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Distribution of Human Papillomavirus Genotypes and Cervical Cytology Results at A Tertiary Center in The Eastern Black Sea Region of Turkey

Year 2019, Volume: 14 Issue: 4, 205 - 213, 26.10.2019

Abstract

    We investigated the genotypes of HPV and the smear
results of patients in the Eastern Black Sea region of Turkey. Four hundred
four patients who were HPV-positive were analyzed; 278 (68.81%) patients had a
single infection, and 126 (31.2%) had multiple infections. Three hundred
seventy-eight (93.6%) of patients were HR-HPV positive. There was no
significant correlation between multiple HPV infection and HR-HPV frequency
with age. The most common HPV genotypes were 16, 18, 31, 51, and 35,
respectively. The smear results of 345 patients were obtained and we found no
correlation between smear abnormalities and multiple HPV infections. In
conclusion, the most common HPV subtypes in the Rize region were HPV type 16, 18,
31, and 51 and regardless of whether HPV 16 and/or 18 were included, multiple
HPV infections were not associated with abnormal cytology results.

References

  • [1] Baseman, J.G. and Koutsky, L.A., (2005). The Epidemiology of Human Papillomavirus Infection. J Clin Virol, 32(1):16-24.
  • [2] Fernandes, J.V., Meissner, Rde. V., de Carvalho, M.G., Fernandes, T.A., de Azevedo, P.R., and et al., (2009). Prevalence of HPV Infection by Cervical Cytologic Status in Brazil. Int J Gynaecol Obstet, 105(1):21-24.
  • [3] Kocjan, B.J., Bzhalava, D., Forslund, O., Dillner, J., and Poljak, M., (2015). Molecular Methods for Identification and Characterization of Novel Papillomaviruses. Clin Microbiol Infect, 21(9):808-816.
  • [4] Munoz, N., Bosch, F.X., de Sanjose, S., Herrero, R., Castellsague, X., Shah, K.V., and et al., (2003). Epidemiologic Classification of Human Papillomavirus Types Associated with Cervical Cancer. N Engl J Med, 348(6):518-527.
  • [5] Bouvard, V., Baan, R., Straif, K., Grosse, Y., Secretan, B., El Ghissassi, F., and et al., (2009). A Review of Human Carcinogens--Part B: Biological Agents. Lancet Oncol, 10(4):321-322.
  • [6] Agents Classified by the IARC Monographs. Internal Agency for Research on Cancer (IARC) Website. Available from: http://www. Monographs.iarc.fr/ENG/Classification/index.php.
  • [7] Bruno, A., Serravalle, K., Travassos, A.G., and Lima, BGC., (2014). Distribuição dos Genótipos de Papillomavírus Humanoemmulheres do Estado da Bahia, Brasil. Rev Bras Ginecol Obstet, 36(9):416-422.
  • [8] Saslow, D., Solomon, D., Lawson, H.W., Killackey, M., Kulasingam, S.L., Cain, J.M., and et al., (2012). American Cancer Society, American Society for Colposcopy and Cervical Pathology, and American Society for Clinical Pathology Screening Guidelines for the Prevention and Early Detection of Cervical Cancer. J Low Genit Tract Dis, 16:175-204.
  • [9] Bruni, L,, Diaz, M., Castellsague, X., Ferrer, E., Bosch, F.X., and de Sanjose, S., (2010). Cervical Human Papillomavirus Prevalence in 5 Continents: Meta-analysis of 1 Million Women with Normal Cytological Findings. J Infect Dis, 202(12):1789-1799.
  • [10] Dursun, P., Ayhan, A., Mutlu, L., Çağlar, M., Haberal, A., Güngör, T., and et al., (2013). HPV Types in Turkey: Multicenter Hospital Based Evaluation of 6388 Patients in Turkish Gynecologic Oncology Group Centers. Türk Patoloji Dergisi, 29(3):210-216.
