The influence of probiotics on genital high-risk human papilloma virus clearance and quality of cervical smear: a randomized placebo-controlled trial
Open accessAbstract
BACKGROUND: Probiotics has been shown to be effective in reducing vaginal colonization of pathogenic organisms. The aim of this study was to investigate the influence of probiotic strains Lactobacillus rhamnosus GR-1 and Lactobacillus reuteri RC-14 on genital high-risk human papilloma virus (HR-HPV) clearance and quality of cervical smear. METHODS: This was a randomized, double-blinded, placebo-controlled trial. Women with genital HR-HPV infection were randomized into study and control groups. A probiotic or placebo preparation was administered orally (one capsule daily) until negative HR-HPV testing. A cervical smear and HR-HPV tests were performed at the beginning of the study and every 3 months thereafter until a negative result was obtained. RESULTS: A total of 121 women with genital HR-HPV infection were enrolled (62 in the study group and 59 in the control group). There was no significant difference in HR-HPV clearance rate between the two groups (58.1% vs. 54.2%). The only factor predicting HR-HPV clearance was a lower initial viral load (HR 3.214; 95% CI: 1.398, 7.392; p = 0.006). Twenty-two women had a mildly abnormal initial cervical smear and nine had an unsatisfactory smear. At 6 months follow-up, both mildly abnormal cervical smear and unsatisfactory smear rates had decreased significantly in the study group compared to the control group (p = 0.017 and 0.027). CONCLUSIONS: The application of probiotic strains Lactobacillus rhamnosus GR-1 and Lactobacillus reuteri RC-14 did not influence genital HR-HPV clearance, but may have decreased the rates of mildly abnormal and unsatisfactory cervical smears. TRIAL REGISTRATION: Clinicaltrials.gov NCT01599416 , May, 2012. Retrospectively registered.
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In the same RCT, a decrease in rates of abnormal and unsatisfactory cervical smears was obtained.
“but a decrease in the rates of abnormal and unsatisfactory cervical smears was obtained [176].”
From The Potential Impact of Probiotics on Human Health: An Update on Their Health-Promoting Properties (2024) · cites this paper as [176]
In a double-blind RCT involving 121 women with genital HR-HPV infection, application of L. rhamnosus GR-1 and Limosilactobacillus reuteri RC-14 for 3 months did not influence HR-HPV genital clearance.
“In another double-blind RCT study involving 121 women with genital high-risk HPV infection (HR-HPV), researchers reported that the application of two strains of probiotics, L. rhamnosus GR- 1 and Limosilactobacillus reuteri RC-14, for 3 months did not influence HR-HPV genital clearance”
From The Potential Impact of Probiotics on Human Health: An Update on Their Health-Promoting Properties (2024) · cites this paper as [176]
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Cites
Natural history and epidemiology of HPV infection and cervical cancer
Castellsagué, X. (2008) · Gynecologic Oncology · doi:10.1016/j.ygyno.2008.07.045 · Cited by 591 · see citing works
Hydrogen Peroxide--Producing Lactobacilli and Acquisition of Vaginal Infections
Hawes, S. E., Hillier, S. L., Benedetti, J., Stevens, C. E., Koutsky, L. A., Wölner‐Hanssen, P., & Holmes, K. K. (1996) · The Journal of Infectious Diseases · doi:10.1093/infdis/174.5.1058 · Cited by 525 · see citing works
Oral probiotics can resolve urogenital infections
Reid, G., Bruce, A. W., Fraser, N., Heinemann, C., Owen, J., & Henning, B. (2001) · FEMS Immunology & Medical Microbiology · doi:10.1016/s0928-8244(00)00233-9 · Cited by 464 · see citing works
Gillet, E., Meys, J. F., Verstraelen, H., Bosire, C., De Sutter, P., Temmerman, M., & Broeck, D. V. (2011) · BMC Infectious Diseases · doi:10.1186/1471-2334-11-10 · Cited by 354 · see citing works
van Baarlen, P., Troost, F. J., van Kraaij, C., Hooiveld, G. J. E. J., Boekschoten, M. V., Brummer, R. J., & Kleerebezem, M. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1000079107 · Cited by 336 · see citing works
High-Risk Human Papillomavirus Testing in Women With ASC-US Cytology
Stoler, M. H., Wright, T. C., Sharma, A., Apple, R. J., Gutekunst, K. A., & Wright, T. L. (2011) · American Journal of Clinical Pathology · doi:10.1309/ajcpz5jy6fcvnmot · Cited by 327 · see citing works
Gupta, K., Stapleton, A. E., Hooton, T. M., Roberts, P. L., Fennell, C. L., & Stamm, W. E. (1998) · The Journal of Infectious Diseases · doi:10.1086/515635 · Cited by 287 · see citing works
