Anti-Nosemosis Activity of Aster scaber and Artemisia dubia Aqueous Extracts

Open access


In our previous study, we demonstrated that the ethanol extracts of Artemisia dubia (A. dubia) and Aster scaber (A. scaber) have anti-nosemosis activity. In our present study, we intend to establish the anti-nosemosis activity of aqueous, ethyl acetate (EA), and butanol (BuOH) extracts of A. dubia and A. scaber. In order to determine the optimal dose, we performed both in vitro and in vivo toxicity for all the extracts and also carried out anti-nosemosis experiments. Although all of the extracts (aqueous, EA, and BuOH) showed in vitro and in vivo anti-nosemosis activity in a dose-dependent manner, the aqueous extracts of A. dubia and A. scaber showed more potent anti-nosemosis activity than the EA and BuOH extracts. Moreover, an aqueous extract of A. dubia + A. scaber demonstrated stronger anti-nosemosis activity compared with the aqueous extracts of either A. dubia or A. scaber alone. Although the main ingredients in A. dubia and A. scaber remain unclear, our results suggest that the active components of A. dubia and A. scaber could dissolve in the aqueous fraction.

Ahameethunisa, A.R., & Hopper, W. (2010). Antibacterial activity of Artemisia nilagirica leaf extracts against clinical and phytopathogenic bacteria. BMC Complementary and Alternative Medicine, 10, 6. DOI: 10.1186/1472-6882-10-6

Bailey, L. (1953). Effect of Fumagillin upon Nosema apis (Zander). Nature, 171: 212-213.

Calderone, N.W. (2012). Insect pollinated crops, insect pollinators and US agriculture: trend analysis of aggregate data for the period 1992-2009. PloS One 7, e37235. DOI: 10.1371/journal.pone.0037235

Chen, Y., Evans, J.D., Zhou, L., Boncristiani, H., Kimura, K., Xiao, T., Litkowski, A.M., Pettis, J.S. (2009). Asymmetrical coexistence of Nosema ceranae and Nosema apis in honey bees. Journal of Invertebrate Pathology, 101, 204-209. DOI: 10.1016/j.jip.2009.05.012

Chen, Y.P., & Huang, Z.Y. (2010). Nosema ceranae, a newly identified pathogen of Apis mellifera in the USA and Asia. Apidologie, 41, 364-374. DOI: 10.1051/apido/2010021

Chung, J.W., Im, J.G., Park, J.H., Han, J.K., Choi, C.G., Han, M.C. (1993). Left paracardiac mass caused by dilated pericardiacophrenic vein: report of four cases. American Journal of Roentgenology, 160, 25-28. DOI: 10.2214/ajr.160.1.8416638

de Graaf,D.C., Masschelein, G., Vandergeynst, F., De Brabander, H.F., Jacobs, F.J. (1993). In Vitro Germination of Nosema apis (Microspora: Nosematidae) Spores and its effect on their αα-trehalose/dglucose ratio. Journal of Invertebrate Pathology, 62, 220-225.

Genersch, E., von der Ohe, W., Kaatz, H., Schroeder, A., Otten, C., Büchler, R., Berg, S., Ritter, W., Mühlen, W., Gisder, S., Meixner, M., Liebig, G., Rosenkranz, P. (2010). The German bee monitoring project: a long term study to understand periodically high winter losses of honey bee colonies. Apidologie, 41, 332-352.

Gisder, S., Hedtke, K., Mockel, N., Frielitz, M.C., Linde, A., Genersch, E. (2010). Five-year cohort study of Nosema spp. in Germany: does climate shape virulence and assertiveness of Nosema ceranae? Applied and Environmental Microbiology, 76, 3032-3038. DOI: 10.1128/AEM.03097-09

Gisder, S., Mockel, N., Linde, A., & Genersch, E. (2011). A cell culture model for Nosema ceranae and Nosema apis allows new insights into the life cycle of these important honey bee-pathogenic microsporidia. Environmental Microbiology, 13, 404-413. DOI: 10.1111/j.1462-2920.2010.02346.x

Higes, M., Nozal, M.J., Alvaro, A., Barrios, L., Meana, A., Martín-Hernández, R., Bernal, J. L., Bernal, J. (2011). The stability and effectiveness of fumagillin in controlling Nosema ceranae (Microsporidia) infection in honey bees (Apis mellifera) under laboratory and field conditions. Apidologie, 42, 364-377. DOI: 10.1007/s13592-011-0003-2

Hirasawa, M., & Takada, K. (2004). Multiple effects of green tea catechin on the antifungal activity of antimycotics against Candida albicans. Journal of Antimicrobial Chemotherapy, 53 (2), 225-229.