  • [11] Akın, L., (2006). Epidemiology of Sexually Transmitted Infection. Review Türkiye Klinikleri Journal of Medical Science, 26:655-665.
  • [12] Solomon, D., Davey, D., Kurman, R., Moriarty, A., O’Connor, D., Prey, M., and et al., (2002). Bethesda 2001 Workshop: The 2001 Bethesda System: Terminology for reporting results of cervical cytology. JAMA, 287:2114–2119.
  • [13] Bosch, F.X., Burchell, A.N., Schiffman, M., Giuliano, A.R., de Sanjose, S., Bruni, L., and et al., (2008). Epidemiology and Natural History of Human Papillomavirus Infections and Type-Specific Implications in Cervical Neoplasia. Vaccine, 26(10):1-16.
  • [14] Delgado, D., Marin, J.M., de Diego, J., Guerra, S., Gonzalez, B., Barrios, J.L., and et al., (2012). Human Papillomavirus (HPV) Genotype Distribution in Women with Abnormal Cervical Cytology in the Basque Country, Spain. Enferm Infec Microbiol Clin, 30(5):230-235.
  • [15] Bao, Y.P., Li, N., Smith, J.S., Qiao, Y.L., and Members, A., (2008). Human Papillomavirus Type Distribution in Women from Asia: A Meta-analysis. Int J Gynecol Cancer, 18:71-79.
  • [16] Wu, R.F., Dai, M., Qiao, Y.L., Clifford, G.M., Liu, Z.H., Arslan, A., and et al., (2007). Human Papillomavirus Infection in Women in Shenzhen City, People’s Republic of China, a Population Typical of Recent Chinese Urbanisation. Int J Cancer, 121(6):1306-1311.
  • [17] Ye, J., Cheng, X., Chen, X., Ye, F., Lu, W., and Xie, X., (2010). Prevalence and Risk Profile of Cervical Human Papillomavirus Infection in Zhejiang Province, Southeast China: a Population-Based Study. Virol J, 7:66.
  • [18] Tao, G., Yaling, G., Zhan, G., Pu, L., and Miao, H., (2008). Human Papillomavirus Genotype Distribution among HPV-positive Women in Sichuan Province, Soutwest China. Arch Virol, 163:65-72.
  • [19] Levi, J.E., Longatto-filho, A., Eluf-neto, J., Rodrigues, C.L., Oliveira, C.M., Carloni, A.C., and et al., (2014). Evaluation of HPV Molecular Tests in Primary Screening for Cervical Cancer in Brazil. Open J Obstet Gynecol, 4:470-478.
  • [20] Todorova, I., Baban, A., Balabanova, D., Panayotova, Y., and Bradley, J., (2006). Providers' Constructions of the Role of Women in Cervical Cancer Screening in Bulgaria and Romania. Soc Sci Med, 63:776-787.
  • [21] Castle, P.E., Porras, C., Quint, W.G., Rodriguez, A.C., Schiffman, M., Gravitt, P.E., and et al., (2008). Comparison of two PCR Based Human Papillomavirus Genotyping Methods. J Clin Microbiol, 46:3437-3445.
  • [22] Forslund, O., Antonsson, A., Edlund, K., van den Brule, A.J., Hansson, B.G., Meijer, C.J., and et al., (2002). Population‐based Type‐specific Prevalence of High‐risk Human Papillomavirus Infection in Middle‐Aged Swedish Women. J Med Virol, 66:535-541.
  • [23] Matos, E., Loria, D., Amestoy, G.M., Herrera, L., Prince, M.A., Moreno, J., and et al., (2003). Prevalence of Human Papillomavirus Infection among Women in Concordia, Argentina: A Population‐based Study. Sex Transm Dis, 30:593-599.
  • [24] Jeng, C.J., Ko, M.L, Ling, Q.D., Shen, J., Lin, H.W., Tzeng, C.R., and et al., (2005). Prevalence of Cervical Human Papillomavirus in Taiwanese Women. Clin Invest Med, 28:261-266.
  • [25] Martin, P., Kilany, L., Garcia, D., Lopez-Garcia, A.M., Martin-Azana, M.J., Abraira, V., and et al., (2011). Human Papillomavirus Genotype Distribution in Madrid and Correlation with Cytological Data. BMC Infect Dis, 11:316.
  • [26] Mejlhede, N., Bonde, J., and Fomsgaard, A., (2009). High Frequency of Multiple HPV types in Cervical Specimens from Danish Women. APMIS, 117(2):108-114.
