The DOI matches its Crossref record; 65 of the 65 references it cites were found in a registry or an index.
Dried whole-plant Artemisia annua slows evolution of malaria drug resistance and overcomes resistance to artemisinin
Open accessAbstract
Significance: Evolution of malaria parasite drug resistance has thwarted efforts to control this deadly disease. Use of drug combinations has been proposed to slow that evolution. Artemisinin is a favorite drug in the global war on malaria and is frequently used in combination therapies. Here we show that using the whole plant ( Artemisia annua ) from which artemisinin is derived can overcome parasite resistance and is actually more resilient to evolution of parasite resistance; i.e., parasites take longer to evolve resistance, thus increasing the effective life span of the therapy.
Overview
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
The source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
In the citing paper
“Another reason for increasing the in planta artemisinin content is that dry leaf consumption of A. annua is showing efficacy in human trials (Daddy et al. 2017; Munyangi et al. 2019) and seems resilient against the evolution of artemisinin drug resistance as maybe shown in humans (Daddy et al. 2017) and in Plasmodium yoelii -infected mice (Elfawal et al. 2015).”
From Enhancing artemisinin content in and delivery from Artemisia annua: a review of alternative, classical, and transgenic approaches (2021) · cites this paper as Elfawal et al. 2015
Experimental — accuracy not yet measured
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Citations
Cites
R: A Language and Environment for Statistical Computing
R Core Team (2000) · doi:10.32614/r.manuals · Cited by 355,893
Linear Mixed-Effects Models using 'Eigen' and S4
Bates, D. M., Maechler, M., Bolker, B. M., & Walker, S. C. (2015) · Cited by 5,924
Biochemistry and molecular biology of plants
Short, T. W. (2001) · Biochemistry and Molecular Biology Education · Cited by 3,833
Artemisinin Resistance in Plasmodium falciparum Malaria
Dondorp, A. M., Nosten, F., Yi, P., Das, D., Phyo, A. P., Tarning, J., Lwin, K. M., Ariey, F., Hanpithakpong, W., Lee, S. J., et al. (2009) · New England Journal of Medicine · doi:10.1056/nejmoa0808859 · Cited by 3,424
Isoprenoid biosynthesis: The evolution of two ancient and distinct pathways across genomes
Lange, B. M., Rujan, T., Martin, W., & Croteau, R. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.240454797 · Cited by 881
Rasoanaivo, P., Wright, C. W., Willcox, M. L., & Gilbert, B. (2011) · Malaria Journal · doi:10.1186/1475-2875-10-s1-s4 · Cited by 566
Ferreira, J., Luthria, D. L., Sasaki, T., & Heyerick, A. (2010) · Molecules · doi:10.3390/molecules15053135 · Cited by 532
Jambou, R., Legrand, E., Niang, M., Khim, N., Lim, P., Volney, B., Ekala, M. T., Bouchier, C., Esterre, P., Fandeur, T., et al. (2005) · Yearbook of Dermatology and Dermatologic Surgery · doi:10.1016/s0093-3619(08)70110-2 · Cited by 511
Yeh, E., & DeRisi, J. L. (2011) · PLoS Biology · doi:10.1371/journal.pbio.1001138 · Cited by 508
White, N. J. (1996) · New England Journal of Medicine · doi:10.1056/nejm199609123351107 · Cited by 494
