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Global Impact of Non-essential Heavy Metal
Contaminants in Industrial Cannabis Bioeconomy
Louis Bengyella ( bengyellalouis@gmail.com )
Penn State: The Pennsylvania State University
Mohammed Q.O. Ali
University of Hail
Piyali Mukherjee
The University of Burdwan
Dobgima J. Fonmboh
University of Bamenda
John E. Kaminski
Penn State: The Pennsylvania State University
Research Article
Keywords: Arbuscular mycorrhizae, cannabidiol, hemp, heavy metals, radioactive cannabis
DOI: https://doi.org/10.21203/rs.3.rs-575683/v1
License: This work is licensed under a Creative Commons Attribution 4.0 International License.
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Abstract
The intrinsic signatures of
Cannabis
species to bioaccumulate non-essential harmful heavy metals
(HMs) are substantially determined by their high tolerance, weedy propensities, phenotypic plasticity
attributes, and pedoclimatic stress adaptation in an ecological niche. The detection trends of HMs
contaminants in cannabis products have reshaped the 2027 forecast and beyond for global cannabis
trade valued at $57 billion. Consumer base awareness for the cohort of HMs contaminants viz., lead (Pb),
mercury (Hg), arsenic (As), chromium (Cr), cadmium (Cd), and radioactive elements, and the associative
dissuading effects signicantly impact cannabis bioeconomy. On the premise that ber hemp (
Cannabis
sativa
L.) could be repurposed to diverse non-consumable products, concerns over HMs contamination
would not signicantly decrease ber trade, a trend that could impact globally by 2025. The economic
trend will depend on acceptable consumer risk, regulatory instruments, and grower's due diligence to
implement agronomic best practices to mitigate HMs contamination in marketable cannabis-related
products. In this unstructured meta-analysis study based on published literature, the application of
Cannabis
species in HMs phytoremediation, new insights into transportation, distribution, homeostasis of
HMs, the impact of HMs on medical cannabis, and cannabis bioeconomic are discussed. Furthermore, a
blueprint of agronomic strategies to alleviate HMs uptake by plant is proposed. Considering that one-third
of the global arable lands are contaminated with HMs, revamping global production of domesticated
cannabis requires a rethinking of agronomic best practices and post-harvest technologies to remove HMs
contaminants.
1. Introduction
The 21st century rejuvenated interest in
Cannabis sativa
Linn, known as industrial hemp (when
expressing tetrahydrocannabinol (THC) < 0.3%) or marijuana (THC > 0.3%) is predicted to grow to a
$57billion bioeconomy by 2025 (Reporterlinker 2019) even though growing the plant remains largely
illegal worldwide. Exposure to air pollutants, domestic euents, direct root absorption from the earth's
crust, cross-contamination during the drying process, and post-processing adulteration with additives to
enhance market value are the main sources of non-essential heavy metals (HMs) in cannabis products
(Busse et al. 2008). Decision-making in industrial cannabis production must integrate the following: (1)
that one-third of the global arable lands are contaminated (Tripathi et al. 2016) with HMs such as lead
(Pb), chromium (Cr), arsenic (As), zinc (Zn), cadmium (Cd), copper (Cu), mercury (Hg), and nickel (Ni), (2)
that
Cannabis
species have a high propensity to bioaccumulate HMs from their growing medium (Galić et
al. 2019; Husain et al. 2019; Linger et al. 2005), and (3) that there is no market value for cannabis product
contaminated with Hg, Cd, As, and Pb above the permissible threshold. This cohort of elements (As, Pb,
Cd, Hg, Cr) are often with unknown biological purposes and toxic at higher concentrations in plants
(Fig.1; Hajar et al. 2014). While deciency and excessive uptake of benecial elements in cannabis is
phenotypically expressed, hyperaccumulation of HMs in the roots and above-ground tissues is
associated with no detectable morphological changes (Galić et al. 2019; Linger et al. 2005). This
suggests that the cultivation of cannabis should be accompanied by HMs monitoring at all growth
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stages. Interestingly, a comparative gene expression analysis for known HMs transporter in six cannabis
genotypes (Fedora 17, Felina 32, Ferimon, Futura 75, Santhica 27, and USO 31 expressing THC < 0.3%)
grown on HMs contaminated soil, and two commercial soils (Miracle-Gro Potting Mix® and PRO-MIX
Mycorrhizae High Porosity Grower Mix®) did not uncover major signicant differential expression for
HMs transporter genes such as
phosphate transporter PHT1:1
and
PHT1:4
,
heavy metal transporter 3
(HMA3)
and
vacuolar cation-proton exchanger (CAX)
genes (Husain et al. 2019). From this study, it is
tempting to hypothesize that domesticated cannabis genotypes have an evolved pedoclimatic stress
adaptation in their ecological niche that enhanced their propensity to function as HMs accumulators by
constitutively expressing HMs transporters. In this light, HMs contamination levels in cannabis products
are positively correlated to the degree of plant exposure to the metals in a given ecological niche that
could severely affect end-users. In this unstructured meta-analysis study based on published literature,
the application of
Cannabis
species in HMs phytoremediation (Fig.1, 2), new insights into the
transportation, distribution, and homeostasis of HMs in the cannabis plant (Fig.3), the impact of HMs on
medical cannabis (Fig.4), and the bioeconomy (Fig.5) are discussed. We proposed novel blueprint
agronomic strategies to mitigate HMs uptake at the farm level. We discuss the direct impact of HMs-
contamination in a hypothetical scenario by 2025 should cannabis stakeholders fail to address the issue
in marketed cannabis products.