  • [27] Gonzalez-Bosquet, E., Esteva, C., Munoz-Almagro, C., Ferrer, P., Perez, M., and Lailla, J.M., (2008). Identification of Vaccine HUMAN PAPILLOMAVIRUS GENOTYPES in Squamous Intraepithelial Lesions (CIN2-3) Gynecol Oncol, 111(1):9–12.
  • [28] Sjoeborg, K.D., Trope, A., Lie, A.K., Jonassen, C.M., Steinbakk, M., Hansen, M., and et al., (2010). HPV Genotype Distribution according to Severity of Cervical Neoplasia. Gynecol Oncol, 118(1):29–34.
  • [29] Zeng, Z., Yang, H., Li, Z., He, X., Griffith, C.C., Chen, X., and et al., (2016). Prevalence and Genotype Distribution of HPV Infection in China: Analysis of 51,345 HPV Genotyping Results from China's Largest CAP Certified Laboratory. J Cancer, 7(9):1037-1043.
  • [30] Ghosh, T., VandeHaar, M.A., Rivera, M., and Henry, M.R., (2018). High-risk HPV Genotype Distribution in HPV Co-test Specimens: Study of a Predominantly Midwestern Population. Journal of the American Society of Cytopathology, 7(2):99-105.
  • [31] Bello, B.D., Spinillo, A., Alberizzi, P., Cesari, S., Gardella, B., D'Ambrosio, G., and et al., (2009). Cervical Infections by Multiple Human Papillomavirus (HPV) Genotypes: Prevalence and Impact on the Risk of Precancerous Epithelial Lesions. J Med Virol, 81:703-712.
  • [32] Herrero, R., Castle, P.E., Schiffman, M., Bratti, M.C., Hildesheim, A., Morales, J., and et al., (2005). Epidemiologic Profile of Type-specific Human Papillomavirus Infection and Cervical Neoplasia in Guanacaste Costa Rica. J Infect Dis, 191(11):1796-1807.
  • [33] Cuschieri, K.S., Cubie, H.A., Whitley, M.W., Seagar, A.L., Arends, M.J., Moore, C., and et al., (2004). Multiple High Risk HPV Infections are Common in Cervical Neoplasia and Young Women in a Cervical Screening Population. J Clin Pathol, 57(1):68-72.
  • [34] Schmitt, M., Depuydt, C., Benoy, I., Bogers, J., Antoine, J., Arbyn, M., and et al., (2013). Multiple Human Papillomavirus Infections with High Viral Loads are Associated with Cervical Lesions but do not Differentiate Grades of Cervical Abnormalities. J Clin Microbiol, 51:1458-1464.
  • [35] Wu, E.Q., Liu, B., Cui, J.F., Chen, W., Wang, J.B, Lu, L., and et al., (2013). Prevalence of Type-specific Human Papillomavirus and Pap Results in Chinese Women: A Multi-center, Population-Based Cross-Sectional Study. Cancer Causes Control, 24(4):795-803.
  • [36] Martins, T.R., Mendes de Oliveira, C., Rosa, L.R., de Campos Centrone, C., Rodrigues, C.L., Villa, L,L., and et al., (2016). HPV Genotype Distribution in Brazilian Women with and without Cervical Lesions: Correlation to Cytological Data. Virol J, 13:138.
  • [37] Ciapponi, A., Bardach, A., Glujovsky, D., Gibbons, L., and Picconi, M.A., (2011). Type-specific HPV Prevalence in Cervical Cancer and High-grade Lesions in Latin America and the Caribbean: Systematic Review and Meta-analysis. PLoS One, 6(10):e25493.
  • [38] Wright, T.C., Jr, Stoler, M.H., Behrens, C.M., Apple, R., Derion, T., and Wright, T.L., (2012). The Athena Human Papillomavirus Study: Design, Methods, and Baseline Results. Am J Obstet Gynecol, 206(1):46 e1–e11.
  • [39] Wheeler, C.M., Hunt, W.C., Cuzick, J., Langsfeld, E., Pearse, A., Montoya, G.D., and et al., (2013). A Population-based Study of Human Papillomavirus Genotype Prevalence in the United States: Baseline Measures Prior to Mass Human Papillomavirus Vaccination. Int J Cancer, 132(1):198–207.

