Retrospective study of small pet tumors treated with Artemisia annua and iron
- Authors:
- Mohamed E.M. Saeed
- Elmar Breuer
- Mohamed‑Elamir F. Hegazy
- Thomas Efferth
-
Affiliations: Department of Pharmaceutical Biology, Institute of Pharmacy and Biochemistry, Johannes Gutenberg University, Mainz, D‑55128 Rhineland‑Palatinate, Germany, Veterinary Clinic for Small Animals, ‘Alte Ziegelei’ Müllheim, D‑79379 Baden, Germany - Published online on: November 25, 2019 https://doi.org/10.3892/ijo.2019.4921
- Pages: 123-138
-
Copyright: © Saeed et al. This is an open access article distributed under the terms of Creative Commons Attribution License.
This article is mentioned in:
Abstract
Talmadge JE, Singh RK, Fidler IJ and Raz A: Murine models to evaluate novel and conventional therapeutic strategies for cancer. Am J Pathol. 170:793–804. 2007. View Article : Google Scholar : PubMed/NCBI | |
Jantscheff P, Beshay J, Lemarchand T, Obodozie C, Schächtele C and Weber H: Mouse-derived isograft (MDI) in vivo tumor models I Spontaneous sMDI models: Characterization and cancer therapeutic approaches. Cancers (Basel). 11:112019. View Article : Google Scholar | |
Choi JW, Yoon HY and Jeong SW: Clinical outcomes of surgically managed spontaneous tumors in 114 client-owned dogs. Immune Netw. 16:116–125. 2016. View Article : Google Scholar : PubMed/NCBI | |
Hellmén E, Bergström R, Holmberg L, Spångberg IB, Hansson K and Lindgren A: Prognostic factors in canine mammary tumors: A multivariate study of 202 consecutive cases. Vet Pathol. 30:20–27. 1993. View Article : Google Scholar : PubMed/NCBI | |
Marconato L: The staging and treatment of multicentric high-grade lymphoma in dogs: A review of recent developments and future prospects. Vet J. 188:34–38. 2011. View Article : Google Scholar | |
Tuohy JL, Selmic LE, Worley DR, Ehrhart NP and Withrow SJ: Outcome following curative-intent surgery for oral melanoma in dogs: 70 cases (1998-2011). J Am Vet Med Assoc. 245:1266–1273. 2014. View Article : Google Scholar : PubMed/NCBI | |
Miller RL, Van Lelyveld S, Warland J, Dobson JM and Foale RD: A retrospective review of treatment and response of high-risk mast cell tumours in dogs. Vet Comp Oncol. 14:361–370. 2016. View Article : Google Scholar | |
Romano FR, Heinze CR, Barber LG, Mason JB and Freeman LM: Association between body condition score and cancer prognosis in dogs with lymphoma and osteosarcoma. J Vet Intern Med. 30:1179–1186. 2016. View Article : Google Scholar : PubMed/NCBI | |
Sarowitz BN, Davis GJ and Kim S: Outcome and prognostic factors following curative-intent surgery for oral tumours in dogs: 234 cases (2004 to 2014). J Small Anim Pract. 58:146–153. 2017. View Article : Google Scholar : PubMed/NCBI | |
Ettinger SN: Principles of treatment for feline lymphoma. Clin Tech Small Anim Pract. 18:98–102. 2003. View Article : Google Scholar : PubMed/NCBI | |
Morris J: Mammary tumours in the cat: Size matters, so early intervention saves lives. J Feline Med Surg. 15:391–400. 2013. View Article : Google Scholar : PubMed/NCBI | |
Zabielska-Koczywąs K, Wojtalewicz A and Lechowski R: Current knowledge on feline injection-site sarcoma treatment. Acta Vet Scand. 59:472017. View Article : Google Scholar : | |
Martano M, Iussich S, Morello E and Buracco P: Canine oral fibrosarcoma: Changes in prognosis over the last 30 years? Vet J. 241:1–7. 2018. View Article : Google Scholar : PubMed/NCBI | |
