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It Is All about Probiotics to Control Cervical Cancer

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Abstract

Cervical cancer (CC) is the fourth most common malignancy in female patients. “Human papillomavirus” (HPV) contamination is a leading cause of all forms of cervical cancer, accounting for an expected 570,000 reported incidents in 2018. Two HPV strains (16 and 18) are responsible for 70% of CC and pre-cancerous cervical abnormalities. CC is one of the foremost reasons for the malignancy death rate in India among women ranging from 30 to 69 years of age in India, responsible for 17% of all cancer deaths. Currently approved cervical cancer treatments are associated with adverse reactions that might harm the lives of women affected by this disease. Consequently, probiotics can play a vital role in the treatment of CC. It is reflected from various studies regarding the role of probiotics in the diagnosis, prevention or treatment of cancer. In this review article, we have discussed the rationale of probiotics for treatment of CC, the role of probiotics as effective adjuvants in anti-cancer therapy and the combined effect of the anti-cancer drug along with probiotics to minimize the side effects due to chemotherapy.

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Data Availability

Data sharing is not applicable to this article as no new data were created or analysed in this study.

Abbreviations

CC:

Cervical cancer

HPV:

Human papillomavirus

MDR:

Multi-drug resistance

ROS:

Reactive oxygen species

RNS:

Reactive nitrogen species

P-gp:

P-glycoprotein

HIV:

Human immunodeficiency virus

GPCRs:

G protein-coupled receptors

Th17:

T-helper 17

SCFAs:

Short-chain fatty acids

N.K. cell:

Natural killer cell

LPS:

Lipopolysaccharide

TLR4:

Toll-like receptor 4

NF-κβ:

Nuclear factor-Κb

D. C. :

Dendritic cell

sIgA:

Soluble IgA

IBS:

Irritable bowel syndrome

IFN-γ:

Interferon-gamma

PRF1:

Perforin 1

SOD:

Superoxide dismutase

Gpx:

Glutathione peroxidase

GST:

Glutathione-S-transferase

CIN:

Intraepithelial neoplasia

O. S.:

Oxidative stress

LAB:

Lactic acid bacteria

4-NOO:

4-Nitroquinoline 1-oxide

EPS:

Exopolysaccharides

TNF-α:

Tumour necrosis factor

CFU:

Colony-forming unit

CTLA-4:

Cytotoxic T lymphocyte antigen 4

PD-1:

Programmed death-1

IL-13:

Interleukin-13

ZO-1:

Zonulae occludentes

L. S.:

lactobacillus Supernatants

G. I.:

Gastrointestinal

References

  1. WHO (2010) Projections of mortality and burden of disease. 2004–2030. Available from www.who.int/healthinfo/global_burden_disease/projections/en/index.html (Accessed 10 Nov 2021)

  2. Nature Biotechnology vol 18 supplement 2000, IT18- 20. Available from: http://biotech.nature.com (Accessed 10 Nov 2021)

  3. Zeller JL, Lynm C, Glass RM (2007) Carcinoma of the cervix. JAMA 298(19):2336–2336

    Article  CAS  PubMed  Google Scholar 

  4. Kaku M, Mathew A, Rajan B (2008) Impact of socio-economic factors in delayed reporting and late-stage presentation among patients with cervix cancer in a major cancer hospital in South India. Asian Pac J Cancer Prev 9(4):589–594

    PubMed  Google Scholar 

  5. Shazly SA, Murad MH, Dowdy SC, Gostout BS, Famuyide AO (2015) Robotic radical hysterectomy in early-stage cervical cancer: a systematic review and meta-analysis. Gynecol Oncol 138(2):457–471

    Article  PubMed  Google Scholar 

  6. Aggarwal P (2014) Cervical cancer: can it be prevented? World journal of clinical oncology 5(4):775

    Article  PubMed  PubMed Central  Google Scholar 

  7. Lorusso D, Petrelli F, Coinu A, Raspagliesi F, Barni S (2014) A systematic review comparing cisplatin and carboplatin plus paclitaxel-based chemotherapy for recurrent or metastatic cervical cancer. Gynecol Oncol 133(1):117–123

    Article  CAS  PubMed  Google Scholar 

  8. Kang YJ, O’Connell DL, Tan J, Lew JB, Demers A, Lotocki R, Canfell K (2015) Optimal uptake rates for initial treatments for cervical cancer in concordance with guidelines in Australia and Canada: results from two large cancer facilities. Cancer Epidemiol 39(4):600–611

