Role Of Chromium Enriched Tobacco In The Occurrence Of Oral Carcinogenesis

International Journal of Current Research and Review

Scopus’ Review Article

Role of Chromium Enriched Tobacco in the
Occurrence of Oral Carcinogenesis

DOI: http://dx.doi.org/10.31782/IICRR.2020.121823

ete ar Smrutipragnya Samal’, Priyanka Debata2, Santosh Kumar Swain?

Sci. Journal Impact

Factor: 6.1 (2018) ‘Department of Otorhinolaryngo logy, IMS and SUM Hosp ital, Siksha O Anusandhan (Deemed to be Univers ity), Bhubaneswar, Odisha,

eee (ee) India; *Department of Oral Pathology and Microbio logy, IMS and SUM Hosp ital, Siksha O Anusandhan (Deemed to be Univers ity),

© OKS Bhubaneswar, Odisha, India.

BY NC
Copyright@IJCRR

ABSTRACT

Cancer is a disease of major concern grasping the entire globe. It is one of the diseases characterized by high rates of incidence
and mortality. Among all the cancer types, oral cancer has a high occurrence in countries like India, where people are more
inclined towards the use of tobacco either for smoking or for chewing purpose. Nicotianatabacum being a hyperaccumulator
plant can thus accumulate high amount of heavy metals in its parts, mostly leaves. The carcinogenicity of tobacco may be linked
to the high concentrations of metals present in it. The presence of chromium in the trivalent or Cr(III) form in the leaves of the
tobacco plant is ignored assuming it to be non-toxic. However, smoking or chewing tobacco can lead to the conversion of Cr(III)
to the toxic Cr(VI) as hypothesized in the current review. The paper in its current form discusses the process of aggregation of
chromium in the above-ground parts of the tobacco plant. The rhizospheric factors that promote the metal uptake by the plant
are also discussed. The notion that Cr in tobacco is harmless has been argued upon. The paper proposes the role of Cr enriched
tobacco in causing oral cancer and predicts the probable underlying mechanism. It emphasizes on the need to regulate rhizos-
pheric factors, to prevent the accumulation of high concentration of the toxic heavy metal in the biomass of the tobacco plant.

Key Words: Cancer, Chromium, Heavy metal, Mutation, Rhizosphere, Tobacco

INTRODUCTION Tobacco has been reported to contain high levels of met-

al possibly resulting in an increased risk of exposure of

Cancer is one of the leading global diseases responsible for these toxic components to the smokers and consumers of
high incidence and mortality rates. In terms of the number various products of smokeless tobacco. The toxic effect of
of deaths, it lies second only to cardiovascular disease ac- these carcinogenic metals present in tobacco depends on

counting for 16% of mortality (Fig.1). As per the 2018 GLO- the dose and the time of exposure. These toxic metals and
BOCAN statistics, one out of five males and one out of six metalloids present in tobacco are poorly studied and the

females are found to suffer from cancer, while one out of mechanism behind their toxicity remains unexplained .°

eight males and one out of eleven females die of the disease. ! Among several chemical compounds present in tobacco,
Cancer of the lip and oral cavity is the second most common 11 of these are metals or metalloids. An expert panel on
cancer in India as far as the incidence (10.4%) and mortality tobacco regulation constituted by WHO prioritized four of
rates (9.3%) are concerned.* Oral cancer is caused due to ad- the heavy metals like nickel, cadmium, arsenic, and lead
diction habits and Human Papilloma Virus (HPV). However, in tobacco and tobacco smoke as of serious concern.’ The
majority of oral cancer in India is caused due to consumption tobacco constituents are mostly related to several diseases
of tobacco products either in form of smoking or non-smoke especially cancer.

forms and account for 80-90% of cases.* “Indian Council of

Medical Research (ICMR) has reported that 30% of all can- Chromium is a toxic heavy metal present in tobacco but its
cers in India are mainly caused due to tobacco. Among the role in carcinogenesis 1s poorly understood and therefore
tobacco linked cancers, oral cancer is the most frequent type 1gnored. The current review explains the probable role of

in India and is responsible for approximately 42% of deaths hexavalent chromium generated from tobacco consumption
ey ee and smoking in oral carcinogenesis. The authors have put

Corresponding Author:

Prof. Santosh Kumar Swain, Professor, Department of Otorhinolaryngology, IMS&SUM Hospital, Siksha O Anusandhan (Deemed to be
University), Kalinga Nagar, Bhubaneswar-751003, Odisha, India; Cell: +91-9556524887; Email:santoshswain@soa.ac.in

ISSN: 2231-2196 (Print) ISSN: 0975-5241 (Online)
Received: 12.06.2020 Revised: 18.07.2020 Accepted: 20.08.2020 Published: 22.09.2020

Blatt onan ee Sa —
Int J Cur Res Rev | Vol 12 + Issue 18 » September 2020

Samal et al.: Role of chromium enriched tobacco in the occurrence of oral carcinogenesis

forward a hypothetical model predicting the possible path-
way of Cr(VI) involvement in oral carcinogenesis.

