Systematic Reviews and Meta Analysis
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A systematic review of antiproliferative and antitumour activity of earthworm extracts

Year 2024, Volume: 25 Issue: 1, 111 - 120, 15.04.2024

Burcu Yüksel Asuman Deveci Özkan

https://doi.org/10.23902/trkjnat.1373797

Abstract

Earthworm extracts have become an interesting research area in cancer research due to their ingredients with anticancer and antiproliferative activities. Determining the anticancer effect of an extract on cancer cells may lead to new treatment strategies and alternative medicine to at least reduce the toxic effects of chemotherapeutic agents. In the present study, we aimed to raise awareness for drug development and future anticancer therapeutics by emphasizing the nature of earthworm extracts and the types of cancer they are used in through a systematic review. A systematic search of CINAHL, PubMed, Medline, Scopus and Web of Science databases was conducted to identify publications published between January 2018 and December 2022. We used different arrangements of the keywords ‘earthworm’, ‘earthworm extract’ and ‘anticancer effect’. We identified original studies written in English depicting in vitro and in vivo cytotoxic effects of earthworm extracts on cancer cells, and included these studies in our review. We found 15 studies matching our search criteria. Among the studies, Eisenia foetida (Savigny) was determined as the most studied earthworm, and colon cancer was the most frequently studied cancer type. The coleomic fluid was found to be the commonly used extract yielding positive results.

Keywords

Anticancer effect Antiproliferative Cancer therapy Coleomic fluid Eisenia foetida Colon cancer

Ethical Statement

Since the article does not contain any studies with human or animal subject, its approval to the ethics committee was not required.

