Factors, associated with elevated concentration of soluble carbonic anhydrase IX in plasma of women with cervical dysplasia
Language English Country England, Great Britain Media electronic
Document type Journal Article, Research Support, Non-U.S. Gov't
PubMed
36100684
PubMed Central
PMC9470728
DOI
10.1038/s41598-022-19492-y
PII: 10.1038/s41598-022-19492-y
Knihovny.cz E-resources
- MeSH
- Antigens, Neoplasm metabolism MeSH
- Uterine Cervical Dysplasia * MeSH
- Carbonic Anhydrase IX metabolism MeSH
- Carbonic Anhydrases * MeSH
- Humans MeSH
- Uterine Cervical Neoplasms * MeSH
- Aged MeSH
- Check Tag
- Humans MeSH
- Aged MeSH
- Female MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Names of Substances
- Antigens, Neoplasm MeSH
- CA9 protein, human MeSH Browser
- Carbonic Anhydrase IX MeSH
- Carbonic Anhydrases * MeSH
UNLABELLED: Precancerous lesions of human cervix uteri have a tendency for regression or progression. In cervical intraepithelial neoplasia grade 2 (CINII) case there is an uncertainty if a lesion will progress or regress. The carbonic anhydrase IX (CAIX) enzyme is overexpressed in cervical cancer which is more sensitive to radiotherapy. CAIX is associated with poor prognosis in solid hypoxic tumors. The aim of this study was to determine factors related to elevated soluble CAIX (s-CAIX) in high-grade intraepithelial lesion (HSIL) cases. METHODS: Patients diagnosed with HSIL (N = 77) were included into the research group whereas without HSIL (N = 72)-the control group. Concentration of the soluble CAIX (s-CAIX) in plasma was determined by the DIANA ligand-antibody-based method. C. trachomatis was detected from cervical samples by PCR. Primary outcomes were risk factors elevating s-CAIX level in HSIL group. Non-parametric statistical analysis methods were used to calculate correlations. RESULTS: The s-CAIX level in patients with HSIL was elevated among older participants (rs = 0.27, p = 0.04) and with C. trachomatis infection (p = 0.028). Among heavy smokers with HSIL, the concentration of s-CAIX was higher in older women (rs = 0.52, p = 0.005), but was not related to the age of heavy smokers' controls (τ = 0.18 p = 0.40). CONCLUSION: The concentration of s-CAIX was higher among older, heavy smoking and diagnosed with C. trachomatis patients. All these factors increased the risk for HSIL progression.
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Bray F, et al. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA. Cancer J. Clin. 2018;68:394–424. doi: 10.3322/caac.21492. PubMed DOI
Brisson M, et al. Impact of HPV vaccination and cervical screening on cervical cancer elimination: A comparative modelling analysis in 78 low-income and lower-middle-income countries. The Lancet. 2020;395:575–590. doi: 10.1016/S0140-6736(20)30068-4. PubMed DOI PMC
Yusupov A, et al. The nonavalent vaccine: A review of high-risk HPVs and a plea to the CDC. Am. J. Stem Cells. 2019;8:52–64. PubMed PMC
Sangrajrang S, et al. Comparative accuracy of Pap smear and HPV screening in Ubon Ratchathani in Thailand. Papillomavirus Res. Amst. Neth. 2017;3:30–35. doi: 10.1016/j.pvr.2016.12.004. PubMed DOI PMC
Human papillomavirus (HPV) test compared to the Papanicolaou (Pap) test to screen for cervical cancer. /CD008587/GYNAECA_human-papillomavirus-hpv-test-compared-papanicolaou-pap-test-screen-cervical-cancer 10.1002/14651858.CD008587.pub2.