Figure 1: Two leading diseases with the highest global mortal-
ity rate.

Chromium in oral carcinogenesis

Chromium, unlike other toxic heavy metals, is available in
several oxidation states, out of which, the trivalent or Cr(III)
and the hexavalent or Cr(VI) are the two highly stable
forms.*Cr(VI) is considered to be a carcinogen because of its
several toxic effects on the living biota including humans.””°
Chromium remains a chief constituent of tobacco. It is most-
ly found in the trivalent form in tobacco products and there-
fore 1s not regarded as toxic. However, the inter-conversion
of Cr in tobacco smoke and non-smoke form and its role in
carcinogenesis has been poorly understood.

Sources of Cr in the environment

Cr mainly occurs from two sources — natural and anthro-
pogenic (Fig.2). Cr occurs naturally over the earth crust in
rocks, soil, water streams, and volcanic dust. It generally re-
mains as Cr(III) bound to primary rocks and other metal ox-
ides like iron.'' Anthropogenic sources are mostly responsi-
ble in increasing the toxic load of Cr(VI) in the environment
and can be further categorized into direct and indirect sourc-
es. The direct sources include industrial operations like min-
ing, leather tanning, chrome plating, wood preservation, and
production of paints, pigments, dyes, paper, and pulp. Water
treatment plants, Portland cement, dumping of wastes and ef-
fluents, incineration of wastes, coke ovens, and cooling tow-
ers are some of the indirect sources ofenvironmentalCr(VI).””
Dumping of Cr rich solid and liquid wastes mainly contrib-
ute towards environmental toxicity.

Anthropogenic
Sources

Natural Sources

Figure 2: Sources of chromium (Cr) in the environment.

Cr(VI) and human carcinogenicity

The chemical structure of Cr(VI) plays a major role in facili-
tating its entry into human cells and thereby causing toxic
effects(Fig.3). Cr(VI) mostly exist in the form of oxyanion
(CrO,) which structurally resembles that of sulphate oxy-
anions (SO,). This structural resemblance allows Cr(VI) to
use sulphate transporters present on the cell surface to enter
the cells.'*Cr(VI) is mutagenic to human cells and is respon-
sible for causing genotoxicity. It leads to the formation of
DNA adducts which includes DNA-proteins crosslinks and
DNA-aminoacids crosslinks’? which in turn inhibits DNA
replication process.Cr(VI) also creates genomic instability
by causing double-strand DNA breaks'®. Cr(VI) causes epi-
genetic silencing, mutations, thereby leading to loss of mis-
match repair mechanism!“ The toxic form of the heavy metal
induces chromosomal instability and abnormalities thereby
causing DNA lesions'’. Cr(VI) has been found to alter gene
expression and actively induce the development of cancer
through several mechanisms. It has also been found to ac-
tively participate in DNA methylation and gene silencing
thereby leading to several types of cancer'®. Cr(VI) is also
believed to have a certain influence on microRNAs. The mi-
croRNAs play an active role in gene regulation and are often
found to be dysregulated in Cr(VI) carcinogenesis thereby
affecting important biological processes’”””.

Chromium in Tobacco: Nicotianatabacum as a
metal accumulator

Plants can uptake essential elements from the soil and utilize
them as nutrients. However, certain plants can aggregate high
metal concentrations in their biomass and are referred to as
hyperaccumulators’*. Such plants are used to clean up soils
contaminated with heavy metals by the process known as phy-
toremediation *'. Similar metal accumulation ability by Nico-
tianatabacum plant makes it a viable option for metal removal
from contaminated soils. However, such ability of the tobacco
plant becomes a threat to health. Nicotianatabacum can up-
take several heavy metals from the soil which includes cadmi-
um, aluminium, arsenic, chromium, nickel, copper, zinc, lead
and mercury. These metals are uptaken by the roots and then
translocated and stored in the above-ground parts of the plant,
mostly leaves. Cr is mostly up taken from the soil and trans-
located to aerial parts of the tobacco plant in its hexavalent
state. The transport of Cr(VI) from roots to shoot is an active
process and occurs through sulphate or phosphate channels”.
Once Cr(VI) reaches the leaves, it gets reduced to Cr(III) by
binding to specific ligands and sequestered into leaf vacuoles”
of the tobacco plant where it is stored as Cr(III).