2. Materials And Methods
2.1 Unbiased database search strategy and synthesis
An unstructured review was performed on HMs contamination in cannabis based on available data in
published literature (from Medline, Scopus, Google Scholar, and CINAHL) and gray literature in book
chapters and unindexed sources, including local and global agencies entries such as the FAO, and WHO
in February–May 2021. Keywords for the unstructured search were
“
cannabis HMs contaminant
”,
“
cannabis trace metals
”, “
hemp HMs contaminant
”, “
hemp trace metals
”
, “cannabis phytoremediation of
HMs”, “hemp phytoremediation of HMs”,
“
cannabis mercury toxicity”,
“
cannabis proteins and chelators
”
and
“
hemp proteins and chelators
”.
Key MeSH terms used included “hemp bioaccumulation of metals
”,
“
hemp bioaccumulation of HMs
”, “
metals in cannabis smoke
”, “
metals in hemp smoke
”
and “harmful
effects of heavy metals in cannabis and hemp”. A rened search was performed using the
aforementioned keywords except that the word “metal” was replaced either by arsenic, cadmium, lead,
and mercury, and cannabis (or hemp) was replaced by
Cannabis sativa
L. After reading the abstract for
relevance, the most appropriate articles were fully reviewed and synthesized. The overarching data set of
25 articles (Additional information S1) were consolidated with the objectives of the study as follows: i)
the application of cannabis in phytoremediation, ii) fate of HMs in cannabis, iii) medical impact of HMs
in cannabis, iv) agronomic strategies to mitigate HMs uptake, and v) impact of HMs in cannabis
bioeconomy.
3. Results And Discussion
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3.1 Cannabis mediated phytoremediation of heavy metals
contaminants
The average cost of remediating HMs contaminant soil using plants is $37.7/m3 (Wan et al. 2016), a
lucrative and cheaper option to other remediation technologies. This led to the search for plant species
having traits for HMs bioaccumulation and tolerance capabilities. We discussed the inherent features of
cannabis to remediates radioactive metals, HMs, the mechanism of transport, and the impact of this
bioaccumulation trait in the cannabis business.
3.1.1 There is a high likelihood that radioactive cannabis ends up with consumers: Increasing detection
of HMs load in
Cannabis sp
ecies on one hand emerged as the ultimate answer to land remediation
efforts owing to its unique morphological characteristics such as stem length, fast growth at the
vegetative stage, root area and leaf surface, high photosynthetic activity, fewer nutrient requirements for
survival, and shorter life cycle (~ 180 days).
Cannabis species
exhibits a great geo-demographic diversity
showing prominence in the wild and cultivated lands (Mura et al. 2004) and on soil pH 5–7 which are
excellent attributes for phytoremediation. The use of plants to remove, transfer, stabilize and destroy
contaminants in the soil and groundwater (Fig.1) is called phytoremediation.