Berretta R, et al. Risk of preterm delivery associated with prior treatment of cervical precancerous lesion according to the depth of the cone. Dis. Markers. 2013;35:721–726. doi: 10.1155/2013/686027. PubMed DOI PMC
Bjørge T, Skare GB, Bjørge L, Tropé A, Lönnberg S. Adverse pregnancy outcomes after treatment for cervical intraepithelial neoplasia. Obstet. Gynecol. 2016;128:1265–1273. doi: 10.1097/AOG.0000000000001777. PubMed DOI
Bevis KS, Biggio JR. Cervical conization and the risk of preterm delivery. Am. J. Obstet. Gynecol. 2011;205:19–27. doi: 10.1016/j.ajog.2011.01.003. PubMed DOI
van Noord-Zaadstra BM, et al. Delaying childbearing: Effect of age on fecundity and outcome of pregnancy. Br. Med. J. 1991;302:1361–1365. doi: 10.1136/bmj.302.6789.1361. PubMed DOI PMC
Cox JT, Schiffman M, Solomon D. Prospective follow-up suggests similar risk of subsequent cervical intraepithelial neoplasia grade 2 or 3 among women with cervical intraepithelial neoplasia grade 1 or negative colposcopy and directed biopsy. Am. J. Obstet. Gynecol. 2003;188:1406–1412. doi: 10.1067/mob.2003.461. PubMed DOI
McCredie MR, et al. Natural history of cervical neoplasia and risk of invasive cancer in women with cervical intraepithelial neoplasia 3: A retrospective cohort study. Lancet Oncol. 2008;9:425–434. doi: 10.1016/S1470-2045(08)70103-7. PubMed DOI
Mailath-Pokorny M, Schwameis R, Grimm C, Reinthaller A, Polterauer S. Natural history of cervical intraepithelial neoplasia in pregnancy: postpartum histo-pathologic outcome and review of the literature. BMC Pregnancy Childbirth. 2016;16:74. doi: 10.1186/s12884-016-0861-8. PubMed DOI PMC
Holowaty P, Miller AB, Rohan T, To T. Natural history of dysplasia of the uterine cervix. J. Natl. Cancer Inst. 1999;91:252–258. doi: 10.1093/jnci/91.3.252. PubMed DOI
Schlecht NF, et al. Human papillomavirus infection and time to progression and regression of cervical intraepithelial neoplasia. J. Natl. Cancer Inst. 2003;95:1336–1343. doi: 10.1093/jnci/djg037. PubMed DOI
Melnikow J, et al. Surveillance after treatment for cervical intraepithelial neoplasia: outcomes, costs, and cost-effectiveness. Obstet. Gynecol. 2010;116:1158–1170. doi: 10.1097/AOG.0b013e3181f88e72. PubMed DOI
van Ballegooijen M, Koopmanschap MA, Habbema JDF. The management of cervical intra-epithelial neoplasia (CIN): Extensiveness and costs in The Netherlands. Eur. J. Cancer. 1995;31:1672–1676. doi: 10.1016/0959-8049(95)00243-C. PubMed DOI
Renshaw AA, DiNisco SA, Minter LJ, Cibas ES. A more accurate measure of the false-negative rate of Papanicolaou smear screening is obtained by determining the false-negative rate of the rescreening process. Cancer. 1997;81:272–276. doi: 10.1002/(SICI)1097-0142(19971025)81:5<272::AID-CNCR3>3.0.CO;2-P. PubMed DOI
Koonmee S, et al. False-negative rate of Papanicolaou Testing: A national survey from the thai society of cytology. Acta Cytol. 2017;61:434–440. doi: 10.1159/000478770. PubMed DOI
Won K-H, et al. Impact of age on the false negative rate of human papillomavirus DNA test in patients with atypical squamous cells of undetermined significance. Obstet. Gynecol. Sci. 2015;58:117–123. doi: 10.5468/ogs.2015.58.2.117. PubMed DOI PMC
Arbyn M, Rezhake R, Yuill S, Canfell K. Triage of HPV-positive women in Norway using cytology, HPV16/18 genotyping and HPV persistence. Br. J. Cancer. 2020;122:1577–1579. doi: 10.1038/s41416-020-0787-9. PubMed DOI PMC
Larimer JL, Schmidt-Nielsen K. A comparison of blood carbonic anhydrase of various mammals. Comp. Biochem. Physiol. 1960;1:19–23. doi: 10.1016/0010-406X(60)90004-9. DOI
Carbonic Anhydrase as Drug Target: Thermodynamics and Structure of Inhibitor Binding. (Springer International Publishing, 2019). 10.1007/978-3-030-12780-0.