Probiotic agents to protect the urogenital tract against infection
Reid, G. (2001) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/73.2.437s · Cited by 258 · see citing works
Anukam, K. C., Osazuwa, E. O., Osadolor, H. B., Bruce, A. W., & Reid, G. (2008) · Journal of Clinical Gastroenterology · doi:10.1097/mcg.0b013e31802c7465 · Cited by 180 · see citing works
Lactobacillus Strains and Vaginal Ecology
Cadieux, P., Burton, J., Gardiner, G., Braunstein, I., Bruce, A. W., Kang, C. Y., & Reid, G. (2002) · JAMA · doi:10.1001/jama.287.15.1940 · Cited by 142 · see citing works
Verhoeven, V., Renard, N., Makar, A., Royen, P. V., Bogers, J.-P., Lardon, F., Peeters, M., & Baay, M. (2013) · European Journal of Cancer Prevention · doi:10.1097/cej.0b013e328355ed23 · Cited by 135 · see citing works
Palma, E., Recine, N., Domenici, L., Giorgini, M., Pierangeli, A., & Panici, P. B. (2018) · BMC Infectious Diseases · doi:10.1186/s12879-017-2938-z · Cited by 132 · see citing works
Chew, S. Y., Cheah, Y. K., Seow, H. F., Sandai, D. A., & Than, L. T. L. (2015) · Journal of Applied Microbiology · doi:10.1111/jam.12772 · Cited by 126 · see citing works
Ho, M., Chang, Y.-Y., Chang, W.-C., Lin, H.-C., Wang, M.-H., Lin, W.-C., & Chiu, T.-H. (2016) · Taiwanese Journal of Obstetrics and Gynecology · doi:10.1016/j.tjog.2016.06.003 · Cited by 121 · see citing works
Self-citationClinical findings among young women with genital human papillomavirus infection
Mao, C., Hughes, J. P., Kiviat, N. B., Kuypers, J. M., Lee, S.-K., Adam, D. E., & Koutsky, L. A. (2003) · American Journal of Obstetrics and Gynecology · doi:10.1067/mob.2003.164 · Cited by 97 · see citing works
Antiviral activity of Bifidobacterium adolescentisSPM1005-A on human papillomavirus type 16
Cha, M.-K., Lee, D., An, H.-M., Lee, S., Shin, S. H., Kwon, J.-H., Kim, K.-J., & Ha, N. (2012) · BMC Medicine · doi:10.1186/1741-7015-10-72 · Cited by 95 · see citing works
Bisanz, J. E., Seney, S. L., McMillan, A., Vongsa, R., Koenig, D. W., Wong, L., Dvoracek, B., Gloor, G. B., Sumarah, M. W., Ford, B., et al. (2014) · PLoS ONE · doi:10.1371/journal.pone.0104511 · Cited by 72 · see citing works
Probiotics in the Prevention and Treatment of Postmenopausal Vaginal Infections: Review Article
Kim, J. M., & Park, Y. J. (2017) · Journal of Menopausal Medicine · doi:10.6118/jmm.2017.23.3.139 · Cited by 72 · see citing works
Arbyn, M., Xu, L., Verdoodt, F., Cuzick, J., Szarewski, A., Belinson, J. L., Wentzensen, N., Gage, J. C., & Khan, M. J. (2017) · Annals of Internal Medicine · doi:10.7326/m15-2735 · Cited by 68 · see citing works
van der Weele, P., van Logchem, E., Wolffs, P. F. G., et al. (2016) · Journal of Clinical Virology · doi:10.1016/j.jcv.2016.07.020 · Cited by 61 · see citing works
Prétet, J., Dalstein, V., Monnier‐Benoit, S., et al. (2004) · Journal of Clinical Virology · doi:10.1016/j.jcv.2004.02.008 · Cited by 50 · see citing works
Anukam, K. C., Hayes, K. C., Summers, K. L., & Reid, G. (2009) · Advances in Urology · doi:10.1155/2009/680363 · Cited by 48 · see citing works
Human Papillomavirus Infection
Huh, W. K. (2009) · Obstetrics and Gynecology · doi:10.1097/aog.0b013e3181ab6878 · Cited by 46 · see citing works
Human papillomavirus type 16 viral load measurement as a predictor of infection clearance
Trevisan, A., Schlecht, N. F., Ramanakumar, A. V., et al. (2013) · Journal of General Virology · doi:10.1099/vir.0.051722-0 · Cited by 44 · see citing works
Siebers, A. G., Klinkhamer, P. J. J. M., Vedder, J. E. M., Arbyn, M., & Bulten, J. (2011) · Archives of Pathology & Laboratory Medicine · doi:10.5858/arpa.2011-0113-oa · Cited by 44 · see citing works
A Comparison of Liquid-Based Cytology with Conventional Cytology in Cervical Cancer Screening
AKAMATSU, S., Kodama, S., Himeji, Y., et al. (2012) · Acta Cytologica · doi:10.1159/000337641 · Cited by 42 · see citing works
Castle, P. E., Bulten, J., Confortini, M., Klinkhamer, P. J. J. M., Pellegrini, A., Siebers, A. G., Ronco, G., & Arbyn, M. (2010) · BJOG An International Journal of Obstetrics & Gynaecology · doi:10.1111/j.1471-0528.2010.02650.x · Cited by 41 · see citing works
da Silva, C. S., Adad, S. J., de Souza, M. A. H., Barcelos, A. C. M., Terra, A. P. S., & Murta, E. F. C. (2004) · Gynecologic and Obstetric Investigation · doi:10.1159/000079822 · Cited by 37 · see citing works
Biological effects of probiotics: what impact does Lactobacillus casei shirota have on us?
