Carotenoid, Retinol and Tocopherol Concentrations and Risk of Cervical Cancer among Chinese Women. Asian Pac. J. Cancer Prev. 2015, 16, 2981–2986. [Google Scholar] [CrossRef] [Green Version]
- Guo, L.; Zhu, H.; Lin, C.; Che, J.; Tian, X.; Han, S.; Zhao, H.; Zhu, Y.; Mao, D. Associations between antioxidant vitamins and the risk of invasive cervical cancer in Chinese women: A case-control study. Sci. Rep. 2015, 5, 13607. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Palan, P.R.; Woodall, A.L.; Anderson, P.S.; Mikhail, M.S. α-Tocopherol and α-tocopheryl quinone levels in cervical intraepithelial neoplasia and cervical cancer. Am. J. Obstet. Gynecol. 2004, 190, 1407–1410. [Google Scholar] [CrossRef]
- Palan, P.R.; Mikhail, M.S.; Shaban, D.W.; Romney, S.L. Plasma concentrations of coenzyme Q10 and tocopherols in cervical intraepithelial neoplasia and cervical cancer. Eur. J. Cancer Prev. 2003, 12, 321–326. [Google Scholar] [CrossRef] [PubMed]
- Goodman, M.T.; Kiviat, N.; McDuffie, K.; Hankin, J.H.; Hernandez, B.; Wilkens, L.R.; Franke, A.; Kuypers, J.; Kolonel, L.N.; Nakamura, J.; et al. The association of plasma micronutrients with the risk of cervical dysplasia in Hawaii. Cancer Epidemiol. Biomark. Prev. 1998, 7, 537–544. [Google Scholar]
- Siegel, E.M.; Craft, N.E.; Duarte-Franco, E.; Villa, L.L.; Franco, E.L.; Giuliano, A.R. Associations between serum carotenoids and tocopherols and type-specific HPV persistence: The Ludwig-McGill cohort study. Int. J. Cancer 2007, 120, 672–680. [Google Scholar] [CrossRef] [Green Version]
- Markowska, A.; Antoszczak, M.; Markowska, J.; Huczyński, A. Role of Vitamin K in Selected Malignant Neoplasms in Women. Nutrients 2022, 14, 3401. [Google Scholar] [CrossRef]
- Shibayama-Imazu, T.; Aiuchi, T.; Nakaya, K. Vitamin K2-Mediated Apoptosis in Cancer Cells: Role of Mitochondrial Transmembrane Potential. In Vitamins & Hormones; Elsevier: Amsterdam, The Netherlands, 2008; pp. 211–226. [Google Scholar]
- Jiang, Y.; Xu, S.; Lan, J.; Zhang, J.; Chen, T. Dietary Vitamin K Intake and HPV-Infection Status Among American Women: A Secondary Analysis from National Health and Nutrition Examination Survey Data from 2003 to 2016. Int. J. Public Health 2022, 67, 1604616. [Google Scholar] [CrossRef]
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Ferrari, F.A.; Magni, F.; Bosco, M.; Biancotto, G.; Zorzato, P.C.; Laganà, A.S.; Chiantera, V.; Raffaelli, R.; Franchi, M.; Uccella, S.; et al. The Role of Micronutrients in Human Papillomavirus Infection, Cervical Dysplasia, and Neoplasm. Healthcare 2023, 11, 1652. https://doi.org/10.3390/healthcare11111652
Ferrari FA, Magni F, Bosco M, Biancotto G, Zorzato PC, Laganà AS, Chiantera V, Raffaelli R, Franchi M, Uccella S, et al. The Role of Micronutrients in Human Papillomavirus Infection, Cervical Dysplasia, and Neoplasm. Healthcare. 2023; 11(11):1652. https://doi.org/10.3390/healthcare11111652
Chicago/Turabian StyleFerrari, Filippo Alberto, Francesca Magni, Mariachiara Bosco, Giulia Biancotto, Pier Carlo Zorzato, Antonio Simone Laganà, Vito Chiantera, Ricciarda Raffaelli, Massimo Franchi, Stefano Uccella, and et al. 2023. "The Role of Micronutrients in Human Papillomavirus Infection, Cervical Dysplasia, and Neoplasm" Healthcare 11, no. 11: 1652. https://doi.org/10.3390/healthcare11111652
APA StyleFerrari, F. A., Magni, F., Bosco, M., Biancotto, G., Zorzato, P. C., Laganà, A. S., Chiantera, V., Raffaelli, R., Franchi, M., Uccella, S., & Garzon, S. (2023). The Role of Micronutrients in Human Papillomavirus Infection, Cervical Dysplasia, and Neoplasm. Healthcare, 11(11), 1652. https://doi.org/10.3390/healthcare11111652