McKenna R, Frost SC. Overview of the carbonic anhydrase family. Subcell Biochem. 2014;75:3–5. doi: 10.1007/978-94-007-7359-2_1. PubMed DOI
Oosterwijk E, et al. Monoclonal antibody G 250 recognizes a determinant present in renal-cell carcinoma and absent from normal kidney. Int. J. Cancer. 1986;38:489–494. doi: 10.1002/ijc.2910380406. PubMed DOI
Pastorek J, et al. Cloning and characterization of MN, a human tumor-associated protein with a domain homologous to carbonic anhydrase and a putative helix-loop-helix DNA binding segment. Oncogene. 1994;9:2877–2888. PubMed
Saarnio J, et al. Immunohistochemical Study of Colorectal Tumors for Expression of a Novel Transmembrane Carbonic Anhydrase, MN/CA IX, with Potential Value as a Marker of Cell Proliferation. Am. J. Pathol. 1998;153:279–285. doi: 10.1016/S0002-9440(10)65569-1. PubMed DOI PMC
Liao S-Y, et al. Carbonic anhydrase IX (CA-IX) and high-risk human papillomavirus (H-HPV) as diagnostic biomarkers of cervical dysplasia/neoplasia in Japanese women with a cytologic diagnosis of atypical glandular cells (AGC): A Gynecologic Oncology Group (GOG) Study. Br. J. Cancer. 2011;104:353–360. doi: 10.1038/sj.bjc.6606049. PubMed DOI PMC
Liao S-Y, et al. Prognostic relevance of carbonic anhydrase-IX in high-risk, early-stage cervical cancer: A gynecologic oncology group study. Gynecol. Oncol. 2010;116:452–458. doi: 10.1016/j.ygyno.2009.10.062. PubMed DOI PMC
Kock L, et al. Serum carbonic anhydrase IX and its prognostic relevance in vulvar cancer. Int. J. Gynecol. Cancer Off J. Int. Gynecol. Cancer Soc. 2011;21:141–148. doi: 10.1097/IGC.0b013e318204c34f. PubMed DOI
Závada J, Závadová Z, Zat’ovicová M, Hyrsl L, Kawaciuk I. Soluble form of carbonic anhydrase IX (CA IX) in the serum and urine of renal carcinoma patients. Br. J. Cancer. 2003;89:1067–1071. doi: 10.1038/sj.bjc.6601264. PubMed DOI PMC
Cheng F, et al. Significance of detection of serum carbonic anhydrase IX in the diagnosis of lung cancer. Zhongguo Fei Ai Za Zhi Chin. J. Lung Cancer. 2015;18:29–33. PubMed PMC
Janning M, et al. Evaluation of soluble carbonic anhydrase IX as predictive marker for efficacy of bevacizumab: A biomarker analysis from the geparquinto phase III neoadjuvant breast cancer trial. Int. J. Cancer. 2019;145:857–868. doi: 10.1002/ijc.32163. PubMed DOI
Sim SH, et al. Prognostic utility of pre-operative circulating osteopontin, carbonic anhydrase IX and CRP in renal cell carcinoma. Br. J. Cancer. 2012;107:1131–1137. doi: 10.1038/bjc.2012.360. PubMed DOI PMC
Hyrsl L, et al. Soluble form of carbonic anhydrase IX (CAIX) in transitional cell carcinoma of urinary tract. Neoplasma. 2009;56:298–302. doi: 10.4149/neo_2009_04_29. PubMed DOI
İlie M, et al. High levels of carbonic anhydrase IX in tumour tissue and plasma are biomarkers of poor prognostic in patients with non-small cell lung cancer. Br. J. Cancer. 2010;102:1627–1635. doi: 10.1038/sj.bjc.6605690. PubMed DOI PMC