  9. Das R, Bhattacharya K, Samanta SK, Pal BC, Mandal C (2014) Improved chemosensitivity in cervical cancer to cisplatin: synergistic activity of mahanine through STAT3 inhibition. Cancer Lett 351(1):81–90

    Article  CAS  PubMed  Google Scholar 

  10. Wolinsky JB, Colson YL, Grinstaff MW (2012) Local drug delivery strategies for cancer treatment: gels, nanoparticles, polymeric films, rods, and wafers. J Control Release 159(1):14–26

    Article  CAS  PubMed  Google Scholar 

  11. Dos Reis SA, da Conceição LL, Peluzio MDCG (2019) Intestinal microbiota and colorectal cancer: changes in the intestinal microenvironment and their relation to the disease. J Med Microbiol 68(10):1391–1407

    Article  PubMed  Google Scholar 

  12. Requena T, Martínez-Cuesta MC, Peláez C (2018) Diet and microbiota linked in health and disease. Food Funct 9(2):688–704

    Article  CAS  PubMed  Google Scholar 

  13. Dos Reis SA, da Conceição LL, Siqueira NP, Rosa DD, da Silva LL, Maria do Carmo, G. P. (2017) Review of the mechanisms of probiotic actions in the prevention of colorectal cancer. Nutr Res 37:1–19

    Article  PubMed  Google Scholar 

  14. Rangel-Colmenero BR, Gomez-Gutierrez JG, Villatoro-Hernández J, Zavala-Flores LM, Quistián-Martínez D, Rojas-Martínez A, Saucedo-Cárdenas O (2014) Enhancement of Ad-CRT/E7-mediated antitumor effect by preimmunization with L. lactis expressing HPV-16 E7. Viral immunol 27(9):463–467

  15. Li Y, Yu T, Yan H, Li D, Yu T, Yuan T, Baloch Z (2020) Vaginal microbiota and HPV infection: novel mechanistic insights and therapeutic strategies. Infect Drug Resist 13:1213

  16. Vétizou M, Pitt JM, Daillère R, Lepage P, Waldschmitt N, Flament C, Zitvogel L (2015) Anticancer immunotherapy by CTLA-4 blockade relies on the gut microbiota. Science 350(6264):1079–1084

  17. Nami Y, Abdullah N, Haghshenas B, Radiah D, Rosli R, Khosroushahi AY (2014) Assessment of probiotic potential and anticancer activity of newly isolated vaginal bacterium Lactobacillus plantarum 5BL. Microbiol Immunol 58(9):492–502

    Article  CAS  PubMed  Google Scholar 

  18. Wang KD, Xu DJ, Wang BY, Yan DH, Lv Z, Su JR (2018) Inhibitory effect of vaginal Lactobacillus supernatants on cervical cancer cells. Probiotics and antimicrobial proteins 10(2):236–242

    Article  PubMed  Google Scholar 

  19. McMillan A, Dell M, Zellar MP, Cribby S, Martz S, Hong E, Reid G (2011) Disruption of urogenital biofilms by lactobacilli. Coll Surf B Biointer 86(1):58–64

  20. Boris S, Barbés C (2000) Role played by lactobacilli in controlling the population of vaginal pathogens. Microbes Infect 2(5):543–546

    Article  CAS  PubMed  Google Scholar 

  21. Li X, Wang H, Du X, Yu W, Jiang J, Geng Y, Ma C (2017) Lactobacilli inhibit cervical cancer cell migration in vitro and reduce tumor burden in vivo through upregulation of E-cadherin. Oncol Rep 38(3):1561–1568

  22. Rashid NN, Rothan HA, Yusoff MSM (2015) The association of mammalian DREAM complex and HPV16 E7 proteins. Am J Cancer Res 5(12):3525

    CAS  PubMed  PubMed Central  Google Scholar 

  23. Gantois I, Ducatelle R, Pasmans F, Haesebrouck F, Hautefort I, Thompson A, Van Immerseel F (2006) Butyrate specifically down-regulates Salmonella pathogenicity island 1 gene expression. Appl Environ Microbiol 72(1):946–949

  24. Falzone L, Salomone S, Libra M (2018) Evolution of cancer pharmacological treatments at the turn of the third millennium. Front Pharmacol 9:1300

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Mego M, Holec V, Drgona L, Hainova K, Ciernikova S, Zajac V (2013) Probiotic bacteria in cancer patients undergoing chemotherapy and radiation therapy. Complement Ther Med 21(6):712–723

    Article  PubMed  Google Scholar 

  26. Maria-Aggeliki KS, Nikolaos KL, Kyrias GM, Vassilis KE (2009) The potential clinical impact of probiotic treatment for the prevention and/or anti-inflammatory therapeutic effect against radiation induced intestinal mucositis. A review. Recent Patents Inflamm Allerg drug Discov 3(3):195–200

