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International Journal of Current Research and Review 

Scopus’ Review Article 

Role of Chromium Enriched Tobacco in the 
Occurrence of Oral Carcinogenesis 


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. 



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; 

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. 


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 

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 

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 

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 

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

And Mn 
High temp, O, 

Cru) MnO, Cr(V1) 

(Highly ——> E. i 
Damaged DNA 



of p53 

Human cell 

Failure to 


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

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 

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. 


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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