Kock, L. et al. Serum carbonic anhydrase IX and its prognostic relevance in vulvar cancer. Int. J. Gynecol. Cancer21, (2011). PubMed
Zheng R-R, et al. Cervical cancer systemic inflammation score: A novel predictor of prognosis. Oncotarget. 2016;7:15230–15242. doi: 10.18632/oncotarget.7378. PubMed DOI PMC
Zhang S, Xu H, Zhang L, Qiao Y. Cervical cancer: Epidemiology, risk factors and screening. Chin. J. Cancer Res. 2020;32:720–728. doi: 10.21147/j.issn.1000-9604.2020.06.05. PubMed DOI PMC
Zhu, H., Shen, Z., Luo, H., Zhang, W. & Zhu, X. Chlamydia trachomatis infection-associated risk of cervical cancer. Medicine (Baltimore)95, (2016). PubMed PMC
Kitchen, F. L. & Cox, C. M. Papanicolaou Smear. in StatPearls (StatPearls Publishing, 2021). PubMed
Simanaviciene V, et al. Studies on the prevalence of oncogenic HPV types among Lithuanian women with cervical pathology. J. Med. Virol. 2015;87:461–471. doi: 10.1002/jmv.24073. PubMed DOI
Colposcopy and treatment of cervical intraepithelial neoplasia: A beginners’ manual. https://screening.iarc.fr/colpo.php.
Svitrigaile Grinceviciene, PhD., M.D. et al. Association of Soluble Carbonic Anhydrase IX in Plasma and Cervical Intraepithelial Neoplasia: Prospective Observatory Study.
Waxman AG, Chelmow D, Darragh TM, Lawson H, Moscicki A-B. Revised terminology for cervical histopathology and its implications for management of high-grade squamous intraepithelial lesions of the cervix. Obstet. Gynecol. 2012;120:1465–1471. doi: 10.1097/AOG.0b013e31827001d5. PubMed DOI PMC
Lan J, et al. Direct detection and genotyping of Chlamydia trachomatis in cervical scrapes by using polymerase chain reaction and restriction fragment length polymorphism analysis. J. Clin. Microbiol. 1993;31:1060–1065. doi: 10.1128/jcm.31.5.1060-1065.1993. PubMed DOI PMC
Pastorekova S, Gillies RJ. The role of carbonic anhydrase IX in cancer development: links to hypoxia, acidosis, and beyond. Cancer Metastasis Rev. 2019;38:65–77. doi: 10.1007/s10555-019-09799-0. PubMed DOI PMC
Fonseca-Moutinho, J. A. Smoking and Cervical Cancer. ISRN Obstet. Gynecol.2011 (2011). PubMed PMC
Brown-Glaberman, U. et al. Circulating Carbonic Anhydrase IX and Antiangiogenic Therapy in Breast Cancer. Disease Markers, 2016 e9810383 https://www.hindawi.com/journals/dm/2016/9810383/ (2016). PubMed PMC
Ananthanarayanan V, Tretiakova M, Husain AN, Krausz T, Antic T. Carbonic anhydrase IX (CAIX) does not differentiate between benign and malignant mesothelium. Am. J. Clin. Pathol. 2014;142:82–87. doi: 10.1309/AJCP8BJ8CJXUEHZD. PubMed DOI
Capkova, L., Koubkova, L. & Kodet, R. Expression of carbonic anhydrase IX (CAIX) in malignant mesothelioma. An immunohistochemical and immunocytochemical study. 9. PubMed
Filippis AD, et al. Chlamydia trachomatis induces an upregulation of molecular biomarkers podoplanin, Wilms’ tumour gene 1, osteopontin and inflammatory cytokines in human mesothelial cells. Microbiology. 2017;163:654–663. doi: 10.1099/mic.0.000465. PubMed DOI