Zhang D, Hedlund EM, Lim S, Chen F, Zhang Y, Sun B and Cao Y: Antiangiogenic agents significantly improve survival in tumor-bearing mice by increasing tolerance to chemotherapy-induced toxicity. Proc Natl Acad Sci USA. 108:4117–4122. 2011. View Article : Google Scholar : PubMed/NCBI | |
Tiwari A, Hadley JA, Hendricks GL III, Elkin RG, Cooper T and Ramachandran R: Characterization of ascites-derived ovarian tumor cells from spontaneously occurring ovarian tumors of the chicken: Evidence for E-cadherin upregulation. PLoS One. 8:e575822013. View Article : Google Scholar : PubMed/NCBI | |
Newman DJ and Cragg GM: Natural products as sources of new drugs from 1981 to 2014. J Nat Prod. 79:629–661. 2016. View Article : Google Scholar : PubMed/NCBI | |
Tu Y: The discovery of artemisinin (qinghaosu) and gifts from Chinese medicine. Nat Med. 17:1217–1220. 2011. View Article : Google Scholar : PubMed/NCBI | |
Bridgford JL, Xie SC, Cobbold SA, Pasaje CFA, Herrmann S, Yang T, Gillett DL, Dick LR, Ralph SA, Dogovski C, et al: Artemisinin kills malaria parasites by damaging proteins and inhibiting the proteasome. Nat Commun. 9:38012018. View Article : Google Scholar : PubMed/NCBI | |
Su XZ and Miller LH: The discovery of artemisinin and the Nobel Prize in Physiology or Medicine. Sci China Life Sci. 58:1175–1179. 2015. View Article : Google Scholar : PubMed/NCBI | |
Tu Y: Artemisinin-a gift from traditional chinese medicine to the world (Nobel Lecture). Angew Chem Int Ed Engl. 55:10210–10226. 2016. View Article : Google Scholar : PubMed/NCBI | |
Daddy NB, Kalisya LM, Bagire PG, Watt RL, Towler MJ and Weathers PJ: Artemisia annua dried leaf tablets treated malaria resistant to ACT and i.v. artesunate: Case reports. Phytomedicine. 32:37–40. 2017. View Article : Google Scholar : PubMed/NCBI | |
Saeed ME, Krishna S, Greten HJ, Kremsner PG and Efferth T: Antischistosomal activity of artemisinin derivatives in vivo and in patients. Pharmacol Res. 110:216–226. 2016. View Article : Google Scholar : PubMed/NCBI | |
Pérez del Villar L, Burguillo FJ, López-Abán J and Muro A: Systematic review and meta-analysis of artemisinin based therapies for the treatment and prevention of schistosomiasis. PLoS One. 7:e458672012. View Article : Google Scholar : PubMed/NCBI | |
Naß J and Efferth T: The activity of Artemisia spp. and their constituents against Trypanosomiasis. Phytomedicine. 47:184–191. 2018. View Article : Google Scholar | |
Efferth T: Beyond malaria: The inhibition of viruses by arte-misinin-type compounds. Biotechnol Adv. 36:1730–1737. 2018. View Article : Google Scholar : PubMed/NCBI | |
Jiang W, Cen Y, Song Y, Li P, Qin R, Liu C, Zhao Y, Zheng J and Zhou H: Artesunate attenuated progression of atherosclerosis lesion formation alone or combined with rosuvastatin through inhibition of pro-inflammatory cytokines and pro-inflammatory chemokines. Phytomedicine. 23:1259–1266. 2016. View Article : Google Scholar : PubMed/NCBI | |
Li J, Casteels T, Frogne T, Ingvorsen C, Honore C, Courtney M, Huber KV, Schmitner N, Kimmel RA, Romanov RA, et al: Artemisinins target GABAA receptor signaling and impair alpha cell Identity. Cell. 168:86–100.e15. 2017. View Article : Google Scholar | |