  27. Zitvogel L, Ma Y, Raoult D, Kroemer G, Gajewski TF (2018) The microbiome in cancer immunotherapy: diagnostic tools and therapeutic strategies. Science 359(6382):1366–1370

    Article  CAS  PubMed  Google Scholar 

  28. Peterson DE, Boers-Doets CB, Bensadoun RJ, Herrstedt J (2015) Management of oral and gastrointestinal mucosal injury: ESMO Clinical Practice Guidelines for diagnosis, treatment, and follow-up. Ann Oncol 26:v139–v151

    Article  PubMed  Google Scholar 

  29. Gianotti L, Morelli L, Galbiati F, Rocchetti S, Coppola S, Beneduce A, Braga M (2010) A randomized double-blind trial on perioperative administration of probiotics in colorectal cancer patients. World journal of gastroenterology: WJG 16(2):167

  30. Demers M, Dagnault A, Desjardins J (2014) A randomized double-blind controlled trial: impact of probiotics on diarrhea in patients treated with pelvic radiation. Clin Nutr 33(5):761–767

    Article  PubMed  Google Scholar 

  31. Theodoropoulos GE, Memos NA, Peitsidou K, Karantanos T, Spyropoulos BG, Zografos G (2016) Synbiotics and gastrointestinal function-related quality of life after elective colorectal cancer resection. Annals of Gastroenterology: Quarterly Publication of the Hellenic Society of Gastroenterology 29(1):56

    Google Scholar 

  32. Flesch AT, Tonial ST, Contu PDC, Damin DC (2017) Perioperative synbiotics administration decreases postoperative infections in patients with colorectal cancer: a randomized, double-blind clinical trial. Rev Col Bras Cir 44:567–573

    Article  PubMed  Google Scholar 

  33. Negi D, Singh A, Joshi N, Mishra N (2020) Cisplatin and probiotic biomass loaded pessaries for the management of cervical cancer. Anticancer Agents in Medicinal Chemistry (Formerly Current Medicinal Chemistry-Anti-Cancer Agents) 20(5):589–598

  34. Chitapanarux I, Chitapanarux T, Traisathit P, Kudumpee S, Tharavichitkul E, Lorvidhaya V (2010) Randomized controlled trial of live lactobacillus acidophilus plus Bifidobacterium bifidum in prophylaxis of diarrhea during radiotherapy in cervical cancer patients. Radiat Oncol 5(1):1–6

    Article  Google Scholar 

  35. Okawa T, Niibe H, Arai T, Sekiba K, Noda K, Takeuchi S, Ogawa N (1993) Effect of LC9018 combined with radiation therapy on carcinoma of the uterine cervix. A phase III, multicenter, randomized, controlled study. Cancer 72(6):1949–1954

  36. Sivan A, Corrales L, Hubert N, Williams JB, Aquino-Michaels K, Earley ZM, Gajewski TF (2015) Commensal Bifidobacterium promotes antitumor immunity and facilitates anti–PD-L1 efficacy. Science 350(6264):1084–1089

  37. Gui QF, Lu HF, Zhang CX, Xu ZR, Yang YH (2015) Well-balanced commensal microbiota contributes to anticancer response in a lung cancer mouse model. Genet Mol Res 14(2):5642–5651

    Article  PubMed  Google Scholar 

  38. Heczko PB, Tomusiak A, Adamski P, Jakimiuk AJ, Stefański G, Mikołajczyk-Cichońska A, Strus M (2015) Supplementation of standard antibiotic therapy with oral probiotics for bacterial vaginosis and aerobic vaginitis: a randomized, double-blind, placebo-controlled trial. BMC Women's Health 15(1):1–12

  39. Recine N, Palma E, Domenici L, Giorgini M, Imperiale L, Sassu C, Panici PB (2016) Restoring vaginal microbiota: biological control of bacterial vaginosis. A prospective case–control study using Lactobacillus rhamnosus BMX 54 as adjuvant treatment against bacterial vaginosis. Archives Gynecol Obstet 293(1):101–107

  40. Laue C, Papazova E, Liesegang A, Pannenbeckers A, Arendarski P, Linnerth B, Schrezenmeir J (2018) Effect of a yoghurt drink containing Lactobacillus strains on bacterial vaginosis in women–a double-blind, randomized, controlled clinical pilot trial. Beneficial Microbes 9(1):35–50