References

  • 1. Augustine, D., Rao, R.S., Jayaraman, A. & Murthy K.C. 2018. Antiproliferative activity of earthworm coelomic fluid using oral squamous carcinoma KB 3-1 cells: an in vitro study with serine protease analysis. Pharmacognosy Magazine, 14(59): 528. http://dx.doi.org/10.4103/pm.pm_412_18
  • 2. Augustine. D., Rao. R.S., Anbu, J. & Murthy, K.C. 2019. In vitro cytotoxic and apoptotic induction effect of earthworm coelomic fluid of Eudrilus eugeniae, Eisenia foetida, and Perionyx excavatus on human oral squamous cell carcinoma-9 cell line. Toxicology Reports, 6: 347-357. https://doi.org/10.1016/j.toxrep.2019.04.005
  • 3. Augustine, D., Rao, R.S., Gns, H.S., Anbu, J. & Saraswathy, G.R. 2022. Anticancer Potential of Eudrilus Eugeniae Coelomic Fluid Protein on SCC-9 Cells-In Vitro Gene Expression entwined with Cutting-Edge In-Silico Strategy, Research Square. https://doi.org/10.21203/rs.3.rs-439242/v1
  • 4. Chabner, B.A. & Roberts, T.G. 2005 Chemotherapy and the war on cancer. Nature Reviews Cancer, 5(1): 65-72. https://doi.org/10.1038/nrc1529
  • 5. Czerwonka, A., Fiołka, M.J., Jędrzejewska, K., Jankowska, E., Zając, A. & Rzeski, W. 2020. Pro-apoptotic action of protein-carbohydrate fraction isolated from coelomic fluid of the earthworm Dendrobaena veneta against human colon adenocarcinoma cells. Biomedicine & Pharmacotherapy, 126: 110035. https://doi.org/10.1016/j.biopha.2020.110035
  • 6. Deveci Özkan, A., Alimudin, J., Kilciler, Y., Yuksel, B., Aksoy, O. & Betts, Z. 2022. In vitro chemo-protective effect of Eisenia foetida coelomic fluid against histone deacetylase inhibitor-induced oxidative toxicity in breast cancer cells. International Journal of Environmental Health Research, 1-10. https://doi.org/10.1080/09603123.2022.2120970
  • 7. Endharti, A.T., Purnamasari, Y., Primasari, R., Poeranto, S. & Permana, S. 2019. The coelomic fluid of Lumbricus rubellus synergistically enhances the cytotoxic effect of 5-Fluorouracil through modulation of focal adhesion kinase and P21 in the HT-29 cancer cell line. The Scientific World Journal, 2019: 5632859. https://doi.org/10.1155/2019/5632859
  • 8. Fiołka, M.J. Rzymowska, J., Bilska, S., Lewtak, K., Dmoszyńska‐Graniczka, M., Grzywnowicz, K. & Urbanik‐Sypniewska, T. 2019. Antitumor activity and apoptotic action of coelomic fluid from the earthworm Dendrobaena veneta against A549 human lung cancer cells. Apmis, 127(6): 435-448. https://doi.org/10.1111/apm.12941
  • 9. Gupta, S. & Yadav, S. 2016. Immuno-Defense Strategy in Earthworms: A Review Article. International Journal of 10. Current Microbiology and Applied Sciences. 5: 1022-1035 http://dx.doi.org/10.20546/ijcmas.2016.504.117.
  • 11. Hanahan, D. 2022. Hallmarks of cancer: new dimensions. Cancer discovery, 12(1): 31-46. https://doi.org/10.1158/2159-8290.CD-21-1059
  • 12. Hussain, M., Liaqat, I., Ali, N.M., Arshad, N., Hanif, U., Sajjad, S., Sardar, A.A., Awan, U.F., Khan, F.S. & Slahuddin. 2023. Antibacterial and Bacteriostatic Potential of Coelomic Fluid and Body Paste of Pheretima Posthuma (Vaillant, 1868) (Clitellata, Megascolecidae) against Ampicillin Resistant Clinical Bacterial Isolates. Brazilian Journal of Biology, 2023: 83, http://doi.org/10.1590/1519-6984.247016
  • 13. Kruk, J., Aboul-Enein, H.Y., Kładna, A. & Bowser, J.E. 2019. Oxidative stress in biological systems and its relationship with pathophysiological functions: the effect of physical activity on cellular redox homeostasis. Free radical research, 53(5): 497-521. https://doi.org/10.1080/10715762.2019.1612059
  • 14. Małota, K., Urbisz, A. & Skonieczna, M. 2022. Dose-dependent proliferative and pro-oxidative effects of earthworm coelomic fluid on the HCT116 colon cancer cell line. Research Square, https://doi.org/10.21203/rs.3.rs-2258914/v1
  • 15. Mustafa, R.G., Saiqa, A., Domínguez, J., Jamil, M., Manzoor, S., Wazir, S., Shaheen, B., Parveen, A., Khan, R., Ali, S., Ali, N.M. & Jalal, F. 2022. Therapeutic Values of Earthworm Species Extract from Azad Kashmir as Anticoagulant, Antibacterial, and Antioxidant Agents. Canadian Journal of Infectious Diseases and Medical Microbiology, 2022: 1-20. http://doi.org/10.1155/2022/6949117.
  • 16. Ozkan, A.D. & Yuksel, B. 2022. POLY I: c-ınduced TLR3 activation on oxidative stress levels in PC-3 (hormone insensıtıve) and LNCAP (hormonesensıtıve) as prostate cancer cells. Journal of Health Sciences of Kocaeli University, 8: 18-24. http://doi.org/10.30934/kusbed.915511
  • 17. Ozkan, A.D., Eskiler, G.G., Sarihan, M., Kazan, N., Aksoy, O., Yuksel, B. & Betts, Z. 2022. Anticancer properties of Eisenia foetida proteins in prostate cancer cells in vitro. International Journal of Peptide Research and Therapeutics, 28(4): 1-11. https://doi.org/10.1007/s10989-022-10428-8
  • 18. Ozkan, A.D., Betts, Z., Yuksel, B., Alimudin, J., Aydin, D. & Guzel, E. 2023. Assessing in vitro anticancer efficacy of sulfonated water-soluble phthalocyanine on breast and prostate cancer cells. Journal of Porphyrins and Phthalocyanines, 27(01n04), 493-500. https://doi.org/10.1142/S1088424623500256
  • 19. Permana, S., Sholihah, Z., Iskandar, A., Susanti, H. & Endharti, A.T. 2018. Cytotoxic effects and antiproliferative cancer activity of coelomic fluid from Lumbricus rubellus promotes apoptosis and reduces G2/M phase progression in HT-29 cells. Journal of Applied Pharmaceutical Science, 8(11): 028-034. https://doi.org/10.7324/JAPS.2018.81104
  • 20. Permana, S., Hadi, R.P., Norahmawati, E. & Endharti, A.T. 2019. Coelomic fluid of Lumbricus rubellus enhances the anti-prolioniferative effect of 5-fluorouracil by modulating focal adhesion kinase express and IL-1β of colorectal cancer in mice. Journal of Applied Pharmaceutical Science, 9(8):041-046 https://doi.org/10.7324/JAPS.2019.90806
  • 21. Permana, S., Putri Fityanti, R., Norahmawati, E., Iskandar, A,, Anggraini Mulyadi, E.D. &Tri Endharti, A. 2020. Coelomic Fluid of Eisenia fetida Ameliorates Cetuximab to Reduce K-Ras and Vimentin Expression through Promoting RUNX3 in an AOM/DSS-Induced Colitis Associated Colon Cancer. Evidence-Based Complementary and Alternative Medicine, 2020: 9418520. https://doi.org/10.1155/2020/9418520
  • 22. Rybicka, M., Czaplewska, P., Rzymowska, J., Sofińska-Chmiel, W., Wójcik-Mieszawska, S., Lewtak, K. & Fiołka, M.J. 2022. Novel Venetin-1 nanoparticle from earthworm coelomic fluid as a promising agent for the treatment of non-small cell lung cancer. Scientific Reports, 12(1): 1-21. https://doi.org/10.1038/s41598-022-21665-8
  • 23. Sadek, S.A., Sayed, M.G., Fahmy, S.R. & Soliman, A.M. 2022. A Coelomic Fluid of Allolobophora caliginosa as Novel Prospects for Medicinal Antioxidants, Anti-inflammatory, Antiproliferative, Analgesics, and Antipyretics. Biointerface Research. Appliend in Chemisrty. 13: 209. https://doi.org/10.33263/BRIAC133.209
  • 24. Shafi, F.A.A. & Faleh, N. 2019. Anticancer activity of earthworm powder (Lumbricus terrestris) against MCF-7 and PC-3 cancer cell lines. Journal of Gastrointestinal Cancer, 50(4): 919-925. https://doi.org/10.1007/s12029-019-00268-z
  • 25. Wahyuni, D. & Waluyo, J. 2018). Acute Toxicity of Earthworm (Pheretima Javanica K.) Powder on Renal Histopathological Description of Rat (Rattus norvegicus B.). Bioedukasi, 15: 1-6. https://doi.org/10.19184/bioedu.v15i2.6930
  • 26. Yuksel, B. & Deveci Ozkan, A. 2021. The Role of Citrus Nobiletin on Oxidative Stress Levels and Superoxide Dismutase Activities in Metastatic Castration-Resistant Prostate Cancer. Commagene Journal of Biology, 5(1): 84-89. https://doi.org/10.31594/commagene.895415
  • 27. Yuksel, B., Ozkan, A.D., Aydın, D. & Betts, Z. 2022. Evaluation of the antioxidative and genotoxic effects of sodium butyrate on breast cancer cells. Saudi Journal of Biological Sciences, 29(3): 1394-1401. https://doi.org/10.1016/j.sjbs.2021.12.061