Guo Y, Fu W, Xin Y, Bai J, Peng H, Fu L, Liu J, Li L, Ma Y and Jiang H: Antidiabetic and antiobesity effects of artemether in db/db mice. BioMed Res Int. 2018:86395232018. View Article : Google Scholar : PubMed/NCBI | |
Efferth T, Dunstan H, Sauerbrey A, Miyachi H and Chitambar CR: The anti-malarial artesunate is also active against cancer. Int J Oncol. 18:767–773. 2001.PubMed/NCBI | |
Efferth T, Sauerbrey A, Olbrich A, Gebhart E, Rauch P, Weber HO, Hengstler JG, Halatsch ME, Volm M, Tew KD, et al: Molecular modes of action of artesunate in tumor cell lines. Mol Pharmacol. 64:382–394. 2003. View Article : Google Scholar : PubMed/NCBI | |
Dell'Eva R, Pfeffer U, Vené R, Anfosso L, Forlani A, Albini A and Efferth T: Inhibition of angiogenesis in vivo and growth of Kaposi's sarcoma xenograft tumors by the anti-malarial arte-sunate. Biochem Pharmacol. 68:2359–2366. 2004. View Article : Google Scholar : PubMed/NCBI | |
Efferth T: From ancient herb to modern drug: Artemisia annua and artemisinin for cancer therapy. Semin Cancer Biol. 46:65–83. 2017. View Article : Google Scholar : PubMed/NCBI | |
Abba ML, Patil N, Leupold JH, Saeed ME, Efferth T and Allgayer H: Prevention of carcinogenesis and metastasis by Artemisinin-type drugs. Cancer Lett. 429:11–18. 2018. View Article : Google Scholar : PubMed/NCBI | |
Krusche B, Arend J and Efferth T: Synergistic inhibition of angiogenesis by artesunate and captopril in vitro and in vivo. Evid Based Complement Alternat Med. 2013:4547832013. View Article : Google Scholar : PubMed/NCBI | |
Efferth T: Cancer combination therapy of the sesquiterpenoid artesunate and the selective EGFR-tyrosine kinase inhibitor erlotinib. Phytomedicine. 37:58–61. 2017. View Article : Google Scholar : PubMed/NCBI | |
Efferth T: Cancer combination therapies with artemisinin-type drugs. Biochem Pharmacol. 139:56–70. 2017. View Article : Google Scholar : PubMed/NCBI | |
Hosoya K, Murahari S, Laio A, London CA, Couto CG and Kisseberth WC: Biological activity of dihydroartemisinin in canine osteosarcoma cell lines. Am J Vet Res. 69:519–526. 2008. View Article : Google Scholar : PubMed/NCBI | |
Hosoya K, Couto CG, London CA, Kisseberth WC, Phelps MA and Dalton JT: Comparison of high-dose intermittent and low-dose continuous oral artemisinin in dogs with naturally occurring tumors. J Am Anim Hosp Assoc. 50:390–395. 2014. View Article : Google Scholar : PubMed/NCBI | |
Rutteman GR, Erich SA, Mol JA, Spee B, Grinwis GC, Fleckenstein L, London CA and Efferth T: Safety and efficacy field study of artesunate for dogs with non-resectable tumours. Anticancer Res. 33:1819–1827. 2013.PubMed/NCBI | |
Berger TG, Dieckmann D, Efferth T, Schultz ES, Funk JO, Baur A and Schuler G: Artesunate in the treatment of metastatic uveal melanoma - first experiences. Oncol Rep. 14:1599–1603. 2005.PubMed/NCBI | |
Michaelsen FW, Saeed ME, Schwarzkopf J and Efferth T: Activity of Artemisia annua and artemisinin derivatives, in prostate carcinoma. Phytomedicine. 22:1223–1231. 2015. View Article : Google Scholar : PubMed/NCBI | |
Jansen FH, Adoubi I, JC KC, DE Cnodder T, Jansen N, Tschulakow A and Efferth T: First study of oral Artenimol-R in advanced cervical cancer: Clinical benefit, tolerability and tumor markers. Anticancer Res. 31:4417–4422. 2011.PubMed/NCBI | |