  41. Gopalakrishnan V, Spencer CN, Nezi L, Reuben A, Andrews MC, Karpinets TV, Prieto PA, Vicente D, Hoffman K, Wei SC, Cogdill AP (2018) Gut microbiome modulates response to anti–PD-1 immunotherapy in melanoma patients. Science 359(6371):97–103

    Article  CAS  PubMed  Google Scholar 

  42. Kim SN, Lee WM, Park KS, Kim JB, Han DJ, Bae J (2015) The effect of Lactobacillus casei extract on cervical cancer cell lines. Contemp Oncol 19(4):306

    CAS  Google Scholar 

  43. Villéger R, Lopès A, Carrier G, Veziant J, Billard E, Barnich N, Bonnet M (2019) Intestinal microbiota: a novel target to improve antitumor treatment?. Intern J Mole Sci 20(18):4584

  44. Pardoll DM (2012) The blockade of immune checkpoints in cancer immunotherapy. Nat Rev Cancer 12(4):252–264

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Vétizou M, Pitt JM, Daillère R, Lepage P, Waldschmitt N, Flament C, Zitvogel L (2015) Anticancer immunotherapy by CTLA-4 blockade relies on the gut microbiota. Science 350(6264):1079–1084

    Article  PubMed  PubMed Central  Google Scholar 

  46. Palma E, Recine N, Domenici L, Giorgini M, Pierangeli A, Panici PB (2018) Long-term Lactobacillus rhamnosus BMX 54 application to restore a balanced vaginal ecosystem: a promising solution against HPV-infection. BMC Infect Dis 18(1):1–7

    Article  Google Scholar 

  47. Devasagayam TPA, Tilak JC, Boloor KK, Sane KS, Ghaskadbi SS, Lele RD (2004) Free radicals and antioxidants in human health: current status and future prospects. Japi 52(794804):4

    Google Scholar 

  48. Nathan C (2003) Specificity of a third kind: reactive oxygen and nitrogen intermediates in cell signaling. J Clin Investig 111(6):769–778

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Bosch FX, Poljak M, Rogovskaya SI, Castellsagué X, Brotons M, Syrjänen S (2013) Comprehensive control of HPV infections and related diseases in the Central and Eastern Europe and Central Asia Region. Vaccine 31(Suppl. 7)

  50. Woodman CB, Collins SI, Young LS (2007) The natural history of cervical HPV infection: unresolved issues. Nat Rev Cancer 7(1):11–22

    Article  CAS  PubMed  Google Scholar 

  51. Zur Hausen H (2002) Papillomaviruses and cancer: from basic studies to clinical application. Nat Rev Cancer 2(5):342–350

    Article  CAS  PubMed  Google Scholar 

  52. Von Knebel Doeberitz M (2002) New markers for cervical dysplasia to visualize the genomic chaos created by aberrant oncogenic papillomavirus infections. Eur J Cancer 38(17):2229–2242

    Article  Google Scholar 

  53. Doorbar J, Quint W, Banks L, Bravo IG, Stoler M, Broker TR, Stanley MA (2012) The biology and life-cycle of human papillomaviruses. Vaccine 30:F55–F70

    Article  CAS  PubMed  Google Scholar 

  54. Kgatle MM, Spearman CW, Kalla AA, Hairwadzi HN (2017) DNA oncogenic virus-induced oxidative stress, genomic damage, and aberrant epigenetic alterations. Oxidative Med Cell Long

  55. Williams VM, Filippova M, Soto U, Duerksen-Hughes PJ (2011) HPV-DNA integration and carcinogenesis: putative roles for inflammation and oxidative stress. Futur Virol 6(1):45–57

    Article  Google Scholar 

  56. Holley AK, Dhar SK, Xu Y, Clair DKS (2012) Manganese superoxide dismutase: beyond life and death. Amino Acids 42(1):139–158

    Article  CAS  PubMed  Google Scholar 

  57. Kinnula VL, Crapo JD (2004) Superoxide dismutases in malignant cells and human tumors. Free Radical Biol Med 36(6):718–744

    Article  CAS  Google Scholar 

  58. Termini L, Fregnani JH, Boccardo E, Da Costa WH, Longatto-Filho A, Andreoli MA, Guimarães GC (2015) SOD2 immunoexpression predicts lymph node metastasis in penile cancer. BMC Clin Pathol 15(1):1–8

  59. Zhang M, Wang F, Jiang L, Liu R, Zhang L, Lei X, Ren F (2013) Lactobacillus salivarius REN inhibits rat oral cancer induced by 4-nitroquioline 1-oxide. Cancer Prev Res 6(7):686–694

  60. Kim JE, Kim JY, Lee KW, Lee HJ (2007) Cancer chemopreventive effects of lactic acid bacteria. J Microbiol Biotechnol 17(8):1227–1235