Chromium accumulation and factors governing
its bioavailability for uptake

Accumulation of Cr(VI) in hyperaccumulator plants like Ni-
cotianatabacumis highly dependent on several rhizospheric

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Samal et al.: Role of chromium enriched tobacco in the occurrence of oral carcinogenesis

soil factors like redox potential, pH, organic content, and
availability of suitable microorganisms *.

The redox potential (Eh) of soil provides idea on the oxida-
tion and reduction nature of the soil and plays a pivotal role
in bioavailability and speciation of Cr( VI) in the soil. At high
soil Eh values, generally, an oxidation reaction occurs*>”°.
Soils with high Eh values can cause the Cr(II) present in the
soil to get oxidized to highly mobile Cr(VI), thereby increas-
ing its availability in the soil for uptake by the plant.

Soil pH also is an important factor in metal availability to
plants. Metals are highly soluble and mobile in acidic pH and
are precipitated over alkaline soil conditions”. However, the
same does not apply to Cr and its bioavailability under varied
pH conditions depends on the form in which it is present in
the soil. Cr(VI) mostly exists in the anionic form (CrO,” and
HCrO,’) in the soil. Its bioavailability and mobility increas-
es under high pH conditions and the reverse happen at low
pH. At high pH, the hydroxyl ions increase providing the soil
with a net negative charge and thereby decreasing sorption
of Cr(VI) ”.

Soil organic matter content also plays a vital role in the
movement and availability of Cr(VI) 7’. Presence of soil or-
ganic matter lowers the soil pH making it acidic and thus
increasing H* ion concentrations. This positive charge of the
soil helps in retention or adsorption of Cr(VI) to soil ma-
trix °°. Moreover, organic matter creates a reduced condition
in the soil and also favours the growth of microorganisms.
Therefore, Cr (VI) 1s reduced in two different ways cata-
lysed in the presence of soil organic content. Firstly organic
content of the soil creates reduced conditions that directly
reduces Cr(VI) to Cr(III)*'. Secondly, it favours microbial
growth indirectly leading to reduction of Cr(VI) to Cr(III)
as a result of biotic interaction between the microbes and the
heavy metal ??.

The rhizosphere soil due to its high nutrient concentration
forms a favourable habitat for the growth of microorganisms.
The microorganisms mostly bacteria have been found to play
a major role in enhancing soil fertility and sustaining plant
growth by processes such as mineralization, decomposition,
nutrient immobilization, and nitrogen fixation *°. As far as
the biogeochemical activity of heavy metals in the plant-soil
rhizosphere is concerned, microbes indeed play an influen-
tial role ** *°. Several groups of microorganisms having the
ability to reduce Cr(VI) to Cr(III) have been identified *°.
These include bacteria °*’, algae*®, fungi”, and yeast“. Micro-
bial reduction of Cr(VI) to Cr(III) highly relies on the micro-
bial strain, concentration of chromium, pH, and temperature
of the soil*!*.

Soil conditions like high redox potential, high pH, low or-
ganic content, and high soil temperature are the driving force
for successful accumulation of Cr(VI) by tobacco plant and
need to be regulated accordingly.

Cr(VI) rich tobacco in oral cancer: A hypoth-
esized model

Chromium is a chief constituent in tobacco which may be at-
tributed to the hyperaccumulation ability of the tobacco plant
under favourable conditions. Cr is found in the trivalent form
in tobacco and therefore not considered to be toxic by several
researchers. The authors in the current review however have
put forward contrasting views. The manuscript in its current
form strongly advocates the probable involvement of Cr(VI)
rich tobacco in oral cancer. A hypothetical model explain-
ing the probable mechanism underlying oral carcinogenesis
due to the presence of chromium in tobacco has been put
forward.