Evidence for the shikimate pathway in apicomplexan parasites
Roberts, F., Roberts, C., Johnson, J. J., Kyle, D., Krell, T., Coggins, J., Coombs, G., Milhous, W., Tzipori, S., Ferguson, D., et al. (1998) · Nature · doi:10.1038/31723 · Cited by 469
The ecosystem and evolutionary contexts of allelopathy
Inderjit, I., Wardle, D. A., Karban, R., & Callaway, R. M. (2011) · Trends in Ecology & Evolution · doi:10.1016/j.tree.2011.08.003 · Cited by 407
A Major Genome Region Underlying Artemisinin Resistance in Malaria
Cheeseman, I. H., Miller, B. A., Nair, S., Nkhoma, S. C., Tan, A., Tan, J. C., Saai, S. A., Phyo, A. P., Moo, C. L., Lwin, K. M., et al. (2012) · Science · doi:10.1126/science.1215966 · Cited by 379
The biosynthesis of C5–C25 terpenoid compounds
Dewick, P. M. (2002) · Natural Product Reports · doi:10.1039/b002685i · Cited by 371
The Biosynthesis of Artemisinin (Qinghaosu) and the Phytochemistry of Artemisia annua L. (Qinghao)
Brown, G. D. (2010) · Molecules · doi:10.3390/molecules15117603 · Cited by 363
The evolution, metabolism and functions of the apicoplast
Lim, L., & McFadden, G. I. (2010) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2009.0273 · Cited by 356
Drug‐resistant malaria: Molecular mechanisms and implications for public health
Petersen, I., Eastman, R. T., & Lanzer, M. (2011) · FEBS Letters · doi:10.1016/j.febslet.2011.04.042 · Cited by 288
The evolution of secondary metabolism – a unifying model
Firn, R. D., & Jones, C. G. (2000) · Molecular Microbiology · doi:10.1046/j.1365-2958.2000.02098.x · Cited by 230
Sen, R., Bandyopadhyay, S., Dutta, A., Mandal, G., Ganguly, S., Saha, P., & Chatterjee, M. (2007) · Journal of Medical Microbiology · doi:10.1099/jmm.0.47364-0 · Cited by 230
Svensson, & Ashton (1999) · British Journal of Clinical Pharmacology · doi:10.1046/j.1365-2125.1999.00044.x · Cited by 207
Weathers, P. J., Arsenault, P. R., Covello, P. S., McMickle, A., Teoh, K. H., & Reed, D. W. (2010) · Phytochemistry Reviews · doi:10.1007/s11101-010-9166-0 · Cited by 202
Self-citationAlker, A. P., Lim, P., Sem, R., Shah, N. K., Yi, P., Bouth, D. M., Tsuyuoka, R., Maguire, J. D., Fandeur, T., Ariey, F., et al. (2007) · American Journal of Tropical Medicine and Hygiene · doi:10.4269/ajtmh.2007.76.641 · Cited by 196
The chemotherapy of rodent malaria
Peters, W., Robinson, B. L., Mutambu, S. L., Warhurst, D. C., Ellis, D. S., & Tovey, D. G. (1989) · Annals of Tropical Medicine and Parasitology · doi:10.1080/00034983.1989.11812304 · Cited by 193
The Biological Activities of 20 Nature Identical Essential Oil Constituents
van Zyl, R. L., Seatlholo, S. T., van Vuuren, S. F., & Viljoen, A. M. (2006) · Journal of Essential Oil Research · doi:10.1080/10412905.2006.12067134 · Cited by 190
Antimalarial activity of Artemisia annua flavonoids from whole plants and cell cultures
Liu, K. C.-S., Yang, S., ROBERTS, M. F., Elford, B. C., & Phillipson, J. D. (1992) · Plant Cell Reports · doi:10.1007/bf00236389 · Cited by 189
Repellency and Toxicity of Oil from Artemisia annua to Certain Stored-Product Beetles
Tripathi, A. K., Prajapati, V., Aggarwal, K. K., Khanuja, S. P. S., & Kumar, S. (2000) · Journal of Economic Entomology · doi:10.1603/0022-0493-93.1.43 · Cited by 187