Cannabis
species are
endowed with stress-tolerant genes which ensure in part their phenotypic and chemotypic plasticity as a
mechanism for adaptation in an ecological niche. Cannabis species act as a hyper-accumulator of
radioactive elements, toxins, pesticides, and polycyclic aromatic hydrocarbons such as chrysene and
benzo[a]pyrene through the fundamental processes of phytoaccumulation, phytovolatilization, and
phytodegradation in their leaves (Campbell et al. 2002; Greipsson 2011; Morin-Crini et al. 2018). When
cannabis was grown in emulated Chernobyl conditions with radiocesium (Cs-137), radioactivity was
detected in all plant tissues as well as retting water, ber, seed oil, and biofuel which could potentially end
up in the hands of consumers (Vandenhove and Van Hees 2005). Akin to the above study, maximum
absorption, and distribution of strontium (Sr
-
90) was 45%, 45%, and 15% in roots, stem, and leaves,
respectively (Hoseini et al. 2012). The extensive rhizosphere of cannabis owing to its long root system (~
2.4 m below the ground level), naturally resistant to pests, thus, obviating the need for pesticides gives
cannabis species an extra edge over other plants used for phytoremediation. With this high propensity to
bioaccumulate radioactive material from the soil, it is obvious that cannabis used in phytoremediation (or
cannabis that is erroneously grown on radioactively contaminated soil) cannot nd its place as animal
feed, human food, supplements nor textile. Thus, impeding the cannabis bioeconomy. Nonetheless,
repurposing radioactive cannabis biomass for electricity and ethanol production could be a possibility to
salvage grower's investment, even though poor oxidation stability in biodiesel production has been
reported (Li et al. 2010).
3.1.2 Non-essential heavy metal contaminated cannabis ends up with consumers: While selenium (Se) is
a benecial element in plants, excess in human results in nausea, vomiting, nail discoloration, nail
brittleness, nail loss, hair loss, fatigue, irritability, and foul breath odor (MacFarquhar et al. 2010).
C.
sativa
sequestrates Se mainly in leaf vasculature and seed embryos, with predominant Se speciation in C
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− Se − C forms (57 − 75% in leaf and more than 86% in seeds) (Stonehouse et al. 2020). Equally, cannabis
seed extracts contain selenomethionine and methyl-selenocysteine which are excellent dietary Se
sources, highlighting the implication of cannabis in phytoremediation as well as biofortication.
Cannabis species follows a unique genotype-dependent pattern for accumulating non-essential HMs as
evident from various studies: For example, when grown in moderate Cd levels of 17 mg/kg soil showed
seasonal changes in photosynthetic performance whereas extreme levels above 800 mg/kg caused
signicant loss of vitality and biomass (Girdhar et al. 2014). The cannabis strain, Zenit (THC < 0.3%) had
a high iron accumulation property (1859 mg/kg) compared to other varieties (Mihoc et al. 2012) while
another study indicated that the Tygra variety accumulated metals as follows Fe > Mn > Zn > Cr > Cu > Ni >
Cd (Zielonka et al. 2020). Interestingly, when these data were correlated with bioavailability in soil, Cd and
Cr were accumulated the most while Fe was absorbed and transported to the aboveground tissues to the
least and stored particularly in plant inorescences (Mihoc et al. 2012; Zielonka et al. 2020). Using
cannabis genotypes viz., Fedora 17, Fibrol, Futura 75, and Santhica (expressing THC < 0.3%) grown on
acid and alkaline soil (Galić et al. 2019) displayed differential accumulation of Pb, Hg, Cd, and As (Fig.2).
From these studies, we postulate that cannabis exhibits bioaccumulation preferences for HMs which is
genotype-dependent as well as growing medium pH-dependent (Fig.3) irrespective of their nutritional
requires. This thesis is supported by the apparent constitutive expression of HMs transporters genes viz.,
PHT1:1
,
PHT1:4
,
HMA3
, and
CAX
genes (Husain et al. 2019). It is tempting to suggest that cannabis has
evolved the HMs accumulation mechanism which is not dependent on the growing medium but the
availability of HMs in the medium, type of heavy metal, plant genotype, and medium pH.
3.1.3 Insights into the molecular mechanism of HMs phytoremediation in cannabis: Differential gene
expression has been observed during phytoremediation of HMs in cannabis. Metal cation uptake is
routed through four steps in the cannabis plant starting from metal uptake through the root system,
loading into the xylem vessels, translocation, chelation, and sequestration during tracking to the
phloem. The inux of metal cations into the root occurs via symplastic and apoplastic pathways wherein
metal tracking ZRT-YRT-like proteins, yellow stripe-like transporters (YSL), and natural resistance-
associated macrophage proteins (NRAMP) play a critical role (Vert et al. 2002). The HMs loading into
xylem vessels occurs via HMA2 and/or HMA4 proteins (Park and Ahn 2017), and sequestration results
from the binding of chelating proteins and transporters (Uraguchi et al. 2009). Heavy metals tracking
from xylem to phloem is mediated by
PHT1:1
,
PHT1:4
, and heavy metal ATPase and cation exchanger 2
(Wong and Cobbett 2009). Recently, Ahmad et al. (2016) identied two important HMs responsive genes,
glutathione-disuldereductase
(
GSR
) and
phospholipase D-α
(
PLDα
) in
C. sativa
that are overregulated by
reactive oxygen species (ROS) produced under stress. In another study, an increase in phytochelatin and
DNA content was observed when
C. sativa
was subjected to heavy metal stress conditions (Citterio et al.
