Industrial Crops and Products 43 (2013) 132–140
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Industrial Crops and Products
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Loss of artemisinin produced by Artemisia annua L. to the soil environment
Karina K. Jessing
a,∗
, Nina Cedergreen
a
, Philipp Mayer
a,b
, Lynn Libous-Bailey
c
, Bjarne W. Strobel
a
,
Agnes Rimando
d
, Stephen O. Duke
d
a
Department of Basic Science and Environment, University of Copenhagen, Thorvaldsensvej 40, 1871 Frederiksberg C, Denmark
b
Department of Environmental Science, Aarhus University, Frederiksborgvej 399, 4000 Roskilde, Denmark
c
United States Department of Agriculture, Crop Protection Systems Research Unit, 141 Experiment Station Rd. Stoneville, MS 38776-0350, USA
d
United States Department of Agriculture, Natural Product Utilization Research, University of Mississippi, University, MS, 38677-8048, USA
a r t i c l e i n f o
Article history:
Received 7 March 2012
Received in revised form 19 June 2012
Accepted 22 June 2012
Keywords:
Production
Yield
Environment
In situ silicone microextraction
a b s t r a c t
Artemisia annua L. synthesizes and accumulates the secondary metabolite artemisinin, a compound with
antimalarial properties. As cultivation of the plant is still the only cost effective source of artemisinin,
the production takes place in monocultures of A. annua. Artemisinin is known to have insecticidal and
herbicidal effects, and also of being toxic to A. annua. Knowing the magnitude of the different routes of loss
of artemisinin from A. annua to the soil environment makes it possible to reduce the risk of decrease in
yield as well as reducing the impact on soil organisms including plants, and reducing the risk of leaching.
The largest contributor (86–108%) of artemisinin loss to the soil environment was found to be from dead
leaves. In the case with A. annua production, the risks can hence be limited by paying attention to the
harvest and drying process, where risk of loss of plant material to the surrounding environment is the
largest. Artemisinin is also lost from A. annua by rain runoff (<0.5%) and root excretion, but to a minor
degree. The in situ silicone tube microextraction method was here successfully applied for the first time
to monitor artemisinin from roots in an A. annua soil–plant system.
© 2012 Elsevier B.V. All rights reserved.
1. Introduction
1.1. Cultivation of Artemisia annua as a medicinal plant
Artemisia annua L. (sweet wormwood, annual wormwood, sweet
annie, sweet sagewort) synthesizes and accumulates the secondary
metabolite artemisinin (Klayman, 1985), a sesquiterpene lactone
with an endoperoxide bridge (Liu et al., 1979). A. annua and
artemisinin have gained considerable attention during the last
three decades due to the antimalarial properties of artemisinin
against chloroquine-resistant strains of Plasmodium falciparum
(Klayman, 1985). At present, total chemical synthesis (Abdin et al.,
2003) or in vitro production of artemisinin (Arsenault et al., 2008)
is not economically feasible, and cultivation of the plant is still the
only cost effective source of artemisinin. Synthesis of artemisinin
is now possible from artemisinic acid (Levesque and Seeberger,
2012), making artemisinin medication cheaper, but the only source
of artemisinic acid is extraction from field grown A. annua. A.
annua is cropped in large scale in China, Vietnam, Turkey, Iran,
Afghanistan and Australia for medicinal purposes (Bhakuni et al.,
2001), and the A. annua area in Africa covers at least 5000 ha, while
∗
Corresponding author.
E-mail address: jessing@life.ku.dk (K.K. Jessing).
the cropped area worldwide for medicinal purposes is estimated
to be 12,000 ha. In Eastern Europe the plant is also cropped for
extraction of essential oils (Heemskerk et al., 2006). In addition, A.
annua is cultivated for experimental purposes in The Netherlands,
Switzerland, Finland (Laughlin et al., 2002) and Denmark. Com-
mercial A. annua is cultivated in monocultures to produce as much
artemisinin as possible, and much effort is invested into enhancing
the artemisinin yield (Abdin et al., 2003). The plants are harvested
before flowering and left on the field to dry before the dry plant
material is transported to extraction facilities.
1.2. Artemisinin distribution in A. annua
Artemisinin is stored in glandular trichomes on the surface of
the leaves and stem (Duke and Paul, 1993) and on the corolla
and on receptacles of the florets. The majority of artemisinin is,
however, located in trichomes on the leaves (Janick and Ferreira,
1996). The glandular trichomes consist of 10 cells where the two
most apical cells form a bilobed sac by the filling and expansion of
the space between the external cell walls and cuticle with secre-
tory products. The subcuticular space in this sac stores secondary
metabolites, including artemisinin. The trichomes burst as they
mature and artemisinin is leaked to the leaf surface (Duke and Paul,
1993). Younger leaves have greater trichome density and produce
more artemisinin per unit of fresh or dry weight than old leaves
0926-6690/$ – see front matter © 2012 Elsevier B.V. All rights reserved.
http://dx.doi.org/10.1016/j.indcrop.2012.06.033