Artemisinin, a Constituent of Annual Wormwood (Artemisia annua), is a Selective Phytotoxin
Duke, S. O., Vaughn, K. C., Croom, E. M., & ElSohly, H. N. (1987) · Weed Science · doi:10.1017/s0043174500060458 · Cited by 186
Common dietary flavonoids inhibit the growth of the intraerythrocytic malaria parasite
Lehane, A. M., & Saliba, K. J. (2008) · BMC Research Notes · doi:10.1186/1756-0500-1-26 · Cited by 175
Shekari, M., Sendi, J. J., Etebari, K., Zibaee, A., & Shadparvar, A. A. (2008) · Pesticide Biochemistry and Physiology · doi:10.1016/j.pestbp.2008.01.003 · Cited by 167
Terpenes Arrest Parasite Development and Inhibit Biosynthesis of Isoprenoids inPlasmodium falciparum
Goulart, H. R., Kimura, E. A., Peres, V. J., Couto, A. S., Duarte, F. A. A., & Katzin, A. M. (2004) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.48.7.2502-2509.2004 · Cited by 165
Herbal Drugs: Ethnomedicine to Modern Medicine
Ramawat, K. G. (2008) · Springer eBooks · doi:10.1007/978-3-540-79116-4 · Cited by 164
Denis, M. B., Tsuyuoka, R., Yi, P., Narann, T. S., Suon, S., Lim, C., Incardona, S., Lim, P., Sem, R., Socheat, D., et al. (2006) · Tropical Medicine & International Health · doi:10.1111/j.1365-3156.2006.01690.x · Cited by 138
Artemisinins Inhibit Trypanosoma cruzi and Trypanosoma brucei rhodesiense In Vitro Growth
Mishina, Y. V., Krishna, S., Haynes, R. K., & Meade, J. C. (2007) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.01544-06 · Cited by 136
Dried Whole Plant Artemisia annua as an Antimalarial Therapy
Elfawal, M. A., Towler, M. J., Reich, N. G., Golenbock, D. T., Weathers, P. J., & Rich, S. M. (2012) · PLoS ONE · doi:10.1371/journal.pone.0052746 · Cited by 134
Self-citationLopes, N. P., Kato, M. J., Andrade, E. H. D. A., Maia, J. G. S., Yoshida, M., Planchart, A. R., & Katzin, A. M. (1999) · Journal of Ethnopharmacology · doi:10.1016/s0378-8741(99)00072-0 · Cited by 124
Artemisia Species: From Traditional Medicines to Modern Antimalarials—and Back Again
Willcox, M. L. (2009) · The Journal of Alternative and Complementary Medicine · doi:10.1089/acm.2008.0327 · Cited by 121
Ferreira, J., Peaden, P. A., & Keiser, J. (2011) · Parasitology Research · doi:10.1007/s00436-011-2418-0 · Cited by 106
Avery, M. A., Muraleedharan, K. M., Desai, P. V., Bandyopadhyaya, A. K., Furtado, M. M., & Tekwani, B. L. (2003) · Journal of Medicinal Chemistry · doi:10.1021/jm030181q · Cited by 103
Suberu, J., Gorka, A. P., Jacobs, L., Roepe, P. D., Sullivan, N., Barker, G. C., & Lapkin, A. A. (2013) · PLoS ONE · doi:10.1371/journal.pone.0080790 · Cited by 97
Deepa, G., Fuehrer, H., Starzengrüber, P., Swoboda, P., Khan, W. A., Reismann, J. A. B., Mueller, M. S. K., Chiba, P., & Noedl, H. (2012) · Parasitology Research · doi:10.1007/s00436-011-2763-z · Cited by 95
Allelopathic activity of annual wormwood (Artemisia annua) and the role of artemisinin
Lydon, J., Teasdale, J. R., & Chen, P. K. (1997) · Weed Science · doi:10.1017/s0043174500089001 · Cited by 91
Characterization of the isoprenoid chain of coenzyme Q in Plasmodium falciparum