Year 2024, Volume: 25 Issue: 1, 111 - 120, 15.04.2024

Burcu Yüksel Asuman Deveci Özkan

https://doi.org/10.23902/trkjnat.1373797

Abstract

Solucan özleri, kanseri durdurucu ve önleyici çeşitli maddeler içermesi nedeniyle kanser araştırmalarında ilgi çekici bir araştırma alanı haline gelmiştir. Ekstraktın kanser hücreleri üzerindeki antikanser etkisinin belirlenmesi, kemoterapötik ajanların toksik etkilerine karşı yeni tedavi stratejilerine ve alternatif tıp yöntemlerine ilgiyi artırabilir. Bu nedenle bu çalışma, solucan ekstraktlarının doğasını ve kullanıldıkları kanser türlerini sistematik bir inceleme yoluyla vurgulayarak ilaç geliştirme ve gelecekteki antikanser tedavileri için farkındalık yaratmayı amaçlamaktadır. Ocak 2018 ile Aralık 2022 arasında yayınlanan makaleleri belirlemek için CINAHL, PubMed, Medline, Scopus ve Web of Science veritabanlarında sistematik bir arama yapıldı. 'Solucan', 'solucan özü' ve 'antikanser etkisi' anahtar kelimelerinin çeşitli düzenlemelerinden yararlandık. Solucan ekstraktlarının kanser hücreleri üzerindeki in vitro ve in vivo sitotoksik etkisini gösteren İngilizce yazılmış orijinal çalışmaları incelemeye dahil ettik. Arama kriterlerimizle eşleşen 15 çalışma bulduk. Yapılan çalışmalar arasında en çok çalışılan solucan türü Eisenia foetida (Savigny) olurken, en sık çalışılan kanser türü ise kolon kanseri oldu. Koleomik Sıvının antikanser aktivitesini pozitif sonuçlarla test etmek için yaygın olarak kullanılan ekstrakt olduğu bulundu.