Krishna S, Ganapathi S, Ster IC, Saeed ME, Cowan M, Finlayson C, Kovacsevics H, Jansen H, Kremsner PG, Efferth T, et al: A randomised, double blind, placebo-controlled pilot study of oral artesunate therapy for colorectal cancer. EBioMedicine. 2:82–90. 2014. View Article : Google Scholar | |
von Hagens C, Walter-Sack I, Goeckenjan M, Osburg J, Storch-Hagenlocher B, Sertel S, Elsässer M, Remppis BA, Edler L, Munzinger J, et al: Prospective open uncontrolled phase I study to define a well-tolerated dose of oral artesunate as add-on therapy in patients with metastatic breast cancer (ARTIC M33/2). Breast Cancer Res Treat. 164:359–369. 2017. View Article : Google Scholar : PubMed/NCBI | |
Breuer E and Efferth T: Treatment of iron-loaded veterinary sarcoma by Artemisia annua. Nat Prod Bioprospect. 4:113–118. 2014. View Article : Google Scholar : PubMed/NCBI | |
Hegazy MF, Abdelfatah S, Hamed AR, Mohamed TA, Elshamy AA, Saleh IA, Reda EH, Abdel-Azim NS, Shams KA, Sakr M, et al: Cytotoxicity of 40 Egyptian plant extracts targeting mechanisms of drug-resistant cancer cells. Phytomedicine. 59:1527712019. View Article : Google Scholar : PubMed/NCBI | |
Chikazawa S, Hori Y, Kanai K, Ito N, Hoshi F, Orino K, Watanabe K and Higuchi S: Factors influencing measurement of serum iron concentration in dogs: Diurnal variation and hyper-ferritinemia. J Vet Med Sci. 75:1615–1618. 2013. View Article : Google Scholar : PubMed/NCBI | |
Carpenter CE and Ward RE: Iron determination by Ferrozine method. Food Analysis Laboratory Manual Springer: Luxembourg: pp. 157–159. 2017, View Article : Google Scholar | |
Stoica G, Lungu G, Martini-Stoica H, Waghela S, Levine J and Smith R III: Identification of cancer stem cells in dog glioblastoma. Vet Pathol. 46:391–406. 2009. View Article : Google Scholar : PubMed/NCBI | |
Wellman ML, Krakowka S, Jacobs RM and Kociba GJ: A macrophage-monocyte cell line from a dog with malignant histiocytosis. In Vitro Cell Dev Biol. 24:223–229. 1988. View Article : Google Scholar : PubMed/NCBI | |
Alley MC, Scudiero DA, Monks A, Hursey ML, Czerwinski MJ, Fine DL, Abbott BJ, Mayo JG, Shoemaker RH and Boyd MR: Feasibility of drug screening with panels of human tumor cell lines using a microculture tetrazolium assay. Cancer Res. 48:589–601. 1988.PubMed/NCBI | |
Rubinstein LV, Shoemaker RH, Paull KD, Simon RM, Tosini S, Skehan P, Scudiero DA, Monks A and Boyd MR: Comparison of in vitro anticancer-drug-screening data generated with a tetra-zolium assay versus a protein assay against a diverse panel of human tumor cell lines. J Natl Cancer Inst. 82:1113–1118. 1990. View Article : Google Scholar : PubMed/NCBI | |
Kuete V, Mbaveng AT, Sandjo LP, Zeino M and Efferth T: Cytotoxicity and mode of action of a naturally occurring naphthoquinone, 2-acetyl-7-methoxynaphtho[2,3-b]furan-4,9-quinone towards multi-factorial drug-resistant cancer cells. Phytomedicine. 33:62–68. 2017. View Article : Google Scholar : PubMed/NCBI | |
O'Brien J, Wilson I, Orton T and Pognan F: Investigation of the Alamar Blue (resazurin) fluorescent dye for the assessment of mammalian cell cytotoxicity. Eur J Biochem. 267:5421–5426. 2000. View Article : Google Scholar : PubMed/NCBI | |
Saeed ME, Mertens R, Handgretinger R and Efferth T: Identification of fatal outcome in a childhood nasopharyngeal carcinoma patient by protein expression profiling. Int J Oncol. 53:1721–1731. 2018.PubMed/NCBI | |