de Macedo, C. S., Uhrig, M. L., Kimura, E. A., & Katzin, A. M. (2002) · FEMS Microbiology Letters · doi:10.1111/j.1574-6968.2002.tb11021.x · Cited by 88
Antimalarial Chemotherapy: Mechanisms of Action, Resistance and New Directions in Drug Discovery
Croft, S. L. (2001) · Drug Discovery Today · doi:10.1016/s1359-6446(01)02035-9 · Cited by 82
Utzinger, J., Shuhua, X., Keiser, J., Minggan, C., Jiang, Z., & Tanner, M. (2001) · Current Medicinal Chemistry · doi:10.2174/0929867013371581 · Cited by 79
Plant growth regulatory activities of artemisinin and its related compounds
Chen, P. K., & Leather, G. R. (1990) · Journal of Chemical Ecology · doi:10.1007/bf01020500 · Cited by 68
From bark to weed: The history of artemisinin
Faurant, C. (2011) · Parasite · doi:10.1051/parasite/2011183215 · Cited by 65
Qinghaosu resistance in rodent malaria
Chawira, A. N., Warhurst, D. C., & Peters, W. (1986) · Transactions of the Royal Society of Tropical Medicine and Hygiene · doi:10.1016/0035-9203(86)90351-2 · Cited by 64
Everard Napier, L. (1951) · PubMed · Cited by 56
Weathers, P. J., Elfawal, M. A., Towler, M. J., Acquaah-Mensah, G. K., & Rich, S. M. (2014) · Journal of Ethnopharmacology · doi:10.1016/j.jep.2014.03.037 · Cited by 54
Self-citationMinireview: Modulation of Hormone Receptor Signaling by Dietary Anticancer Indoles
Firestone, G. L., & Sundar, S. N. (2009) · Molecular Endocrinology · doi:10.1210/me.2009-0149 · Cited by 50
Herbicide and Pharmaceutical Relationships
Duke, S. O. (2010) · Weed Science · doi:10.1614/ws-09-102.1 · Cited by 43
Composition of the Essential Oil ofTanacetum polycephalumSchultz Bip.
Morteza‐Semnani, K. (2006) · Journal of Essential Oil Research · doi:10.1080/10412905.2006.9699041 · Cited by 39
Peters, W. (1999) · Annals of Tropical Medicine and Parasitology · doi:10.1080/00034989958087 · Cited by 35
Zhang, Y., Ding, W., Zhi-mo, Z. H. A. O., Wu, J., & Yu-hu, F. A. N. (2008) · Agricultural Sciences in China · doi:10.1016/s1671-2927(08)60055-3 · Cited by 31
Plasmodium falciparum growth is arrested by monoterpenes from eucalyptus oil
Su, V., King, D. J., Woodrow, I. E., McFadden, G. I., & Gleadow, R. M. (2008) · Flavour and Fragrance Journal · doi:10.1002/ffj.1880 · Cited by 31
W. Peters, B. L. R. (2000) · Annals of Tropical Medicine and Parasitology · doi:10.1080/00034980057581 · Cited by 27
Artemisinin: A Versatile Weapon from Traditional Chinese Medicine
Efferth, T. (2008) · Springer eBooks · doi:10.1007/978-3-540-79116-4_11 · Cited by 26
Rodrigues, L., Henriques, G., Borges, S. T., Hunt, P., Sanchez, C. P., Martinelli, A., & Cravo, P. (2010) · PLoS ONE · doi:10.1371/journal.pone.0011593 · Cited by 25
Terpenoids from the Genus Artemisia as Potential Pesticides
Duke, S. O., Paul, R. N., & Lee, S. M. (1988) · ACS symposium series · doi:10.1021/bk-1988-0380.ch021 · Cited by 21
Artemisinin Inhibits Chloroplast Electron Transport Activity: Mode of Action
Bharati, A., Kar, M., & Sabat, S. C. (2012) · PLoS ONE · doi:10.1371/journal.pone.0038942 · Cited by 20
Zhang, Yongqiang, Ding, Wei, Zhao, Zhi-mo, Wu, Jing, Fan, & Yuhu (2008) · Journal of Integrative Agriculture · Cited by 15
Larvicidal activity of Artemisia annua L. callus culture against Anopheles stephensi larvae.