Distribution of Human Papillomavirus Genotypes and Cervical Cytology Results at A Tertiary Center in The Eastern Black Sea Region of Turkey

Year 2019, Volume: 14 Issue: 4, 205 - 213, 26.10.2019

Abstract

We investigated the genotypes of HPV and the smear results of patients in the Eastern Black Sea region of Turkey. Four hundred four patients who were HPV-positive were analyzed; 278 (68.81%) patients had a single infection, and 126 (31.2%) had multiple infections. Three hundred seventy-eight (93.6%) of patients were HR-HPV positive. There was no significant correlation between multiple HPV infection and HR-HPV frequency with age. The most common HPV genotypes were 16, 18, 31, 51, and 35, respectively. The smear results of 345 patients were obtained and we found no correlation between smear abnormalities and multiple HPV infections. In conclusion, the most common HPV subtypes in the Rize region were HPV type 16, 18, 31, and 51 and regardless of whether HPV 16 and/or 18 were included, multiple HPV infections were not associated with abnormal cytology results.

References

  • [1] Baseman, J.G. and Koutsky, L.A., (2005). The Epidemiology of Human Papillomavirus Infection. J Clin Virol, 32(1):16-24.
  • [2] Fernandes, J.V., Meissner, Rde. V., de Carvalho, M.G., Fernandes, T.A., de Azevedo, P.R., and et al., (2009). Prevalence of HPV Infection by Cervical Cytologic Status in Brazil. Int J Gynaecol Obstet, 105(1):21-24.
  • [3] Kocjan, B.J., Bzhalava, D., Forslund, O., Dillner, J., and Poljak, M., (2015). Molecular Methods for Identification and Characterization of Novel Papillomaviruses. Clin Microbiol Infect, 21(9):808-816.
  • [4] Munoz, N., Bosch, F.X., de Sanjose, S., Herrero, R., Castellsague, X., Shah, K.V., and et al., (2003). Epidemiologic Classification of Human Papillomavirus Types Associated with Cervical Cancer. N Engl J Med, 348(6):518-527.
  • [5] Bouvard, V., Baan, R., Straif, K., Grosse, Y., Secretan, B., El Ghissassi, F., and et al., (2009). A Review of Human Carcinogens--Part B: Biological Agents. Lancet Oncol, 10(4):321-322.
  • [6] Agents Classified by the IARC Monographs. Internal Agency for Research on Cancer (IARC) Website. Available from: http://www. Monographs.iarc.fr/ENG/Classification/index.php.
  • [7] Bruno, A., Serravalle, K., Travassos, A.G., and Lima, BGC., (2014). Distribuição dos Genótipos de Papillomavírus Humanoemmulheres do Estado da Bahia, Brasil. Rev Bras Ginecol Obstet, 36(9):416-422.
  • [8] Saslow, D., Solomon, D., Lawson, H.W., Killackey, M., Kulasingam, S.L., Cain, J.M., and et al., (2012). American Cancer Society, American Society for Colposcopy and Cervical Pathology, and American Society for Clinical Pathology Screening Guidelines for the Prevention and Early Detection of Cervical Cancer. J Low Genit Tract Dis, 16:175-204.
  • [9] Bruni, L,, Diaz, M., Castellsague, X., Ferrer, E., Bosch, F.X., and de Sanjose, S., (2010). Cervical Human Papillomavirus Prevalence in 5 Continents: Meta-analysis of 1 Million Women with Normal Cytological Findings. J Infect Dis, 202(12):1789-1799.
  • [10] Dursun, P., Ayhan, A., Mutlu, L., Çağlar, M., Haberal, A., Güngör, T., and et al., (2013). HPV Types in Turkey: Multicenter Hospital Based Evaluation of 6388 Patients in Turkish Gynecologic Oncology Group Centers. Türk Patoloji Dergisi, 29(3):210-216.
  • [11] Akın, L., (2006). Epidemiology of Sexually Transmitted Infection. Review Türkiye Klinikleri Journal of Medical Science, 26:655-665.