Blaskó G, Cordell GA and Lankin DC: Definitive 1H-and 13C-NMR assignments of artemisinin (Qinghaosu). J Nat Prod. 51:1273–1276. 1988. View Article : Google Scholar | |
Haynes RK, Cheu KW, N'Da D, Coghi P and Monti D: Considerations on the mechanism of action of artemisinin anti-malarials: Part 1 - the 'carbon radical' and 'heme' hypotheses. Infect Disord Drug Targets. 13:217–277. 2013. View Article : Google Scholar : PubMed/NCBI | |
Klonis N, Creek DJ and Tilley L: Iron and heme metabolism in Plasmodium falciparum and the mechanism of action of arte-misinins. Curr Opin Microbiol. 16:722–727. 2013. View Article : Google Scholar : PubMed/NCBI | |
Efferth T, Benakis A, Romero MR, Tomicic M, Rauh R, Steinbach D, Häfer R, Stamminger T, Oesch F, Kaina B, et al: Enhancement of cytotoxicity of artemisinins toward cancer cells by ferrous iron. Free Radic Biol Med. 37:998–1009. 2004. View Article : Google Scholar : PubMed/NCBI | |
Kelter G, Steinbach D, Konkimalla VB, Tahara T, Taketani S, Fiebig HH and Efferth T: Role of transferrin receptor and the ABC transporters ABCB6 and ABCB7 for resistance and differentiation of tumor cells towards artesunate. PLoS One. 2:e7982007. View Article : Google Scholar : PubMed/NCBI | |
Aulbert E, Disselhoff W, Sörje H, Schulz E and Gericke D: Lysosomal accumulation of 67Ga - transferrin in malignant tumors in relation to their growth rate. Eur J Cancer. 16:1217–1232. 1980. View Article : Google Scholar : PubMed/NCBI | |
Sadava D, Phillips T, Lin C and Kane SE: Transferrin overcomes drug resistance to artemisinin in human small-cell lung carcinoma cells. Cancer Lett. 179:151–156. 2002. View Article : Google Scholar : PubMed/NCBI | |
Zhao F, Wang H, Kunda P, Chen X, Liu QL and Liu T: Artesunate exerts specific cytotoxicity in retinoblastoma cells via CD71. Oncol Rep. 30:1473–1482. 2013. View Article : Google Scholar : PubMed/NCBI | |
Wang Q, Wu S, Zhao X, Zhao C, Zhao H and Huo L: Mechanisms of dihydroartemisinin and dihydroartemisinin/holotransferrin cytotoxicity in t-cell lymphoma cells. PLoS One. 10:e01373312015. View Article : Google Scholar : PubMed/NCBI | |
Judd W, Poodry CA and Strominger JL: Novel surface antigen expressed on dividing cells but absent from nondividing cells. J Exp Med. 152:1430–1435. 1980. View Article : Google Scholar : PubMed/NCBI | |
Sutherland R, Delia D, Schneider C, Newman R, Kemshead J and Greaves M: Ubiquitous cell-surface glycoprotein on tumor cells is proliferation-associated receptor for transferrin. Proc Natl Acad Sci USA. 78:4515–4519. 1981. View Article : Google Scholar : PubMed/NCBI | |
Trowbridge IS and Omary MB: Human cell surface glycoprotein related to cell proliferation is the receptor for transferrin. Proc Natl Acad Sci USA. 78:3039–3043. 1981. View Article : Google Scholar : PubMed/NCBI | |
Gatter KC, Brown G, Trowbridge IS, Woolston RE and Mason DY: Transferrin receptors in human tissues: Their distribution and possible clinical relevance. J Clin Pathol. 36:539–545. 1983. View Article : Google Scholar : PubMed/NCBI | |
Tortorella S and Karagiannis TC: Transferrin receptor-mediated endocytosis: A useful target for cancer therapy. J Membr Biol. 247:291–307. 2014. View Article : Google Scholar : PubMed/NCBI | |
Luria-Pérez R, Helguera G and Rodríguez JA: Antibody-mediated targeting of the transferrin receptor in cancer cells. Bol Méd Hosp Infant México. 73:372–379. 2016. | |