Huang, W.F., Bocquet, M., Lee, K.C., Sung, I.H., Jiang, J.H., Chen, Y.W., Wang, C.H. (2008). The comparison of rDNA spacer regions of Nosema ceranae isolates from different hosts and locations. Journal of Invertebrate Pathology, 97, 9-13. DOI: 10.1016/j.jip.2007.07.001

Huang, W.F., Solter, L.F., Yau, P.M., & Imai, B.S. (2013). Nosema ceranae escapes fumagillin control in honey bees. PLoS Pathog, 9, e1003185. DOI: 10.1371/journal.ppat.1003185

Kiani, B.H., Suberu, J., & Mirza, B. (2016). Cellular engineering of Artemisia annua and Artemisia dubia with the rol ABC genes for enhanced production of potent anti-malarial drug artemisinin. Malariya Journal, 15, 252.

Kim, J.H., Park, J.K., & Lee, J.K. (2016). Evaluation of antimicrosporidian activity of plant extracts on Nosema Ceranae. Journal of Apicultural Science, 60(1), 167-178. DOI: 10.1515/jas-2016-0027

Klee, J., Besana, A. M., Genersch, E., Gisder, S., Nanetti, A., Tam, D.Q., … Paxton R.J. (2007). Widespread dispersal of the microsporidian Nosema ceranae, an emergent pathogen of the western honey bee, Apis mellifera. Journal of Invertebrate Pathology, 96, 1-10. DOI: 10.1016/j.jip.2007.02.014

Kulić, M., Aleksić, N., Stanimirović, Z., Ristić, S., Medenica, S. (2009). Examination of genotoxic effects of fumagillin in vivo. Genetika, 41, 329-338.

Kwon, H.C., Jung, C.M., Shin, C.G., Lee, J.K., Choi, S.U., Kim, S.Y., Lee, K.R. (2000). A new caffeoyl quinic acid from aster scaber and its inhibitory activity against human immunodeficiency virus-1 (HIV-1) integrase. Chemical and Pharmaceutical Bulletin, 48, 1796-1798.

Li, Z.J., Liu, M., Dawuti, G., Dou, Q., Ma, Y., Liu, H. G., Aibai, S. (2017). Antifungal activity of gallic acid in vitro and in vivo. Phytotherapy Research, 31(7), 1039-1045.

Lopez, M.I., Pettis, J.S., Smith, I.B., & Chu, P.S. (2008). Multiclass determination and confirmation of antibiotic residues in honey using LC-MS/MS. Journal of Agricultural and Food Chemistry, 56, 1553-1559. DOI: 10.1021/jf073236w

Mahilranjan, S., Nandakumar, J., Kailayalingam, R., Manoharan, N.A., SriVijeindran, S. (2014). Screening the antifungal activity of essential oils against decay fungi from palmyrah leaf handicrafts. Biological Research, 47(1), 35.

Molina, J.M., Goguel, J., Sarfati, C., Michiels, J.F., Desportes-Livage, I., Balkan, S., … Decazes J.M. (2000). Trial of oral fumagillin for the treatment of intestinal microsporidiosis in patients with HIV infection. ANRS 054 Study Group. Agence Nationale de Recherche sur le SIDA. AIDS, 14, 1341-1348.

Molina, J.M., Tourneur, M., Sarfati, C., Chevret, S., de Gouvello, A., Gobert, J.G., Balkan, S., Derouin, F. (2002). Fumagillin treatment of intestinal microsporidiosis. The New England Journal of Medicine, 346, 1963-1969. DOI: 10.1056/NEJMoa012924

Montagner, C., de Souza, S.M., Groposoa, C., Delle Monache, F., Smânia, E.F., Smânia, A.(2008). Antifungal activity of coumarins. Zeitschrift für Naturforschung C, 63(1-2), 21-8.

Pajuelo, A.G., Torres, C., & Bermejo, F.J.O. (2008). Colony losses: a double blind trial on the influence of supplementary protein nutrition and preventative treatment with fumagillin against Nosema ceranae. Journal of Apicultural Research, 47, 84-86.

Pohorecka, K. (2004). Laboratory studies on the effect of standardized Artemisia absinthium L. extract on Nosema apis infection in the worker Apis mellifera. Journal of Apicultural Science, 48, 131-136.

Porrini, M.P., Fernández, N.J., Garrido, P.M., Gende, L.B., Medici, S.K., Eguaras, M.J. (2011). In vivo evaluation of antiparasitic activity of plant extracts on Nosema ceranae (Microsporidia). Apidologie, 42, 700-707. DOI: 10.1007/s13592-011-0076-y

Ptaszynska, A.A., Borsuk, G., Anusiewicz, M., & Mulenko, W. (2012). Location of Nosema spp. spores within the body of the honey bee. Medycyna weterynaryjna, 68 (10), 618-621.