2003). The cannabis genome consists of 54 GRAS transcription factors (involved in growth and
development) that regulate 40 homologous GRAS genes under cadmium stress (Ming-Yin et al. 2020).
Thus, we suggest the application of reverse genetics to silence HMs transporters in the developmental
process of next-generation domesticated cannabis. This approach has the potential to mitigate the
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intrinsic phytoremediation propensity, ensure consumer safety, and boost cannabis safety and its
bioeconomy.
3.2 The fate of non-essential heavy metals in cannabis
trichome, seed, and consumers
Cannabis reproductive structures such as seed and ower are arguably highly valued on the market for
phytocannabinoids, avonoids, terpenoids, rich protein sources, and omega-6 and omega-3 oil-rich in a
desirable range between 1:2 and 1:3 (Callaway 2004). Understanding the fate of HMs homeostasis in
these reproductive structures is thus critical for consumer safety as more than 500 different compounds
characterized in
Cannabis
species are used for several medical interventions (Alves et al. 2020). Plants
often counter the destructive effects of HMs by: (i) inactivating the HMs and preventing them from
forming a complex with metal chelators such as phytochelatins (PCs) and metallothioneins, and (ii)
compartmentation of HMs in idioblasts, vacuoles, and cells walls (Harada et al. 2010; Mazen and El
Maghraby 1997). Plants, therefore, rely on low-molecular-weight proteins, the metallochaperones or
chelators (such as spermine, spermidine, putrescine, nicotianamine, glutathione, phytochelatins, and
other organic acids), metallothioneins, phenylpropanoid compounds (such as avonoids and
anthocyanins), amino acids (proline and histidine), stress-responsive phytohormones and even heat
shock proteins (Dalvi and Bhalerao 2013) to effectively counter HMs. Glandular trichomes in cannabis
species are microscopic protrusion of variable sizes on ower and leaf surfaces that often-entrap
phytocannabinoids (Fig.3) could potentially play a critical role in HMs homeostasis.
High accumulation of metals in trichomes (Sarret et al. 2006), their role in sequestration and
compartmentalization of HMs have been reported (Harada et al. 2010). Long and short glandular
trichomes of
Nicotiana tabacum
(tobacco) accumulate and excretes HMs at the tips of trichomes cells
(Harada et al. 2010). For instance, Cd and Zn are expelled at the tip of trichomes cells as calcium-crystal
precipitates (Sarret et al. 2006). Putative cysteine-rich pathogenesis resistance proteins (PR) such as
osmotin, thaumatin-like proteins, non-specic lipid transfer proteins (nsLTPs), and
metallocarboxypeptidase inhibitors in tobacco trichomes were shown to be sequestrating agents of Cd
(Harada et al. 2010). Since trichome apparently is one of the exit points of HMs in the narcotic tobacco
plant, it could be interesting for cannabis breeders to incorporate trichome HMs metabolism in their
breeding program as trichome quality is a determining factor in the market value of cannabis ower. Akin,
this creates an avenue to investigate which of the HMs exit the cannabis plant at the tip of trichome cells.
On the other hand, cannabis seed is valuable on the essential oil market. Contamination of seeds with Cd
at 1.3–4.0 ppm (Mihoc et al. 2012) and Cr at 15.2–15.25 ppm (Eboh and Thomas 2005) have been
reported, making it possible to postulate that vertical transmission and storage of HMs in cannabis
reproductive tissues is apparent. A total of 181 proteins have been identied in cannabis seed (Aiello et
al. 2017). Two major storage cannabis seed proteins identied are the legumin-type globulin edestin and
globular-type albumin constituting 67–75% and 25–37% of total cannabis protein, respectively (Aiello et
al. 2017). These proteins are void of enzymatic activities but have high Zinc–metal binding capacity
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(Wang and Xiong 2018) an indication that they serve as zinc sequestration and storage-hub in the
reproductive tissues of cannabis. While these two seed storage proteins have not been reported in
trichomes, one might be tempted to ask whether cannabis seed storage proteins play a role in entrapping
and sequestering non-essential Hg, Cr, Cd, As, and Pd akin to Zn? It could be interesting to investigate the
interactions of HMs with metallothionein and phytochelatins at the trichome level to gain insights into
their potential to form complexes that could be transferred to end-users of cannabis products.