    PubMed  Google Scholar 

  61. Zhang M, Wang F, Jiang L, Liu R, Zhang L, Lei X, Li J, Jiang J, Guo H, Fang B, Zhao L (2013) Lactobacillus salivarius REN inhibits rat oral cancer induced by 4-nitroquioline 1-oxide. Cancer Prev Res 6(7):686–694

    Article  CAS  Google Scholar 

  62. Ramesh V, Kumar R, Singh RRB, Kaushik JK, Mann B (2012) Comparative evaluation of selected strains of lactobacilli for the development of antioxidant activity in milk. Dairy science & technology 92(2):179–188

    Article  CAS  Google Scholar 

  63. Kishk YF, Al-Sayed HM (2007) Free-radical scavenging and antioxidative activities of some polysaccharides in emulsions. LWT-Food Science and Technology 40(2):270–277

    Article  CAS  Google Scholar 

  64. Bruno-Bárcena JM, Andrus JM, Libby SL, Klaenhammer TR, Hassan HM (2004) Expression of a heterologous manganese superoxide dismutase gene in intestinal lactobacilli provides protection against hydrogen peroxide toxicity. Appl Environ Microbiol 70(8):4702–4710

    Article  PubMed  PubMed Central  Google Scholar 

  65. Li GL, Jiang W, Xia Q, Chen SH, Ge XR, Gui SQ, Xu CJ (2010) HPV E6 down-regulation and apoptosis induction of human cervical cancer cells by a novel lipid-soluble extract (P.E.) from Pinellia pedatisecta Schott in vitro. J Ethnopharmacol 132(1):56–64

  66. Lin MY, Chang FJ (2000) Antioxidative effect of intestinal bacteria Bifidobacterium longum ATCC 15708 and Lactobacillus acidophilus ATCC 4356. Dig Dis Sci 45(8):1617–1622

    Article  CAS  PubMed  Google Scholar 

  67. Choi SS, Kim Y, Han KS, You S, Oh S, Kim SH (2006) Effects of Lactobacillus strains on cancer cell proliferation and oxidative stress in vitro. Lett Appl Microbiol 42(5):452–458

    Article  CAS  PubMed  Google Scholar 

  68. Azad M, Kalam A, Sarker M, Li T, Yin J (2018) Probiotic species in the modulation of gut microbiota: an overview. BioMed Res Intern

  69. Hill C, Guarner F, Reid G, Gibson GR, Merenstein DJ, Pot B, Sanders ME (2014) Expert consensus document: The International Scientific Association for Probiotics and Prebiotics consensus statement on the scope and appropriate use of the term probiotic. Nat Rev Gastroenterol Hepatol

  70. Brown AC, Valiere A (2004) Probiotics and medical nutrition therapy. Nutrition in clinical care: an official publication of Tufts University 7(2):56

    PubMed  Google Scholar 

  71. Kristensen NB, Bryrup T, Allin KH, Nielsen T, Hansen TH, Pedersen O (2016) Alterations in fecal microbiota composition by probiotic supplementation in healthy adults: a systematic review of randomized controlled trials. Genome medicine 8(1):1–11

    Article  Google Scholar 

  72. Rao SC, Athalye-Jape GK, Deshpande GC, Simmer KN, Patole SK (2016) Probiotic supplementation and late-onset sepsis in preterm infants: a meta-analysis. Pediatrics 137(3)

  73. Kankaanpää P, Sütas Y, Salminen S, Isolauri E (2003) Homogenates derived from probiotic bacteria provide down-regulatory signals for peripheral blood mononuclear cells. Food Chem 83(2):269–277

    Article  Google Scholar 

  74. Di Felice G, Barletta B, Butteroni C, Corinti S, Tinghino R, Colombo P, Boirivant M (2008) Use of probiotic bacteria for prevention and therapy of allergic diseases: studies in mouse model of allergic sensitization. J Clin Gastroenterol 42:S130–S132

    Article  PubMed  Google Scholar 

  75. Sagheddu V, Guidesi E, Galletti S, Elli M (2019) Original paper selection and characterization criteria of probiotics intended for human use from the past to the future. Food Sci Nutr 3(10.22158)

  76. Koller VJ, Marian B, Stidl R, Nersesyan A, Winter H, Simić T, Knasmüller S (2008) Impact of lactic acid bacteria on oxidative DNA damage in human derived colon cells. Food Chem Toxicol 46(4):1221–1229