Ptaszyńska, A.A., Paleolog, J., & Borsuk, G. (2016) Nosema ceranae infection promotes proliferation of yeasts in honey bee intestines. PLoS ONE, 11(10), e0164477.

Rhimi, W., Salem, I.B., Immediato, D., Saidi, M., Boulila, A., Cafarchia, C. (2017). Chemical Composition, Antibacterial and Antifungal Activities of Crude Dittrichia viscosa (L.) Greuter Leaf Extracts. Molecules, 22, 942.

Sardi, J.C., Gullo, F.P., Freires, I.A., Pitangui, N.S., Segalla, M.P., Fusco-Almeida, A.M., ..., Mendes-Giannini, M.J.(2016). Synthesis, antifungal activity of caffeic acid derivative esters, and their synergism with fluconazole and nystatin against Candida spp. Diagnostic Microbiology and Infectious Disease, 86 (4), 387-391.

Sprague, V., & Becnel, J.J. (1998). Note on the name-author-date combination for the taxon “Microsporidies” Balbiani, 1882, when ranked as a phylum. Journal of Invertebrate Pathology, 71, 91-94.

Sprague, V., & Becnel, J.J. (1999). Appendix: checklist of available generic names for Microsporidia with-type species and type hosts, Wittner M., Weiss L. M. (eds.): Microsporidia and Microsporidiosis. ASM Press, Washington, D.C. 517-530.

Stanimirović, Z., Aleksić, N., Kulić, M., & Maletić, M. (2010). Fumagillininduced chromosome aberrations in mouse bone-marrow cells. Archives of Biological Sciences, 62, 47-55.

Strachecka, A., Krauze, M., Olszewski, K., Borsuk, G., Paleolog, J., Merska, M., …, Grzywnowicz, K. (2014a). Unexpectedly strong effect of caffeine on the vitality of western honeybees (Apis mellifera). Biochemistry (Moscow), 79(11), 1192-1201.

Strachecka, A., Olszewski, K., Paleolog, J., Borsuk, G., Bajda, M. (2014b). Coenzyme Q10 treatments influence the lifespan and key biochemical resistance systems in the honeybee, Apis mellifera. Archives of Insect Biochemistry and Physiology, 86(3), 165-179. DOI: 10.1002/arch.21159

Strachecka, A., Olszewski, K., & Paleolog, J. (2015). Curcurmin stimulates biochemical mechanisms of Apis Mellifera resistance and extends the apian lifespan. Journal of Apiculture Science, 59(1), 129-141.

Tariq, K.A., Chishti, M.Z., Ahmad, F., & Shawl, A.S. (2009). Anthelmintic activity of extracts of Artemisia absinthium against ovine nematodes. Veterinary Parasitology, 160, 83-88. DOI: 10.1016/

Whittington, R., & Winston, M.L. (2003). Effects of Nosema bombi and its treatment fumagillin on bumble bee (Bombus occidentalis) colonies. Journal of Invertebrate Pathology, 84, 54-58.

Williams, G.R., Sampson, M.A., Shutler, D., & Rogers, R.E. (2008). Does fumagillin control the recently detected invasive parasite Nosema ceranae in western honey bees (Apis mellifera)? Journal of Invertebrate Pathology, 99, 342-344. DOI: 10.1016/j.jip.2008.04.005

Williams, G.R., Shutler, D., Burgher-MacLellan, K.L., & Rogers, R.E. (2014). Infra-population and -community dynamics of the parasites Nosema apis and Nosema ceranae, and consequences for honey bee (Apis mellifera) hosts. PloS One 9, e99465. DOI: 10.1371/Journal.pone.0099465

Yanase, T., Tamura, M., Fujita, K., Kodama, S., Tanaka, K. (1993). Inhibitory effect of angiogenesis inhibitor TNP-470 on tumor growth and metastasis of human cell lines in vitro and in vivo. Cancer Research, 53, 2566-2570.

Journal of Apicultural Science

The Journal of Research Institute of Horticulture and Apicultural Research Association

Journal Information

IMPACT FACTOR 2017: 0.75
5-year IMPACT FACTOR: 1.007

CiteScore 2017: 0.92

SCImago Journal Rank (SJR) 2017: 0.345
Source Normalized Impact per Paper (SNIP) 2017: 0.461


All Time Past Year Past 30 Days
Abstract Views 0 0 0
Full Text Views 229 229 59
PDF Downloads 154 154 34