  • [12] Solomon, D., Davey, D., Kurman, R., Moriarty, A., O’Connor, D., Prey, M., and et al., (2002). Bethesda 2001 Workshop: The 2001 Bethesda System: Terminology for reporting results of cervical cytology. JAMA, 287:2114–2119.
  • [13] Bosch, F.X., Burchell, A.N., Schiffman, M., Giuliano, A.R., de Sanjose, S., Bruni, L., and et al., (2008). Epidemiology and Natural History of Human Papillomavirus Infections and Type-Specific Implications in Cervical Neoplasia. Vaccine, 26(10):1-16.
  • [14] Delgado, D., Marin, J.M., de Diego, J., Guerra, S., Gonzalez, B., Barrios, J.L., and et al., (2012). Human Papillomavirus (HPV) Genotype Distribution in Women with Abnormal Cervical Cytology in the Basque Country, Spain. Enferm Infec Microbiol Clin, 30(5):230-235.
  • [15] Bao, Y.P., Li, N., Smith, J.S., Qiao, Y.L., and Members, A., (2008). Human Papillomavirus Type Distribution in Women from Asia: A Meta-analysis. Int J Gynecol Cancer, 18:71-79.
  • [16] Wu, R.F., Dai, M., Qiao, Y.L., Clifford, G.M., Liu, Z.H., Arslan, A., and et al., (2007). Human Papillomavirus Infection in Women in Shenzhen City, People’s Republic of China, a Population Typical of Recent Chinese Urbanisation. Int J Cancer, 121(6):1306-1311.
  • [17] Ye, J., Cheng, X., Chen, X., Ye, F., Lu, W., and Xie, X., (2010). Prevalence and Risk Profile of Cervical Human Papillomavirus Infection in Zhejiang Province, Southeast China: a Population-Based Study. Virol J, 7:66.
  • [18] Tao, G., Yaling, G., Zhan, G., Pu, L., and Miao, H., (2008). Human Papillomavirus Genotype Distribution among HPV-positive Women in Sichuan Province, Soutwest China. Arch Virol, 163:65-72.
  • [19] Levi, J.E., Longatto-filho, A., Eluf-neto, J., Rodrigues, C.L., Oliveira, C.M., Carloni, A.C., and et al., (2014). Evaluation of HPV Molecular Tests in Primary Screening for Cervical Cancer in Brazil. Open J Obstet Gynecol, 4:470-478.
  • [20] Todorova, I., Baban, A., Balabanova, D., Panayotova, Y., and Bradley, J., (2006). Providers' Constructions of the Role of Women in Cervical Cancer Screening in Bulgaria and Romania. Soc Sci Med, 63:776-787.
  • [21] Castle, P.E., Porras, C., Quint, W.G., Rodriguez, A.C., Schiffman, M., Gravitt, P.E., and et al., (2008). Comparison of two PCR Based Human Papillomavirus Genotyping Methods. J Clin Microbiol, 46:3437-3445.
  • [22] Forslund, O., Antonsson, A., Edlund, K., van den Brule, A.J., Hansson, B.G., Meijer, C.J., and et al., (2002). Population‐based Type‐specific Prevalence of High‐risk Human Papillomavirus Infection in Middle‐Aged Swedish Women. J Med Virol, 66:535-541.
  • [23] Matos, E., Loria, D., Amestoy, G.M., Herrera, L., Prince, M.A., Moreno, J., and et al., (2003). Prevalence of Human Papillomavirus Infection among Women in Concordia, Argentina: A Population‐based Study. Sex Transm Dis, 30:593-599.
  • [24] Jeng, C.J., Ko, M.L, Ling, Q.D., Shen, J., Lin, H.W., Tzeng, C.R., and et al., (2005). Prevalence of Cervical Human Papillomavirus in Taiwanese Women. Clin Invest Med, 28:261-266.
  • [25] Martin, P., Kilany, L., Garcia, D., Lopez-Garcia, A.M., Martin-Azana, M.J., Abraira, V., and et al., (2011). Human Papillomavirus Genotype Distribution in Madrid and Correlation with Cytological Data. BMC Infect Dis, 11:316.
  • [26] Mejlhede, N., Bonde, J., and Fomsgaard, A., (2009). High Frequency of Multiple HPV types in Cervical Specimens from Danish Women. APMIS, 117(2):108-114.