3.3 Medical implications of regulated heavy metals in
cannabis
The current trends at which non-essential HMs is been detected in cannabis products (Saltiola 2020;
Wakshlag et al. 2020) had failed to dissuade human interest in the crop bers and therapeutic uses
despite concerns of accumulation in the body of end-users. Cannabis, like other crops, richly contains
essential heavy metals such as iron, cobalt, copper, manganese, molybdenum, and zinc which are
required for biochemical and physiological processes (Briffa et al. 2020) but toxic at higher
concentrations (Singh et al. 2011). Evidence-based concerns over Cd, Pb, Hg, As, and Cr contaminations
encountered during the cultivation and post-harvest processing (Gauvin et al. 2018) have emerged as a
major drawback to the global use of cannabis species in medicine. Also, premeditated adulteration of
cannabis products for market prot as in the case of Leipzig, Germany that resulted in acute poisoning of
150 people (Busse et al. 2008) is an inhibitive factor for medical utilization in several countries. The high
amount of HMs contamination in cannabis can cause various health problems because these elements
are rarely metabolized, thus, accumulates in specic areas of the human body (Fig.4).
The most common mechanism of HMs toxicity in the human body is via the production of reactive
oxygen species (ROS) and free radicals which damage either enzymes, proteins, lipids, and nucleic acids
resulting in carcinogenesis and neurotoxicity (Engwa et al. 2019). Cannabis consumed in combustive
form represents the greatest danger to human health. Using tobacco, it was shown that less than one
percent of Hg remains in the ash after combustion (“smoking”), while elemental mercury (Hg°) is carried
in the smoke (Andren and Harriss 1971). Furthermore, smoking any form of contaminated cannabis
introduces the whole mercury load in the biomass into the lungs where 75–85% of Hg is absorbed and
retained within 40 hours (Siegel et al. 1988), a scenario more likely for Cd, Cr, As, and Pb. Interestingly,
most smoke from unltered cannabis products is rich in aluminum, Cr, Cu, Pb, and Hg (Gauvin et al.
2018). Furthermore, analysis of HMs in the smoke of cannabis (THC > 0.3%, marijuana) revealed the
presence of selenium (Se), Hg, Cd, Pb, Cr, Ni, and As (Moir et al. 2008).
A recent study showed that NatureDry© lyophilized FINOLA® hemp juice grown on ne-sandymoraine
soil in central Finland contained minute concentrations of Cd, Hg, and Pb (Saltiola 2020), but, sucient to
trigger a long-term chronic effect. Chronic toxicity effects of HMs often damage and alter the functioning
of organs such as the brain, kidney, lungs, liver, and blood, which lead to muscular, physical, and
neurological disorders associated with Parkinson disease, Alzheimer disease, multiple sclerosis, muscular
dystrophy and cancer (Engwa et al. 2019; Jaishankar et al. 2014). In essence, chromium III (Cr3+) and
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inorganic arsenic (As3+, arsenite; As5+, Arsenate) abundantly generates different free radicals including
superoxide (O2 •−), nitric oxide (NO•), hydrogen peroxide (H2O2), peroxyl radical (ROO•) and dimethylarsinic
peroxyl radicals ((CH3)2AsOO•) (Liu and Shi 2001; Pi et al. 2003; Rin et al. 1995) responsible for oxidative
stress and cause cellular damages
in vivo
(Fig.1). Non-essential cadmium (Cd2+ ions) promotes
apoptosis, DNA methylation, and DNA damage (Engwa et al. 2019). Besides HMs ROS-mediated harmful
effects, it was shown that the smoke from cannabis contains HCN, NO, NOx, and polycyclic aromatic
hydrocarbons, which are toxic to human health more than tobacco (Moir et al. 2008). Lead (Pb) causes
neurological toxicity in three stages
viz
., (i) inhibits N-methyl-d-aspartate receptor, (ii) block the neuronal
voltage-gated calcium (Ca2+) channels, and (iii) reduce the expression of brain-derived neurotrophic
factor (Neal and Guilarte 2013). Hence, consumption of HMs contaminated cannabis above permissible
levels might lead to severe medical conditions in the long term (Fig.4). Thus, this could dissuade new
medical and recreational consumers of cannabis products impeding the cannabis bioeconomy worldwide
from achieving the predicted $57billion trade value by 2027.
3.4 Blueprint agronomic strategies to mitigate non-essential
HMs in cannabis product
Atomic absorption spectrometer and inductively coupled plasma mass spectrometry (ICP–MS) have
emerged as the method of choice to detect and quantify HMs in cannabis products in the United States.