Madeleine MM, et al. Risk of cervical cancer associated with chlamydia trachomatis antibodies by histology, HPV Type, and HPV Cofactors. Int. J. Cancer J. Int. Cancer. 2007;120:650–655. doi: 10.1002/ijc.22325. PubMed DOI PMC
Ji Y, et al. The burden of human papillomavirus and chlamydia trachomatis coinfection in women: A large cohort study in inner mongolia. China. J. Infect. Dis. 2019;219:206–214. doi: 10.1093/infdis/jiy497. PubMed DOI
Ward C, et al. Carbonic Anhydrase IX (CAIX), Cancer, and Radiation Responsiveness. Metabolites. 2018;8:13. doi: 10.3390/metabo8010013. PubMed DOI PMC
Nordfors, K., Haapasalo, J., Haapasalo, H. & Parkkila, S. Carbonic Anhydrase IX in Adult and Pediatric Brain Tumors. Evol. Mol. Biol. Brain Tumors Ther. Implic. (2013) 10.5772/52358.
Beasley NJP, et al. Carbonic Anhydrase IX, an endogenous hypoxia marker, expression in head and neck squamous cell carcinoma and its relationship to hypoxia, necrosis, and microvessel density. Cancer Res. 2001;61:5262–5267. PubMed
Kim, S. J. et al. Prognostic value of carbonic anhydrase IX and Ki-67 expression in squamous cell carcinoma of the tongue. Jpn J Clin Oncol8. PubMed
Li Y, Dong M, Sheng W, Huang L. Roles of carbonic Anhydrase IX in Development of pancreatic cancer. Pathol. Oncol. Res. 2016;22:277–286. doi: 10.1007/s12253-015-9935-6. PubMed DOI
Pan P, et al. Brain phenotype of carbonic anhydrase IX-deficient mice. Transgenic Res. 2012;21:163–176. doi: 10.1007/s11248-011-9520-z. PubMed DOI
Yeo E-J. Hypoxia and aging. Exp. Mol. Med. 2019;51:1–15. PubMed PMC
Chen A, et al. Intermittent hypoxia induces a metastatic phenotype in breast cancer. Oncogene. 2018;37:4214–4225. doi: 10.1038/s41388-018-0259-3. PubMed DOI
Kim BW, et al. Prognostic assessment of hypoxia and metabolic markers in cervical cancer using automated digital image analysis of immunohistochemistry. J. Transl. Med. 2013;11:185. doi: 10.1186/1479-5876-11-185. PubMed DOI PMC
Lu ZH, Wright JD, Belt B, Cardiff RD, Arbeit JM. Hypoxia-inducible factor-1 facilitates cervical cancer progression in human papillomavirus type 16 transgenic mice. Am. J. Pathol. 2007;171:667–681. doi: 10.2353/ajpath.2007.061138. PubMed DOI PMC
Soto, D., Song, C. & McLaughlin-Drubin, M. E. Epigenetic alterations in human papillomavirus-associated cancers. Viruses9, (2017). PubMed PMC
Alves MGO, et al. Gene expression and carbonic anhydrase IX promoter methylation in oral cancer and smokers oral mucosa: A pilot study. Stomatol. Dis. Sci. 2017;1:109–115.
Warren GW, et al. Nicotinic modulation of therapeutic response in vitro and in vivo. Int. J. Cancer. 2012;131:2519–2527. doi: 10.1002/ijc.27556. PubMed DOI
Schweiger T, et al. Carbonic anhydrase IX is associated with early pulmonary spreading of primary colorectal carcinoma and tobacco smoking. Eur. J. Cardiothorac. Surg. 2014;46:92–99. doi: 10.1093/ejcts/ezt542. PubMed DOI