  77. Łaniewski P, Ilhan ZE, Herbst-Kralovetz MM (2020) The microbiome and gynaecological cancer development, prevention and therapy. Nat Rev Urol 17(4):232–250

    Article  PubMed  PubMed Central  Google Scholar 

  78. Kailasapathy K, Chin J (2000) Survival and therapeutic potential of probiotic organisms with reference to Lactobacillus acidophilus and Bifidobacterium spp. Immunol Cell Biol 78(1):80–88

    Article  CAS  PubMed  Google Scholar 

  79. Saber A, Alipour B, Faghfoori Z, Yari Khosroushahi A (2017) Cellular and molecular effects of yeast probiotics on cancer. Crit Rev Microbiol 43(1):96–115

    Article  PubMed  Google Scholar 

  80. Wang Y, Wu Y, Wang Y, Xu H, Mei X, Yu D, Li W (2017) Antioxidant properties of probiotic bacteria. Nutrients 9(5):521

  81. Chen CC, Lin WC, Kong MS, Shi HN, Walker WA, Lin CY, Lin TY (2012) Oral inoculation of probiotics Lactobacillus acidophilus NCFM suppresses tumour growth both in segmental orthotopic colon cancer and extra-intestinal tissue. Brit J Nutrit 107(11):1623–1634

  82. Drago L (2019) Probiotics and colon cancer Microorganisms 7(3):66

    CAS  PubMed  Google Scholar 

  83. El-Nezami HS, Polychronaki NN, Ma J, Zhu H, Ling W, Salminen EK, Mykkänen HM (2006) Probiotic supplementation reduces a biomarker for increased risk of liver cancer in young men from Southern China. Am J Clin Nutr 83(5):1199–1203

    Article  CAS  PubMed  Google Scholar 

  84. Liu ZH, Huang MJ, Zhang XW, Wang L, Huang NQ, Peng H, Wang JP (2013) The effects of perioperative probiotic treatment on serum zonulin concentration and subsequent postoperative infectious complications after colorectal cancer surgery: a double-center and double-blind randomized clinical trial. Am J Clin Nutrition 97(1):117–126

  85. Kassayova M, Bobrov N, Strojný L, Kiskova T, Mikeš J, Demečková V, Bomba A (2014) Preventive effects of probiotic bacteria Lactobacillus plantarum and dietary fiber in chemically-induced mammary carcinogenesis. Anticancer Research 34(9):4969–4975

  86. Tian Y, Li M, Song W, Jiang R, Li YQ (2019) Effects of probiotics on chemotherapy in patients with lung cancer. Oncol Lett 17(3):2836–2848

    CAS  PubMed  PubMed Central  Google Scholar 

  87. Fettweis, J. M., Brooks, J. P., Serrano, M. G., Sheth, N. U., Girerd, P. H., Edwards, D. J., … & Vaginal Microbiome Consortium (2014) Differences in vaginal microbiome in African American women versus women of European ancestry. Microbiology 160(Pt 10):2272

    Google Scholar 

  88. Pourmollaei S, Barzegari A, Farshbaf-Khalili A, Nouri M, Fattahi A, Shahnazi M, Dittrich R (2020) Anticancer effect of bacteria on cervical cancer: m olecular aspects and therapeutic implications. Life Sci 246:117413

    Article  CAS  PubMed  Google Scholar 

  89. Yim EK, Park JS (2005) The role of HPV E6 and E7 oncoproteins in HPV-associated cervical carcinogenesis. Cancer research and treatment: official journal of Korean Cancer Association 37(6):319

    Article  Google Scholar 

  90. Rajoka MSR, Zhao H, Lu Y, Lian Z, Li N, Hussain N, Shi J (2018) Anticancer potential against cervix cancer (HeLa) cell line of probiotic Lactobacillus casei and Lactobacillus paracasei strains isolated from human breast milk. Food Funct 9(5):2705–2715

  91. Sungur T, Aslim B, Karaaslan C, Aktas B (2017) Impact of Exopolysaccharides (EPSs) of Lactobacillus gasseri strains isolated from human vagina on cervical tumor cells (HeLa). Anaerobe 47:137–144

    Article  PubMed  Google Scholar 

  92. Nouri Z, Karami F, Neyazi N, Modarressi MH, Karimi R, Khorramizadeh MR, Motevaseli E (2016) Dual anti-metastatic and anti-proliferative activity assessment of two probiotics on HeLa and HT-29 cell lines. Cell J (Yakhteh) 18(2):127

  93. Cha MK, Lee DK, An HM, Lee SW, Shin SH, Kwon JH, Ha NJ (2012) Antiviral activity of Bifidobacterium adolescentis SPM1005-A on human papillomavirus type 16. BMC Med 10(1):1–6

