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These alterations can result from exposure to radiation and to chemical, biological, and genetic factors Table 16.2.For example, ionizing radiations, such as x-rays and g-rays, can produ

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Environmental Cancer

16.1 INTRODUCTION

Cancer refers to any of a group of diseases characterized by uncontrolled

growth and spread of abnormal cells In the scientific or medical community,

the term malignant neoplasm (tumor) is often used in place of cancer

Malignant tumors develop most commonly in major organs, such as the

lungs, liver, stomach, intestines, skin, breasts, or pancreas, but they may also

develop in lips, tongue, testes, or ovaries Cancer may also develop in the

blood-cell-forming tissues of the bone marrow (the leukemias) and in the

lymphatic system or bones

In recent decades there has been growing concern about the possible effects

of a large number of environmental toxicants on carcinogenesis As noted in

previous chapters, cancer incidence and mortality have increased dramatically

over the past century Researchers consider that there are two main reasons for

the observed increase: the aging of the population, and an increase of

carcinogens present in and released into the environment through human

activities Studies show that nearly 30% of the total mortality in many

industrialized countries is attributed to cancer In the U.S., cancer remains the

number-two killer, accounting for nearly one fourth of all deaths Despite the

recent decline in the mortality rate, the total number of cancer deaths continues

to rise as the elderly population increases For example, the death toll in the

U.S in 1980 was 416,509, in 1995 it was 538,455,1and it is estimated to be

556,500 in 2003.2

One of the most common characteristics of the development of a neoplasm

in an organism is the long period of time between the initial application of a

carcinogenic (cancer-causing) agent, or carcinogen, and the appearance of a

neoplasm The latency period varies with the type of carcinogen, its dosage,

and certain characteristics of the target cells within the host In humans, cancer

may not be manifested until at least 10 or more years after an initial exposure

to a carcinogen

16.2 CAUSES OF CANCER

Many factors can lead to cancer These factors include: diet, smoking, alcohol,

reproductive and sexual behavior, occupational hazard, geographical factors,

and environmental agents An estimate of the contribution of various agents or

life styles to the cause of cancers is presented inTable 16.1.It is notable that

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diet and smoking account for approximately two thirds of all cancers Smoking

is particularly implicated in lung and bladder cancers

Although there are many theories concerning the causes of cancer, the

fundamental principle underlying these theories is the alteration of the genetic

material of the cell, the DNA The various theories attempt to explain how this

change is brought about The DNA of a cancer cell is slightly different from

that of a normal cell This means that the sequence of the bases – adenine (A),

guanine (G), thymine (T), and cytosine (C) – in a given strand of DNA is not

the same as that of the bases in a normal cell As mentioned in Chapter 15,

these sequences dictate the sequences of the transcribed messenger RNA

(mRNA), which in turn specify the kinds of proteins to be synthesized in a cell

Alteration in the DNA base sequence in cancer cells results in abnormal

proteins These new proteins influence the mechanisms of growth control in

such a way that cell division continues indefinitely

As discussed in Chapter 15, several types of DNA damage can occur The

most common ones include: single- and double-strand breaks in the DNA

backbone, formation of crosslinks between DNA bases and between DNA

bases and proteins, and chemical addition to the DNA bases These alterations

can result from exposure to radiation and to chemical, biological, and genetic

factors (Table 16.2).For example, ionizing radiations, such as x-rays and

g-rays, can produce DNA single- and double-strand breaks and various forms of

damage to bases Ultraviolet (UV) light, which is a non-ionizing radiation, is

capable of producing dimers A variety of chemicals can cause DNA damage

through base alterations Alteration may be induced directly through

formation of adducts, or indirectly through intercalation formed by a chemical

between two bases Many electrophilic chemicals can react with DNA, forming

covalent additional products termed adducts For example, alkylating agents

can yield a reactive alkyl group that can react with base material, such as

guanine, to produce an adduct

Table 16.1 Speculative Proportion of Cancer Deaths Attributed to Various Factors

Factor or class of factors Percent of all cancer deaths

Reproductive and sexual behavior 7

Medicine and medical procedures 1

Source: Adapted from USDHHS, The Surgeon General’s Report on Nutrition and Health, U.S Government Printing Office, Washington, D.C., 1988.