With the prevailing evidence that cannabis species have the propensity to uptake HMs from any growing
medium, efforts to shield consumers from HMs should occur principally at the farm level through best
agronomic practices. This is because one-third of global arable lands are contaminated with non-
essential HMs (Tripathi et al. 2016). Agronomic practices must improve and adopt diverse strategies that
mitigate bioaccumulation of HMs in cannabis. Important agronomic practices are herein discussed:
3.4.1 Primary agronomic best practices base on site selection: Lowering post-harvest losses should be
prioritized by cannabis growers since HMs awareness is growing within the consumer base. For instance,
the Business and Professions Code (BPC 2019) of the State of California, USA have set limits for Cd, Pb,
Ar, and Hg per gram of inhalable cannabis products (ICP) and other cannabis products (OCP) as follows:
Cd (0.2 µg/g ICP and 0.5 µg/g OCP), Pb (0.5 µg/g ICP and 0.5 µg/g OCP), Ar (0.2 µg/g ICP and 1.5 µg/g
OCP) and Hg (0.1 µg/g ICP and 3.0 µg/g OCP). These values suggest that outdoor growers must perform
their due diligence in choosing their outdoor cultivation sites. The following blueprints can be adopted to
avoid post-harvest losses caused by HMs:
i) Select cultivation sites away from industrialized zones, zones with mining activities), zones with
contemporary volcanic activities (Siegel et al., 1988), and consult the soil conservation service for HMs
data.
ii) Perform air quality test for HMs emanating from industrially polluted air-To this effect, analyses on
invasive weeds growing on the selected site could provide clues for soil quality and HMs content.
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iii) Perform irrigation water test, soil test, and soil pH test before and during cannabis Soil pH is very
critical for HMs bioaccumulation in cannabis At pH > 7.0 bioaccumulation of HMs from the soil in
decreasing order is Cu > Cr > Cd > Mo > Hg > Zn > Ni > Co > As > Pb while at pH < 7.0 the pattern is as follows
Zn > Cd > Cr > Ni > Hg > Cu > Mo > As > Co > Pb (Galić et al. 2019). By exploring the data in Galić et al.
(2019) we found that mercury accumulates more in the leaf (~ 0.015 ppm) and roots (0.038 ppm) of
cannabis in acid soil more than in basic soil (Fig.2).
iv) Monitor the crop at all development stages, notably at the vegetative phase as cannabis draws a large
number of minerals to maintain its fast growth rate.
v) Use only fertilizers, grow selected variety with certied seeds, and use only pesticides with a certicate
of analysis stating HMs-free.
3.4.2 Advanced agronomic practice-based on-site management: Laboratory research must be integrated
with agronomic practices to deliver instruments that can mitigate uptake of HMs. We proposed the
following blueprints:
i) Avoid the use of arbuscular mycorrhizae
(AM): Previous studies show that AM enhanced the
translocation of Cd, Ni, and Cr (VI) from the root to the shoot of
C. sativa
(Citterio et al. 2005). In
cultivation practice where
C. sativa
was fertilized with sewage sludge and phosphogypsum, AM was
detected (Zielonka et al. 2020). Akin, the interaction of AM and sunower (
Helianthus annuus
L.) on
heavily contaminated soil was shown to signicantly promote shoot phytoextraction of Cd, Pb, Cu, Cr, Zn,
and Ni (Zhang et al. 2018). Previously, it was shown that the interactions of AM with plant
Lygeum
spartum
and
Anthyllis cytisoides
in the presence of either Pb or Zn stimulated the plant growth in direct
proportion to the amount of Pb and Zn added to the soil (Díaz et al. 1996). Taken together with this
evidence, it is tempting to suggest that cultivation practices of cannabis for grains and cannabinoids
should completely avoid the use of AM.
ii) Avoid the use of Achromobacter
: Another trigger for increased HMs uptake in cannabis is associated
with
Achromobacter sp
. strain AO22 that had been shown to concomitantly enhanced plant growth
accumulation of Cd and Zn in ber crop plant; sunn hemp (
Crotolaria juncea
) (Stanbrough et al. 2013).
iii) Field monitoring
: Farmers must perform a robust soil test after heavy torrential rainfall and This is
applicable for farming sites located in areas where snowfall and snow melting activities are common.
iv) pH modication of chemigation, and irrigation water
: Cannabis is acidophilic (~ 5.56–7.and the
uptake of Pb and Hg in plants occurred at pH below 6.Thus, ensuring pH stays above 6.5 in all
chemigation practices can mitigate Pb and Hg absorption from the soil (Azevedo and Rodriguez, 2012).