Nanno, M., Kato, I., Kobayashi, T., & Shida, K. (2011) · PubMed · Cited by 37 · see citing works
The influence of probiotics on the cervical malignancy diagnostics quality
Perisić, Z., Perisic, N., Goločorbin-Kon, S., Vešović, D., Mitrovic‐Jovanovic, A., & Mikov, M. (2011) · Vojnosanitetski pregled · doi:10.2298/vsp100809001p · Cited by 13 · see citing works
Cianci, A., Giordano, R., Delia, A., Grasso, E., Amodeo, A., Leo, V. D., & Caccamo, F. (2008) · PubMed · Cited by 9 · see citing works
Persistence of Lactobacilli in Postmenopausal Women - A Double-Blind, Randomized, Pilot Study
Kwak, Y., Daroczy, K., Colque, P., et al. (2016) · Gynecologic and Obstetric Investigation · doi:10.1159/000446946 · Cited by 9 · see citing works
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The Potential Impact of Probiotics on Human Health: An Update on Their Health-Promoting Properties
Maftei, N.-M., Raileanu, C. R., Balta, A. A., Ambrose, L., Boev, M., Marin, D. B., & Lisa, E. L. (2024) · Microorganisms · doi:10.3390/microorganisms12020234 · Cited by 381 · see citing works
Viral Infections, the Microbiome, and Probiotics
Harper, A., Vijayakumar, V., Ouwehand, A. C., ter Haar, J., Obis, D., Espadaler, J., Binda, S., Desiraju, S., & Day, R. (2021) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2020.596166 · Cited by 177 · see citing works
- Authors
- Ou, Y.-C., Fu, H.-C., Tseng, C.-W., Wu, C.-H., Tsai, C.-C., & Lin, H.
- Affiliations
- Chang Gung Memorial Hospital (TW)
- Chang Gung University (TW)
- Corresponding author
- Lin, Hao
- Venue
- BMC Women's Health
- Published
- 2019-07-24
- Volume
- 19
- Issue
- 1
- Pages
- 103-103
- ISSN
- 1472-6874 (ISSN-L)
- PMC
- PMC6657108
- OpenAlex
- W2963362732
- Cited by
- 87
- References
- 32
- Citations by year
- 2026: 14 · 2025: 16 · 2024: 14 · 2023: 20 · 2022: 7 · 2021: 13 · 2020: 3
- FWCI
- 4.22
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- BMC Women s Health (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- Chang Gung Memorial Research Grant (CMRPG890891)
- Topics
- Life Sciences › Immunology and Microbiology › Microbiology › Reproductive tract infections research
- Life Sciences › Agricultural and Biological Sciences › Food Science › Probiotics and Fermented Foods
- Health Sciences › Medicine › Epidemiology › Cervical Cancer and HPV Research
- Keywords
- probiotics, high-risk HPV, HPV clearance, Lactobacillus rhamnosus GR-1, Lactobacillus reuteri RC-14, vaginal microbiota, viral load, cervical cancer prevention
- MeSH terms
- Adult, Cervix Uteri, Double-Blind Method, Female, Genotype, Humans, Middle Aged, Retrospective Studies, Vagina, Vaginal Smears, Viral Load, Probiotics, Papillomaviridae, Papillomavirus Infections, Limosilactobacillus reuteri, Lacticaseibacillus rhamnosus
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