Akbari B, Farajnia S, Ahdi Khosroshahi S, Safari F, Yousefi M, Dariushnejad H and Rahbarnia L: Immunotoxins in cancer therapy: Review and update. Int Rev Immunol. 36:207–219. 2017. View Article : Google Scholar : PubMed/NCBI | |
Lai H, Sasaki T, Singh NP and Messay A: Effects of arte-misinin-tagged holotransferrin on cancer cells. Life Sci. 76:1267–1279. 2005. View Article : Google Scholar : PubMed/NCBI | |
Nakase I, Gallis B, Takatani-Nakase T, Oh S, Lacoste E, Singh NP, Goodlett DR, Tanaka S, Futaki S, Lai H, et al: Transferrin receptor-dependent cytotoxicity of artemisinin-transferrin conjugates on prostate cancer cells and induction of apoptosis. Cancer Lett. 274:290–298. 2009. View Article : Google Scholar | |
Gong Y, Gallis BM, Goodlett DR, Yang Y, Lu H, Lacoste E, Lai H and Sasaki T: Effects of transferrin conjugates of artemisinin and artemisinin dimer on breast cancer cell lines. Anticancer Res. 33:123–132. 2013. | |
Zhong YR: Chemical constituents of volatile oils of Artemisia annua. Zhong Yao Tong Bao. 8:31–32. 1983.In Chinese. PubMed/NCBI | |
Liao HW, Wang DY and Li XM: Studies on the chemical constituents of essential oil of Hunan Artemisia annua. Zhong Yao Cai. 29:562–564. 2006.In Chinese. PubMed/NCBI | |
Efferth T, Herrmann F, Tahrani A and Wink M: Cytotoxic activity of secondary metabolites derived from Artemisia annua L. towards cancer cells in comparison to its designated active constituent artemisinin. Phytomedicine. 18:959–969. 2011. View Article : Google Scholar : PubMed/NCBI | |
Zhang X, Zhao Y, Guo L, Qiu Z, Huang L and Qu X: Differences in chemical constituents of Artemisia annua L. from different geographical regions in China. PLoS One. 12:e01830472017. View Article : Google Scholar | |
Efferth T, Konkimalla VB, Wang YF, Sauerbrey A, Meinhardt S, Zintl F, Mattern J and Volm M: Prediction of broad spectrum resistance of tumors towards anticancer drugs. Clin Cancer Res. 14:2405–2412. 2008. View Article : Google Scholar : PubMed/NCBI | |
Volm M and Efferth T: Prediction of cancer drug resistance and implications for personalized medicine. Front Oncol. 5:2822015. View Article : Google Scholar | |
Duffy MJ, Harbeck N, Nap M, Molina R, Nicolini A, Senkus E and Cardoso F: Clinical use of biomarkers in breast cancer: Updated guidelines from the European Group on Tumor Markers (EGTM). Eur J Cancer. 75:284–298. 2017. View Article : Google Scholar : PubMed/NCBI | |
Sun X and Kaufman PD: Ki-67: More than a proliferation marker. Chromosoma. 127:175–186. 2018. View Article : Google Scholar : PubMed/NCBI | |
Scott CS, Ramsden W, Limbert HJ, Master PS and Roberts BE: Membrane transferrin receptor (TfR) and nuclear proliferation-associated Ki-67 expression in hemopoietic malignancies. Leukemia. 2:438–442. 1988.PubMed/NCBI | |
Soyer HP, Smolle J, Smolle-Juettner FM and Kerl H: Proliferation antigens in cutaneous melanocytic tumors - an immunohisto-chemical study comparing the transferrin receptor and the Ki-67 antigen. Dermatologica. 179:3–9. 1989. View Article : Google Scholar | |
Wrba F, Chott A, Reiner A, Reiner G, Markis-Ritzinger E and Holzner JH: Ki-67 immunoreactivity in breast carcinomas in relation to transferrin receptor expression, estrogen receptor status and morphological criteria. An immunohistochemical study. Oncology. 46:255–259. 1989. View Article : Google Scholar : PubMed/NCBI | |