This approach heavily depends on the soil test results for HMs. Unlike Pb and Hg, the highest absorption
of Cd in perennial ryegrass (
Lolium perenne
L), Cocksfoot (
Dactylis glomerata
L), lettuce (
Lactuca sativa
L), and watercress (
Rorippa nasturstium-aquaticum
L) was observed at pH 5.0–7.0 (Hatch et al. 1988).
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Thus, while pH modication might confer HMs mitigation control, the uniqueness of cannabis biology
requires similar experiments to be performed.
v) Coupling ozone water treatment with water softener system
: Ozone water treatment could help
oxidized HMs in irrigation water and coupling ozonized system with a water softener system, could help
remove oxidized forms of the HMs before they are delivered to the cannabis crops.
3.5 Impact of heavy metals contamination on cannabis
bioeconomic by 2025
Relaxation on regulatory laws governing industrial cannabis production had generated fortunes to many
industrialized nations, notably the United States. For instance, the industrial hemp- cannabidiol (CBD)
market contributed $4billion to the United States economy in 2020, forecasted and valued at $16billion
by 2025 (Kristen 2019) while at the same period the entire hemp industry is expected to generate
$26.6billion (Reporterlinker 2019).
Since 21st -century consumers generally exhibit high demand for quality and health benets for products
they buy (Sajdakowska et al. 2018), we took the case of the United States of America to illustrate how
increasing consumer awareness of HMs contamination in hemp could affect total estimated retail
revenue and found divergent pattern as follows. From Hemp Industrial Daily (HID) data (Fig.5a), we used
the yearly prediction upper and lower limits of estimated retail sales to generate average estimated
revenue and differential growth (ΔG) as follows:
Where ΔG – is differential growth over 5 years based on HMs dissuading impact on consumers
U – upper estimate retail sales
L – lower estimate retail sales and N – number of years covered by the prediction
Based on the average estimated retails (Fig.5b) assuming that consumers are less aware and concern
about HMs contaminated CBD-related products, an exponential economic return valued at about
$10.3billion by 2024 is expected, a margin decreased of $1.5billion than predicted by Hemp Industrial
Daily. This economic boom is only possible should the hemp industry retain the current consumer base,
leverage consumer enthusiasm and raise awareness for new benecial CBD-related products, and
prioritized consumer health within 2021 to 2025. By considering the differential growth (ΔG) in a scenario
where the consumer-base become aware of HMs contaminants, develops resentment and fewer new
consumer are attracted, the CBD total retail sales will slump to about $9.7billion (Fig.5b). This
represents a margin decrease of $2.1billion less than predicted by Hemp Industrial Daily at $11.8billion.
Although the cannabis CBD market had developed faster than the ber market, consumer awareness for
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HMs contamination could trigger a dramatic repurposing of HMs contaminated crop for bers-related
products at the farm level, causing a paradigm-shift in ber production.
Interestingly, it has been shown that HMs pollution in industrial hemp does not have any signicant
inuence on ber properties such as neness and tensile strength of single ber bundles (Linger et al.
2005). Based on mean values for HMs in bers (Pb = 2.8 ppm and Cd = 0.8 ppm) and in seeds (Pb = 0.8
ppm and Pb = 1.8 ppm) from Linger et al. (2005), and mindful of the Öko-Tex-Initiative-2000 for textile
contamination set for Pb (0.2–1.0 ppm), Ni (1.0–4.0 ppm) and Cd (0.1 ppm) will disqualify the use of
most industrial hemp bers produced in the USA to be used in the European Union textile industry. This
economic upheaval can be avoided by applying the proposed agronomic blueprints and developing
agronomic technologies such as breeding for heavy metal sensitive cannabis genotypes.
Based on these factors: (1) consumer-base awareness for HMs contaminated cannabis, and (2)
development of hempcrete and textile derivatives market, we forecast that ber retail trade will soar over
the cannabis oil market by 2023, and signicantly contribute towards the total estimated retail sales
(Fig.5C). This scenario will force consumable CBD-related products to enter a stationary phase in
economic return while the global cannabis bioeconomy will continuously grow as multiple governments
slowly relax production laws on cannabis species.