Bartarya, R., Srivastava, A., Tonk, S., Bhatnagar, V. P., Srivastava, S., & Kumari, K. M. (2009) · PubMed · Cited by 13
Peters, W. (1999) · Annals of Tropical Medicine and Parasitology · doi:10.1080/00034983.1999.11813461 · Cited by 12
Peters, W., & Robinson, B. L. (2000) · Annals of Tropical Medicine and Parasitology · doi:10.1080/00034983.2000.11813510 · Cited by 10
Peters, W., Robinson, B. L., Stewart, L. B., & Butcher, G. A. (2000) · Annals of Tropical Medicine and Parasitology · doi:10.1080/00034983.2000.11813592 · Cited by 7
Flagged first, then by citations
Research works printed but not linked: 2
- 10.1016/S0140-6736(05)67787-2 · DOI
- RS Bhakuni, DC Jain, RP Sharma, S Kumar, Secondary metabolites of Artemisia annua and their biological activity. Curr Sci India 80, 35–48 (2001).
Cited by
Sorted by citations
Shen, Q., Zhang, L., Liao, Z., Wang, S., Yan, T., Shi, P., Liu, M., Fu, X., Pan, Q., Wang, Y., et al. (2018) · Molecular Plant · doi:10.1016/j.molp.2018.03.015 · Cited by 315
GLANDULAR TRICHOME ‐ SPECIFIC WRKY 1 promotes artemisinin biosynthesis in Artemisia annua
Chen, M., Yan, T., Shen, Q., Lu, X., Pan, Q., Huang, Y., Tang, Y., Fu, X., Liu, M., Jiang, W., et al. (2016) · New Phytologist · doi:10.1111/nph.14373 · Cited by 230
Traditional application and modern pharmacological research of Artemisia annua L.
Feng, X., Cao, S., Qiu, F., & Zhang, B. (2020) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2020.107650 · Cited by 193
Zhao, Q. S., Luan, X., Zheng, M., Tian, X.-H., Zhao, J., Zhang, W., & Ma, B. (2020) · Pharmaceutics · doi:10.3390/pharmaceutics12020128 · Cited by 164
Artemisinin and artemisinin derivatives as anti-fibrotic therapeutics
Dolivo, D., Weathers, P., & Dominko, T. (2021) · Acta Pharmaceutica Sinica B · doi:10.1016/j.apsb.2020.09.001 · Cited by 132
Self-citation
Metadata
- Authors
- Elfawal, M. A., Towler, M. J., Reich, N. G., Weathers, P. J., & Rich, S. M.
- Affiliations
- University of Massachusetts Amherst (US)
- Worcester Polytechnic Institute (US)
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2015-01-05
- Volume
- 112
- Issue
- 3
- Pages
- 821-826
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC4311864
- OpenAlex
- W2088835649
- Cited by
- 124
- References
- 65
- Citations by year
- 2026: 9 · 2025: 14 · 2024: 6 · 2023: 11 · 2022: 11 · 2021: 10 · 2020: 11 · 2019: 10 · 2018: 9 · 2017: 7 · 2016: 17 · 2015: 9
- FWCI
- 15.01
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Center for Clinical and Translational Sciences (na)
- Topics
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Malaria Research and Control
- Life Sciences › Pharmacology, Toxicology and Pharmaceutics › Drug Discovery › Phytochemical compounds biological activities
- Physical Sciences › Chemistry › Organic Chemistry › Sesquiterpenes and Asteraceae Studies
- Keywords
- Artemisia annua, artemisinin, antimalarial drug resistance, Plasmodium yoelii, Plasmodium chabaudi, whole plant extract, malaria treatment, resistance evolution, secondary metabolites, plant defense, combination therapy, rodent malaria model
- MeSH terms
- Animals, Antimalarials, Drug Resistance, Artemisia annua, Artemisinins, Mice
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review