References

  • 1. Augustine, D., Rao, R.S., Jayaraman, A. & Murthy K.C. 2018. Antiproliferative activity of earthworm coelomic fluid using oral squamous carcinoma KB 3-1 cells: an in vitro study with serine protease analysis. Pharmacognosy Magazine, 14(59): 528. http://dx.doi.org/10.4103/pm.pm_412_18
  • 2. Augustine. D., Rao. R.S., Anbu, J. & Murthy, K.C. 2019. In vitro cytotoxic and apoptotic induction effect of earthworm coelomic fluid of Eudrilus eugeniae, Eisenia foetida, and Perionyx excavatus on human oral squamous cell carcinoma-9 cell line. Toxicology Reports, 6: 347-357. https://doi.org/10.1016/j.toxrep.2019.04.005
  • 3. Augustine, D., Rao, R.S., Gns, H.S., Anbu, J. & Saraswathy, G.R. 2022. Anticancer Potential of Eudrilus Eugeniae Coelomic Fluid Protein on SCC-9 Cells-In Vitro Gene Expression entwined with Cutting-Edge In-Silico Strategy, Research Square. https://doi.org/10.21203/rs.3.rs-439242/v1
  • 4. Chabner, B.A. & Roberts, T.G. 2005 Chemotherapy and the war on cancer. Nature Reviews Cancer, 5(1): 65-72. https://doi.org/10.1038/nrc1529
  • 5. Czerwonka, A., Fiołka, M.J., Jędrzejewska, K., Jankowska, E., Zając, A. & Rzeski, W. 2020. Pro-apoptotic action of protein-carbohydrate fraction isolated from coelomic fluid of the earthworm Dendrobaena veneta against human colon adenocarcinoma cells. Biomedicine & Pharmacotherapy, 126: 110035. https://doi.org/10.1016/j.biopha.2020.110035
  • 6. Deveci Özkan, A., Alimudin, J., Kilciler, Y., Yuksel, B., Aksoy, O. & Betts, Z. 2022. In vitro chemo-protective effect of Eisenia foetida coelomic fluid against histone deacetylase inhibitor-induced oxidative toxicity in breast cancer cells. International Journal of Environmental Health Research, 1-10. https://doi.org/10.1080/09603123.2022.2120970
  • 7. Endharti, A.T., Purnamasari, Y., Primasari, R., Poeranto, S. & Permana, S. 2019. The coelomic fluid of Lumbricus rubellus synergistically enhances the cytotoxic effect of 5-Fluorouracil through modulation of focal adhesion kinase and P21 in the HT-29 cancer cell line. The Scientific World Journal, 2019: 5632859. https://doi.org/10.1155/2019/5632859
  • 8. Fiołka, M.J. Rzymowska, J., Bilska, S., Lewtak, K., Dmoszyńska‐Graniczka, M., Grzywnowicz, K. & Urbanik‐Sypniewska, T. 2019. Antitumor activity and apoptotic action of coelomic fluid from the earthworm Dendrobaena veneta against A549 human lung cancer cells. Apmis, 127(6): 435-448. https://doi.org/10.1111/apm.12941
  • 9. Gupta, S. & Yadav, S. 2016. Immuno-Defense Strategy in Earthworms: A Review Article. International Journal of 10. Current Microbiology and Applied Sciences. 5: 1022-1035 http://dx.doi.org/10.20546/ijcmas.2016.504.117.
  • 11. Hanahan, D. 2022. Hallmarks of cancer: new dimensions. Cancer discovery, 12(1): 31-46. https://doi.org/10.1158/2159-8290.CD-21-1059
  • 12. Hussain, M., Liaqat, I., Ali, N.M., Arshad, N., Hanif, U., Sajjad, S., Sardar, A.A., Awan, U.F., Khan, F.S. & Slahuddin. 2023. Antibacterial and Bacteriostatic Potential of Coelomic Fluid and Body Paste of Pheretima Posthuma (Vaillant, 1868) (Clitellata, Megascolecidae) against Ampicillin Resistant Clinical Bacterial Isolates. Brazilian Journal of Biology, 2023: 83, http://doi.org/10.1590/1519-6984.247016
  • 13. Kruk, J., Aboul-Enein, H.Y., Kładna, A. & Bowser, J.E. 2019. Oxidative stress in biological systems and its relationship with pathophysiological functions: the effect of physical activity on cellular redox homeostasis. Free radical research, 53(5): 497-521. https://doi.org/10.1080/10715762.2019.1612059
  • 14. Małota, K., Urbisz, A. & Skonieczna, M. 2022. Dose-dependent proliferative and pro-oxidative effects of earthworm coelomic fluid on the HCT116 colon cancer cell line. Research Square, https://doi.org/10.21203/rs.3.rs-2258914/v1