For the hemp industry to experience a global boom, information gaps between cannabis research,
production, and the consumer-base must be bridged by implementing some of these blueprints:
i. New hemp consumers should be attracted via reliable, transparent, and regulated marketing.
ii. Efforts towards building consumer condence should be intensied by testing, certifying, labeling,
and branding cannabis products as “
heavy metal-free
” specifying the actual concentration of HMs
such as As, Pb, Hg, Cr, and Cd against their permissible levels. Importantly, studies have shown that
consumers often rely on label displayed ingredients, expiration date, health information, and
environmental attributes in the purchasing-process (Prentice et al. 2019).
iii. Hemp education should be intensied at all levels spear-headed by top-tier universities.
iv. Heavy metal monitoring at the eld level and appropriate repurposing of hemp crop should be
promoted over the 0.3% THC threshold values which dene whether a cannabis plant should be
classied as hemp or marijuana.
v. New farmland in developing countries having low-level environmental pollution could be used for
cannabis-essential oil production or invest in hydroponics cropping system.
vi. The cannabis industry must invest in research that seeks to understand consumer perception of a
quality product.
vii. Promote hemp research on heavy metal metabolism and breed for the following cannabis strains: a)
heavy metal sensitive, b) heavy metal tolerant, and c) heavy metal resistant varieties and enable
knowledge transfer to growers.
Page 12/20
Conclusion Of The Matter And Future Directions
The intrinsic signatures of
Cannabis
species to bioaccumulate heavy metals (HMs) from the earth's crust
are substantially determined by their high tolerance, weedy propensities, phenotypic plasticity, and
adaptation in an ecological niche. Although HMs accumulation in cannabis seems to be useful for
phytoremediation, it does pose a threat from the consumer-base. Application of agronomic best practices
such as the choice of cannabis seed varieties, abiding by the industry standards, and choice farmland
can critically mitigate HMs contamination. The choice for farmland should include soil pH, nutrient levels,
pesticides, microbial communities especially
A. mycorrhizae
, and heavy metal content. It would be in the
interest of growers to avoid re outbreaks near their farms since their crops could absorb chemicals from
the re. At the retail level, growers must disclose information on the soil type based on data from soil
conservation services and such transparency should be made available to consumers when requested.
Cannabis plants grown for land remediation should not be repurposed for human and animal
consumption which might dissuade consumers in the long-term and trigger a slump in the global
cannabis trade.
Declarations
Acknowledgments:
We thank the different cannabis growers from Washington State, the USA for providing valuable insights
into the best agronomic practices for establishing cannabis species.
Competing Interests:
The authors have declared that no competing interests exist.
Author contributions:
Conceptualization, LB.; Methodology, LB.; formal analysis, LB.; writing–original draft preparation, LB.;
MQOA, PM, and DFJ.; writing – review and editing, LB., and JEK.; supervision, LB and JEK. All authors
have read and agree to the published version of the manuscript.
Data Availability:
All data supporting the ndings of this study are available within the article.
Ethics Approval:
No ethical approval was required except authors were above 21 years in handling the cannabis plant.
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Additional Information
Additional Information S1 is not available with this version.
Figures
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Figure 1
Bioaccumulation and distribution of heavy metals (Cd, As, Hg, Cr, and Pb) in the cannabis plant. The
constitutive uptake of HMs is associated with no phenotypic alterations at the moderate levels. Excessive
accumulation and stabilized contamination in the plant triggers an advent of oxidative outburst
manifested by severe leaf and stem disorder.
Page 18/20
Figure 2
Effect of pedoclimatic pH on bioaccumulation of cadmium (Cd), arsenic (As), mercury (Hg), and lead (Pb)
in hemp varieties. This graphic representation was produced by mining mean quantitative data (P < 0.05)
generated in Galić et al. (2019).
Figure 3
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Example of cannabis gland visualized with a stereoscope at 1000X showing glands bearing resin of
cannabinoids in a Sour-diesel strain of marijuana (THC > 0.3%). The homeostasis of heavy metals at the
level of cannabis trichome is still unknown.
Figure 4
Typical effects of non-essential heavy metals above the permissible level on the human body.
Hypothetically, the accumulation of HMs below the permissive levels represents a long-term risk factor for
several chronic medical conditions.
Page 20/20
Figure 5
Forecasting unforeseen effects of heavy metals and mycotoxins on industrial hemp. A) Hemp Industry
Daily predictions on estimated hemp-derived CBD sales for 2019-2024. B) Unforeseen repercussion based
on differential growth on total estimated hemp-derived CBD sales for 2019-2024 in situations of
consumer aversion caused by HMs contamination awareness. C) Prediction on the total estimated
market value for bers should mitigation strategies to counter HMs contamination in hemp-derived CBD
fails forcing growers to shift production to hemp bers. All dotted lines are trend lines of the displayed
phenomenon.