  • [27] Gonzalez-Bosquet, E., Esteva, C., Munoz-Almagro, C., Ferrer, P., Perez, M., and Lailla, J.M., (2008). Identification of Vaccine HUMAN PAPILLOMAVIRUS GENOTYPES in Squamous Intraepithelial Lesions (CIN2-3) Gynecol Oncol, 111(1):9–12.
  • [28] Sjoeborg, K.D., Trope, A., Lie, A.K., Jonassen, C.M., Steinbakk, M., Hansen, M., and et al., (2010). HPV Genotype Distribution according to Severity of Cervical Neoplasia. Gynecol Oncol, 118(1):29–34.
  • [29] Zeng, Z., Yang, H., Li, Z., He, X., Griffith, C.C., Chen, X., and et al., (2016). Prevalence and Genotype Distribution of HPV Infection in China: Analysis of 51,345 HPV Genotyping Results from China's Largest CAP Certified Laboratory. J Cancer, 7(9):1037-1043.
  • [30] Ghosh, T., VandeHaar, M.A., Rivera, M., and Henry, M.R., (2018). High-risk HPV Genotype Distribution in HPV Co-test Specimens: Study of a Predominantly Midwestern Population. Journal of the American Society of Cytopathology, 7(2):99-105.
  • [31] Bello, B.D., Spinillo, A., Alberizzi, P., Cesari, S., Gardella, B., D'Ambrosio, G., and et al., (2009). Cervical Infections by Multiple Human Papillomavirus (HPV) Genotypes: Prevalence and Impact on the Risk of Precancerous Epithelial Lesions. J Med Virol, 81:703-712.
  • [32] Herrero, R., Castle, P.E., Schiffman, M., Bratti, M.C., Hildesheim, A., Morales, J., and et al., (2005). Epidemiologic Profile of Type-specific Human Papillomavirus Infection and Cervical Neoplasia in Guanacaste Costa Rica. J Infect Dis, 191(11):1796-1807.
  • [33] Cuschieri, K.S., Cubie, H.A., Whitley, M.W., Seagar, A.L., Arends, M.J., Moore, C., and et al., (2004). Multiple High Risk HPV Infections are Common in Cervical Neoplasia and Young Women in a Cervical Screening Population. J Clin Pathol, 57(1):68-72.
  • [34] Schmitt, M., Depuydt, C., Benoy, I., Bogers, J., Antoine, J., Arbyn, M., and et al., (2013). Multiple Human Papillomavirus Infections with High Viral Loads are Associated with Cervical Lesions but do not Differentiate Grades of Cervical Abnormalities. J Clin Microbiol, 51:1458-1464.
  • [35] Wu, E.Q., Liu, B., Cui, J.F., Chen, W., Wang, J.B, Lu, L., and et al., (2013). Prevalence of Type-specific Human Papillomavirus and Pap Results in Chinese Women: A Multi-center, Population-Based Cross-Sectional Study. Cancer Causes Control, 24(4):795-803.
  • [36] Martins, T.R., Mendes de Oliveira, C., Rosa, L.R., de Campos Centrone, C., Rodrigues, C.L., Villa, L,L., and et al., (2016). HPV Genotype Distribution in Brazilian Women with and without Cervical Lesions: Correlation to Cytological Data. Virol J, 13:138.
  • [37] Ciapponi, A., Bardach, A., Glujovsky, D., Gibbons, L., and Picconi, M.A., (2011). Type-specific HPV Prevalence in Cervical Cancer and High-grade Lesions in Latin America and the Caribbean: Systematic Review and Meta-analysis. PLoS One, 6(10):e25493.
  • [38] Wright, T.C., Jr, Stoler, M.H., Behrens, C.M., Apple, R., Derion, T., and Wright, T.L., (2012). The Athena Human Papillomavirus Study: Design, Methods, and Baseline Results. Am J Obstet Gynecol, 206(1):46 e1–e11.
  • [39] Wheeler, C.M., Hunt, W.C., Cuzick, J., Langsfeld, E., Pearse, A., Montoya, G.D., and et al., (2013). A Population-based Study of Human Papillomavirus Genotype Prevalence in the United States: Baseline Measures Prior to Mass Human Papillomavirus Vaccination. Int J Cancer, 132(1):198–207.
There are 39 citations in total.