Prior R, Reifenberger G and Wechsler W: Transferrin receptor expression in tumours of the human nervous system: Relation to tumour type, grading and tumour growth fraction. Virchows Arch A Pathol Anat Histopathol. 416:491–496. 1990. View Article : Google Scholar : PubMed/NCBI | |
Kearsley JH, Furlong KL, Cooke RA and Waters MJ: An immuno-histochemical assessment of cellular proliferation markers in head and neck squamous cell cancers. Br J Cancer. 61:821–827. 1990. View Article : Google Scholar : PubMed/NCBI | |
Chan KT, Choi MY, Lai KK, Tan W, Tung LN, Lam HY, Tong DK, Lee NP and Law S: Overexpression of transferrin receptor CD71 and its tumorigenic properties in esophageal squamous cell carcinoma. Oncol Rep. 31:1296–1304. 2014. View Article : Google Scholar : PubMed/NCBI | |
Motamedi M, Xu L and Elahi S: Correlation of transferrin receptor (CD71) with Ki67 expression on stimulated human and mouse T cells: The kinetics of expression of T cell activation markers. J Immunol Methods. 437:43–52. 2016. View Article : Google Scholar : PubMed/NCBI | |
Darb-Esfahani S, Kolaschinski I, Trillsch F, Mahner S, Concin N, Vergote I, Van Nieuwenhuysen E, Achimas-Cadariu P, Glajzer J, Woopen H, et al: Morphology and tumour-infiltrating lymphocytes in high-stage, high-grade serous ovarian carcinoma correlated with long-term survival. Histopathology. 73:1002–1012. 2018. View Article : Google Scholar : PubMed/NCBI | |
Lee JS, Won HS, Sun S, Hong JH and Ko YH: Prognostic role of tumor-infiltrating lymphocytes in gastric cancer: A systematic review and meta-analysis. Medicine (Baltimore). 97:e117692018. View Article : Google Scholar | |
Shen M, Wang J and Ren X: New insights into tumor-infiltrating B lymphocytes in breast cancer: Clinical impacts and regulatory mechanisms. Front Immunol. 9:4702018. View Article : Google Scholar : PubMed/NCBI | |
Uhl M, Schwab S and Efferth T: Fatal liver and bone marrow toxicity by combination treatment of dichloroacetate and arte-sunate in a glioblastoma multiforme patient: Case report and review of the literature. Front Oncol. 6:2042016. View Article : Google Scholar | |
Efferth T, Schöttler U, Krishna S, Schmiedek P, Wenz F and Giordano FA: Answer to the comment of Hai Lu et al. regarding 'Hepatotoxicity by combination treatment of temozolomide, artesunate and Chinese herbs in a glioblastoma multiforme patient: Case report and review of the literature. Arch Toxicol (2016). Arch Toxicol. 91:2491–2492. 2017. View Article : Google Scholar : PubMed/NCBI | |
Eigbibhalu UG, Albert Taiwo EO, Douglass IA and Abimbola EA: Effect of selected anti-malarial drugs on the blood chemistry and brain serotonin levels in male rabbits. Pak J Pharm Sci. 26:125–129. 2013. | |
Zhu CY, Xu QH, Mao ZY and Lin N: Application of three arte-misinin derivatives in neuropathic pain: Evaluating co-curation of nociceptive and emotional syndromes in spinal cord ligation mice. Zhongguo Zhong Yao Za Zhi. 43:3058–3063. 2018.In Chinese. PubMed/NCBI | |
Amos S, Chindo BA, Abbah J, Vongtau HO, Edmond I, Binda L, Akah PA, Wambebe C and Gamaniel KS: Postsynaptic dopamine (D(2))-mediated behavioural effects of high acute doses of arte-misinin in rodents. Brain Res Bull. 62:255–260. 2003. View Article : Google Scholar : PubMed/NCBI |