The tobacco plant has been known to accumulate heavy met-
als like Cr in its aerial parts, mostly leaves. The leaves of the
plant accumulate the heavy metal in its trivalent (non-toxic)
form. Therefore, Cr(III) is not considered as a carcinogen
in tobacco. However, there is always a chance that the non-
toxic Cr(III) may get oxidized to the toxic Cr(VI) under fa-
vourable conditions thus promoting carcinogenesis. Cr(II)
and Cr(VI) are the two most stable states of Cr that can inter-
change their oxidation states by undergoing redox reactions
under conditions like metal content, presence of oxygen, high
temperature, and moisture. Tobacco leaves in addition to Cr
also contain manganese (Mn) which further oxidizes the less
toxic Cr(III) to the highly toxic Cr(VI). During smoking of
tobacco, the Cr(III) present in it may get oxidized to Cr(VI)
due to the combustion of tobacco that involves oxygen and
high temperature. Moreover, tobacco smoke when inhaled
through mouth or nose gets mixed up with moisture thereby
also leading to the formation of Cr(VI). Cr(VI) toxicity not
only spreads from tobacco smoke but also smokeless forms.
Tobacco, when taken in chewable form, gets in contact with
oxygen and moisture thereby converting the elemental man-
ganese present in it into MnO,, that catalyses the oxidation
of Cr(II) to Cr(VI)(Fig.3).

Heavy metal
accumulator

. | ae Rich in Cr(VI)
Rich in Cr ®©-
ana tobaccum)

And Mn
(Nicoti
High temp, O,
Moisture

—
Cru) MnO, Cr(V1)

Cr(V1)
(Highly ——> E. i
Soluble)
Damaged DNA

TT
+

Suppressor

of p53
ead
ee

Human cell

Failure to

CANCER

Figure 3: Mechanism underlying role of chromium enriched
tobacco in causing oral cancer

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Samal et al.: Role of chromium enriched tobacco in the occurrence of oral carcinogenesis

The oral cavity being the first point of contact of both smok-
ing and non-smoking form of tobacco products 1s hence more
exposed to Cr(VI) and most probably its toxic impacts like
the occurrence of oral cancer. Cr(VI) being highly mobile
and permeable easily passes through the human cell mem-
brane. Cr(VI) generated from cigarette smoke or chewing of
tobacco can easily get absorbed into the squamous epithe-
lial cells present in the internal surface of the oral cavity.
Once Cr(VI) enters into the cells, it undergoes detoxifica-
tion. Cr(VI) either gets reduced to Cr(II) directly or indi-
rectly in a stepwise manner. In the indirect reduction process
Cr(VI) gets converted to Cr(III) via several intermediates
like Cr(V) and Cr([V). During the reduction, the different
species of chromium produce intracellular reactive oxygen
species (ROS). Chemical compounds present in the cells like
ascorbic acid and glutathione act as ROS scavengers thereby
reducing Cr(VI) to Cr(III) and in the process lead to the pro-
duction of free radicals (hydroxyl radicals) #. Production of
hydroxyl radicals inside the cells occurs in the presence of
H,O, through a Fenton-like reaction “. ROS in the form of
hydroxyl radicals can activate various pathways like apopto-
sis #. Cr(VI) reduction inside the cells can also directly cause
damage to the DNA by interacting with the proteins, amino
acids, and even the DNA directly leading to single or double-
strand breakage*. Cr(VI) after reduction to Cr(III) can form
bulky binary and ternary DNA adducts, thereby causing se-
vere damage due to mutations *.

Cr(VI) induced oxidative damage mostly occurs to the DNA
of p? gene*® present in the oral squamous cells thereby af-
fecting the gene function. Being a tumour suppressor gene,
př works as a control centre of the cell and regulates the
activity of several genes under stress conditions and also is
involved in DNA repair. Damage to this gene leads to fail-
ure of repair mechanism in DNA of the oral epithelial cells,
thereby resulting in mutations, uncontrolled cell division and
finally cancer of the oral cavity.

CONCLUSION

Tobacco consumption remains a significant threat to public
health around the world and smoking-related diseases are
considered the world’s most preventable cause of death.

Consumption of tobacco causes a significant threat to pub-
lic health. Tobacco-related diseases are linked to the world’s
most prevalent cause of death. Tobacco has several carcino-
gens. Chromium has a strong link with the carcinogenesis
of oral cancer.Cr(VI) is a toxic heavy metal that arises from
several anthropogenic activities. Nicotianatabacum is a plant
hyperaccumulator that can easily accumulate heavy metals
like Cr(VI) in large quantities from contaminated soil and
water bodies. This is the main reason behind the presence
of the toxic heavy metal in tobacco and tobacco products.

Being a major component of tobacco, Cr(VI) has all the pos-
sibility of causing oral cancer by bringing about DNA muta-
tions in the p? and other linked genes. The author(s) hereby
advises preventing the accumulation of the toxic Cr(VT) in
tobacco plant that is meant for commercial purposes to pre-
vent the risk of oral carcinogenesis. This could be achieved
by appropriately regulating the rhizospheric factors govern-
ing its uptake by the tobacco plant.

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