Details

Primary Language English
Subjects Health Care Administration
Journal Section Articles
Authors

Hacı Öztürk Şahin 0000-0002-7915-8235

Beril Gürlek 0000-0002-9108-2990

Publication Date October 26, 2019
Published in Issue Year 2019 Volume: 14 Issue: 4

Cite

APA Şahin, H. Ö., & Gürlek, B. (2019). Distribution of Human Papillomavirus Genotypes and Cervical Cytology Results at A Tertiary Center in The Eastern Black Sea Region of Turkey. Medical Sciences, 14(4), 205-213.
AMA Şahin HÖ, Gürlek B. Distribution of Human Papillomavirus Genotypes and Cervical Cytology Results at A Tertiary Center in The Eastern Black Sea Region of Turkey. Medical Sciences. October 2019;14(4):205-213.
Chicago Şahin, Hacı Öztürk, and Beril Gürlek. “Distribution of Human Papillomavirus Genotypes and Cervical Cytology Results at A Tertiary Center in The Eastern Black Sea Region of Turkey”. Medical Sciences 14, no. 4 (October 2019): 205-13.
EndNote Şahin HÖ, Gürlek B (October 1, 2019) Distribution of Human Papillomavirus Genotypes and Cervical Cytology Results at A Tertiary Center in The Eastern Black Sea Region of Turkey. Medical Sciences 14 4 205–213.
IEEE H. Ö. Şahin and B. Gürlek, “Distribution of Human Papillomavirus Genotypes and Cervical Cytology Results at A Tertiary Center in The Eastern Black Sea Region of Turkey”, Medical Sciences, vol. 14, no. 4, pp. 205–213, 2019.
ISNAD Şahin, Hacı Öztürk - Gürlek, Beril. “Distribution of Human Papillomavirus Genotypes and Cervical Cytology Results at A Tertiary Center in The Eastern Black Sea Region of Turkey”. Medical Sciences 14/4 (October 2019), 205-213.
JAMA Şahin HÖ, Gürlek B. Distribution of Human Papillomavirus Genotypes and Cervical Cytology Results at A Tertiary Center in The Eastern Black Sea Region of Turkey. Medical Sciences. 2019;14:205–213.
MLA Şahin, Hacı Öztürk and Beril Gürlek. “Distribution of Human Papillomavirus Genotypes and Cervical Cytology Results at A Tertiary Center in The Eastern Black Sea Region of Turkey”. Medical Sciences, vol. 14, no. 4, 2019, pp. 205-13.
Vancouver Şahin HÖ, Gürlek B. Distribution of Human Papillomavirus Genotypes and Cervical Cytology Results at A Tertiary Center in The Eastern Black Sea Region of Turkey. Medical Sciences. 2019;14(4):205-13.