  94. Li C, Jia L, Yu Y, Jin L (2019) Lactic acid induced microRNA-744 enhances motility of SiHa cervical cancer cells through targeting ARHGAP5. Chem Biol Interact 298:86–95

    Article  CAS  PubMed  Google Scholar 

  95. Linn YH, Thu KK, Win NHH (2019) Effect of probiotics for the prevention of acute radiation-induced diarrhoea among cervical cancer patients: a randomized double-blind placebo-controlled study. Probiotics and antimicrobial proteins 11(2):638–647

    Article  CAS  PubMed  Google Scholar 

  96. Giralt J, Regadera JP, Verges R, Romero J, de la Fuente I, Biete A, Guarner F (2008) Effects of probiotic Lactobacillus casei DN-114 001 in prevention of radiation-induced diarrhea: results from multicenter, randomized, placebo-controlled nutritional trial. Intern J Rad Oncol Biol Phys 71(4):1213–1219

  97. Delia P, Sansotta G, Donato V, Frosina P, Messina G, De Renzis C, Famularo G (2007) Use of probiotics for prevention of radiation-induced diarrhea. World J Gastroenterol: WJG 13(6):912

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  98. Kaur IP, Chopra K, Saini A (2002) Probiotics: potential pharmaceutical applications. Eur J Pharm Sci 15(1):1–9

    Article  CAS  PubMed  Google Scholar 

  99. Ortiz GG, de Loera Rodríguez LH, Moragrega PR et al (2018) Effect of symbiotic supplementation on fecal calprotectin levels and lactic acid bacteria, Bifidobacteria, Escherichia coli and Salmonella DNA in patients with cervical cancer. Nutr Hosp 35(6):1394–1400

    PubMed  Google Scholar 

  100. Pardini B, De Maria D, Francavilla A, Di Gaetano C, Ronco G, Naccarati A (2018) MicroRNAs as markers of progression in cervical cancer: a systematic review. BMC Cancer 18(1):1–17

    Article  Google Scholar 

  101. Saadat YR, Pourseif MM, Vahed SZ, Barzegari A, Omidi Y, Barar J (2020) Modulatory role of vaginal-isolated lactococcus lactis on the expression of miR-21, miR-200b, and TLR-4 in CAOV-4 cells and in silico revalidation. Probiotics and antimicrobial proteins 12(3):1083–1096

    Article  Google Scholar 

  102. Rodríguez-Nogales A, Algieri F, Garrido-Mesa J, Vezza T, Utrilla MP, Chueca N, Gálvez J (2018) The administration of Escherichia coli Nissle 1917 ameliorates development of DSS-induced colitis in mice. Front Pharmacol 9:468

  103. Yousefi B, Eslami M, Ghasemian A, Kokhaei P, Salek Farrokhi A, Darabi N (2019) Probiotics importance and their immunomodulatory properties. J Cell Physiol 234(6):8008–8018

    Article  CAS  PubMed  Google Scholar 

  104. Kim DE, Kim JK, Han SK, Jang SE, Han MJ, Kim DH (2019) Lactobacillus plantarum NK3 and Bifidobacterium longum NK49 alleviate bacterial vaginosis and osteoporosis in mice by suppressing NF-κ B-Linked TNF-α expression. J Med Food 22(10):1022–1031

    Article  CAS  PubMed  Google Scholar 

  105. Lee HJ, Lim SM, Kim DH (2018) Lactobacillus johnsonii CJLJ103 attenuates scopolamine-Induced memory impairment in mice by increasing BDNF expression and inhibiting NF-κB activation. J Microbiol Biotechnol 28(9):1443–1446

    Article  CAS  PubMed  Google Scholar 

  106. Yang SF, Yuan SSF, Yeh YT, Wu MT, Su JH, Hung SC, Chai CY (2005) The role of p-STAT3 (ser727) revealed by its association with Ki-67 in cervical intraepithelial neoplasia. Gynecol Oncol 98(3):446–452

    Article  CAS  PubMed  Google Scholar 

  107. Chen CL, Hsieh FC, Lieblein JC, Brown J, Chan C, Wallace JA, Lin J (2007) Stat3 activation in human endometrial and cervical cancers. British J Cancer 96(4):591–599

  108. Shukla S, Shishodia G, Mahata S, Hedau S, Pandey A, Bhambhani S, Bharti AC (2010) Aberrant expression and constitutive activation of STAT3 in cervical carcinogenesis: implications in high-risk human papillomavirus infection. Molecular Cancer 9(1):1–17