  • 15. Mustafa, R.G., Saiqa, A., Domínguez, J., Jamil, M., Manzoor, S., Wazir, S., Shaheen, B., Parveen, A., Khan, R., Ali, S., Ali, N.M. & Jalal, F. 2022. Therapeutic Values of Earthworm Species Extract from Azad Kashmir as Anticoagulant, Antibacterial, and Antioxidant Agents. Canadian Journal of Infectious Diseases and Medical Microbiology, 2022: 1-20. http://doi.org/10.1155/2022/6949117.
  • 16. Ozkan, A.D. & Yuksel, B. 2022. POLY I: c-ınduced TLR3 activation on oxidative stress levels in PC-3 (hormone insensıtıve) and LNCAP (hormonesensıtıve) as prostate cancer cells. Journal of Health Sciences of Kocaeli University, 8: 18-24. http://doi.org/10.30934/kusbed.915511
  • 17. Ozkan, A.D., Eskiler, G.G., Sarihan, M., Kazan, N., Aksoy, O., Yuksel, B. & Betts, Z. 2022. Anticancer properties of Eisenia foetida proteins in prostate cancer cells in vitro. International Journal of Peptide Research and Therapeutics, 28(4): 1-11. https://doi.org/10.1007/s10989-022-10428-8
  • 18. Ozkan, A.D., Betts, Z., Yuksel, B., Alimudin, J., Aydin, D. & Guzel, E. 2023. Assessing in vitro anticancer efficacy of sulfonated water-soluble phthalocyanine on breast and prostate cancer cells. Journal of Porphyrins and Phthalocyanines, 27(01n04), 493-500. https://doi.org/10.1142/S1088424623500256
  • 19. Permana, S., Sholihah, Z., Iskandar, A., Susanti, H. & Endharti, A.T. 2018. Cytotoxic effects and antiproliferative cancer activity of coelomic fluid from Lumbricus rubellus promotes apoptosis and reduces G2/M phase progression in HT-29 cells. Journal of Applied Pharmaceutical Science, 8(11): 028-034. https://doi.org/10.7324/JAPS.2018.81104
  • 20. Permana, S., Hadi, R.P., Norahmawati, E. & Endharti, A.T. 2019. Coelomic fluid of Lumbricus rubellus enhances the anti-prolioniferative effect of 5-fluorouracil by modulating focal adhesion kinase express and IL-1β of colorectal cancer in mice. Journal of Applied Pharmaceutical Science, 9(8):041-046 https://doi.org/10.7324/JAPS.2019.90806
  • 21. Permana, S., Putri Fityanti, R., Norahmawati, E., Iskandar, A,, Anggraini Mulyadi, E.D. &Tri Endharti, A. 2020. Coelomic Fluid of Eisenia fetida Ameliorates Cetuximab to Reduce K-Ras and Vimentin Expression through Promoting RUNX3 in an AOM/DSS-Induced Colitis Associated Colon Cancer. Evidence-Based Complementary and Alternative Medicine, 2020: 9418520. https://doi.org/10.1155/2020/9418520
  • 22. Rybicka, M., Czaplewska, P., Rzymowska, J., Sofińska-Chmiel, W., Wójcik-Mieszawska, S., Lewtak, K. & Fiołka, M.J. 2022. Novel Venetin-1 nanoparticle from earthworm coelomic fluid as a promising agent for the treatment of non-small cell lung cancer. Scientific Reports, 12(1): 1-21. https://doi.org/10.1038/s41598-022-21665-8
  • 23. Sadek, S.A., Sayed, M.G., Fahmy, S.R. & Soliman, A.M. 2022. A Coelomic Fluid of Allolobophora caliginosa as Novel Prospects for Medicinal Antioxidants, Anti-inflammatory, Antiproliferative, Analgesics, and Antipyretics. Biointerface Research. Appliend in Chemisrty. 13: 209. https://doi.org/10.33263/BRIAC133.209
  • 24. Shafi, F.A.A. & Faleh, N. 2019. Anticancer activity of earthworm powder (Lumbricus terrestris) against MCF-7 and PC-3 cancer cell lines. Journal of Gastrointestinal Cancer, 50(4): 919-925. https://doi.org/10.1007/s12029-019-00268-z
  • 25. Wahyuni, D. & Waluyo, J. 2018). Acute Toxicity of Earthworm (Pheretima Javanica K.) Powder on Renal Histopathological Description of Rat (Rattus norvegicus B.). Bioedukasi, 15: 1-6. https://doi.org/10.19184/bioedu.v15i2.6930
  • 26. Yuksel, B. & Deveci Ozkan, A. 2021. The Role of Citrus Nobiletin on Oxidative Stress Levels and Superoxide Dismutase Activities in Metastatic Castration-Resistant Prostate Cancer. Commagene Journal of Biology, 5(1): 84-89. https://doi.org/10.31594/commagene.895415
  • 27. Yuksel, B., Ozkan, A.D., Aydın, D. & Betts, Z. 2022. Evaluation of the antioxidative and genotoxic effects of sodium butyrate on breast cancer cells. Saudi Journal of Biological Sciences, 29(3): 1394-1401. https://doi.org/10.1016/j.sjbs.2021.12.061
There are 26 citations in total.