  109. Morgan EL, Macdonald A (2019) Autocrine STAT3 activation in HPV positive cervical cancer through a virus-driven Rac1—NFκB—IL-6 signalling axis. PLoS Pathog 15(6):e1007835

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  110. Do EJ, Hwang SW, Kim SY, Ryu YM, Cho EA, Chung EJ, Myung SJ (2016) Suppression of colitis‐associated carcinogenesis through modulation of IL‐6/STAT3 pathway by balsalazide and VSL# 3. J Gastroenterol Hepatol 31(8):1453–1461

  111. Zhou X, Qi W, Hong T, Xiong T, Gong D, Xie M, Nie S (2018) Exopolysaccharides from Lactobacillus plantarum NCU116 regulate intestinal barrier function via STAT3 signaling pathway. J Agric Food Chem 66(37):9719–9727

    Article  CAS  PubMed  Google Scholar 

  112. Hou Q, Ye L, Liu H, Huang L, Yang Q, Turner JR, Yu Q (2018) Lactobacillus accelerates ISCs regeneration to protect the integrity of intestinal mucosa through activation of STAT3 signaling pathway induced by LPLs secretion of IL-22. Cell Death Differ 25(9):1657–1670

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  113. Hütt P, Lapp E, Štšepetova J, Smidt I, Taelma H, Borovkova N, Mändar R (2016) Characterization of probiotic properties in human vaginal lactobacilli strains. Microbial Ecol Health Dis 27(1):30484

  114. Zitvogel L, Daillère R, Roberti MP, Routy B, Kroemer G (2017) Anticancer effects of the microbiome and its products. Nat Rev Microbiol 15(8):465–478

    Article  CAS  PubMed  Google Scholar 

  115. Sharma P, Kaur S, Kaur R, Kaur M, Kaur S (2018) Proteinaceous secretory metabolites of probiotic human commensal Enterococcus hirae 20c, E. faecium 12a and L12b as antiproliferative agents against cancer cell lines. Front Microbiol 9:948

  116. Piqué N, Berlanga M, Miñana-Galbis D (2019) Health benefits of heat-killed (Tyndallized) probiotics: an overview. Int J Mol Sci 20(10):2534

    Article  PubMed  PubMed Central  Google Scholar 

  117. Han KJ, Lee NK, Park H, Paik HD (2015) Anticancer and anti-inflammatory activity of probiotic Lactococcus lactis NK34. J Microbiol Biotechnol 25(10):1697–1701

    Article  PubMed  Google Scholar 

  118. Perwez Hussain S, Harris CC (2007) Inflammation and cancer: an ancient link with novel potentials. Int J Cancer 121(11):2373–2380

    Article  PubMed  Google Scholar 

  119. Blasingame CA, Billups LH, Graham T, Henry J, Carter B, Threadgill DW, Alexander AD (2016) Modulation of colorectal cancer by the probiotic organism Lactobacillus reuteri. Prof Agricul Work J (PAWJ) 3(174–2016–2152)

  120. Liu CT, Chu FJ, Chou CC, Yu RC (2011) Antiproliferative and anticytotoxic effects of cell fractions and exopolysaccharides from Lactobacillus casei 01. Mutation Research/Genetic Toxicology and Environmental Mutagenesis 721(2):157–162

    Article  CAS  Google Scholar 

  121. Li J, Sung CYJ, Lee N, Ni Y, Pihlajamäki J, Panagiotou G, El-Nezami H (2016) Probiotics modulated gut microbiota suppresses hepatocellular carcinoma growth in mice. Proc Natl Acad Sci 113(9):E1306–E1315

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  122. Fooladi AAI, Yazdi MH, Pourmand MR, Mirshafiey A, Hassan ZM, Azizi T, Dallal MMS (2015) Th1 cytokine production induced by Lactobacillus acidophilus in BALB/c mice bearing transplanted breast tumor. Jundishapur J Microbiol 8(4)

  123. Kassayova M, Bobrov N, Strojný L, Orendáš P, Demečková V, Jendželovský R, Fedoročko P (2016) Anticancer and immunomodulatory effects of Lactobacillus plantarum L.S./07, inulin and melatonin in NMU-induced rat model of breast cancer. Anticancer Research 36(6):2719–2728

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S.A. Concept and drafting, A.F. Review and research methodology, F.J.A. Editing and visualization, T.K. Writing, N.M. Data curation.

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Ashique, S., Faruk, A., Ahmad, F.J. et al. It Is All about Probiotics to Control Cervical Cancer. Probiotics & Antimicro. Prot. 16, 979–992 (2024). https://doi.org/10.1007/s12602-023-10183-2

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