Details

Primary Language English
Subjects Biochemistry and Cell Biology (Other)
Journal Section Systematic Reviews and Meta-Analysis
Authors

Burcu Yüksel 0000-0001-8691-6447

Asuman Deveci Özkan 0000-0002-3248-4279

Early Pub Date March 11, 2024
Publication Date April 15, 2024
Submission Date October 10, 2023
Acceptance Date January 17, 2024
Published in Issue Year 2024 Volume: 25 Issue: 1

Cite

APA Yüksel, B., & Deveci Özkan, A. (2024). A systematic review of antiproliferative and antitumour activity of earthworm extracts. Trakya University Journal of Natural Sciences, 25(1), 111-120. https://doi.org/10.23902/trkjnat.1373797
AMA Yüksel B, Deveci Özkan A. A systematic review of antiproliferative and antitumour activity of earthworm extracts. Trakya Univ J Nat Sci. April 2024;25(1):111-120. doi:10.23902/trkjnat.1373797
Chicago Yüksel, Burcu, and Asuman Deveci Özkan. “A Systematic Review of Antiproliferative and Antitumour Activity of Earthworm Extracts”. Trakya University Journal of Natural Sciences 25, no. 1 (April 2024): 111-20. https://doi.org/10.23902/trkjnat.1373797.
EndNote Yüksel B, Deveci Özkan A (April 1, 2024) A systematic review of antiproliferative and antitumour activity of earthworm extracts. Trakya University Journal of Natural Sciences 25 1 111–120.
IEEE B. Yüksel and A. Deveci Özkan, “A systematic review of antiproliferative and antitumour activity of earthworm extracts”, Trakya Univ J Nat Sci, vol. 25, no. 1, pp. 111–120, 2024, doi: 10.23902/trkjnat.1373797.
ISNAD Yüksel, Burcu - Deveci Özkan, Asuman. “A Systematic Review of Antiproliferative and Antitumour Activity of Earthworm Extracts”. Trakya University Journal of Natural Sciences 25/1 (April 2024), 111-120. https://doi.org/10.23902/trkjnat.1373797.
JAMA Yüksel B, Deveci Özkan A. A systematic review of antiproliferative and antitumour activity of earthworm extracts. Trakya Univ J Nat Sci. 2024;25:111–120.
MLA Yüksel, Burcu and Asuman Deveci Özkan. “A Systematic Review of Antiproliferative and Antitumour Activity of Earthworm Extracts”. Trakya University Journal of Natural Sciences, vol. 25, no. 1, 2024, pp. 111-20, doi:10.23902/trkjnat.1373797.
Vancouver Yüksel B, Deveci Özkan A. A systematic review of antiproliferative and antitumour activity of earthworm extracts. Trakya Univ J Nat Sci. 2024;25(1):111-20.

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