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16.3 STAGES IN THE DEVELOPMENT OF CANCER

It is generally accepted that the pathway leading to carcinogenesis includes

three stages: initiation, promotion, and progression (Figure 16.1).3 Initiation

results from a simple mutation in one or more cellular genes that control key

regulatory pathways of the cell It requires cell division for the fixation of the

process Unlike promotion or progression, initiation is irreversible in a viable

cell.4The efficiency of initiation is sensitive to xenobiotic and other chemical

factors, and the stage can be altered by both endogenous and exogenous

factors For example, a variety of chemicals in different tissues can inhibit the

metabolism of a procarcinogen to an ultimate carcinogen (see Section 16.6),

thereby blocking the initiation process Initiators may also produce

trans-Table 16.2 General Classification of Carcinogenic Agents

Radiation Ultraviolet and ionizing radiations

Chemical Polycyclic aromatic hydrocarbons, aromatic amines and halides, benzene, vinyl

chloride, aflatoxin B 1 , urethane, asbestos, certain metals, diet, and tobacco smoke

Genetic Viruses

Biological Transgenesis by enhancer–promoter–oncogene constructs

F IGURE 16.1 Three stages of carcinogenesis.

Source: Adapted from USDHHS, The Surgeon General’s Report on Nutrition and Health, 1988.

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formed cells that can persist for the life-span of an individual without

producing cancer In such cases, the damaged gene in the transformed cells

remains recessive because the damaged gene does not express an abnormal

protein

Promotion results from the selective functional enhancement of signal

transduction pathways induced in the initiated cell and its progeny by the

continuous exposure to the promoting agent.4 This stage involves gene

activation, leading to the synthesis of the abnormal protein Rapid cell division

then occurs, which is accompanied by interruption of the organism’s normal

functions or health Promotion then leads to the expression of the genetic

changes as malignancy, which involves loss of control over cellular

prolifera-tion Examples of promoting agents include: saccharin, butylated

hydroxyto-luene, 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD, see Chapter 13), and

androgens and estrogens In contrast to initiation, promotion is reversible

Therefore, if the promoting agent is withdrawn well before tumors are

manifested, the appearance of tumors can be delayed or prevented

Furthermore, promotion may be continually modulated by various

environ-mental factors, including frequency with which the promoting agent is

administered, age and sex of the subject, hormonal balance, and composition

and amount of diet Research shows that many promoting agents exert their

effects on the cell through mediation of receptor mechanisms.5

Some chemicals act as both initiators and promoters Benzo(a)pyrene is

such a chemical In small doses it initiates genetic damage, and in higher or

repeated doses, it enhances promotion

Promoting agents involved in the onset of promotion do not cause cancer

by themselves; they only have a specific impact on an initiated cell Promotion

is gradual, and some of the earlier steps are reversible In the promotion stage,

abnormal proliferation of the affected cell occurs, presumably because of a

high concentration of growth factors or modified cell-surface receptors If the

damage to the gene is not drastic, most of the normal components of the cell

will be produced and will be responsive to normal growth-inhibiting factors

Experiments with animals suggest that the time lapse between initiation and

promotion is not critical During the latter stage of promotion, however,

cumulative genetic changes occur, leading to totally irreversible neoplastic

transformation

Progression results from continuing evolution of an unstable karyotype

This stage usually develops from cells in the stage of promotion, but, in certain

conditions, it may develop directly from normal cells The critical molecular

characteristic of this stage is karyotypic instability, and morphologically

discernible changes in cellular or genomic structure occur.4 Furthermore,

benign or malignant tumors may be observed in this stage The growth of

altered cells is sensitive to environmental factors during the early phase of

progression

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16.4 METASTASIS

The most fearsome aspect of cancer is the spread of malignant cells from the

primary site to other parts of the body – a process called metastasis This is the

late stage of the disease and is characterized by invasive activity and the

appearance of a variety of cancer-cell types Some of the cells that have the

inherent ability to detach from the primary site eventually travel via the blood

or lymph to start a secondary tumor at another site Metastasis is the primary

cause of the failure of treatment in cancer patients The extent of the

dissemination of the malignant cells is determined by the physiological

condition of the host During metastasis, continuous changes occur in the

tumor, and the function and behavior of the tumor cells in the late stage are

quite different from those in the early stage Most frequently, the location of

metastasis is in the organ or organs that are served by blood vessels from the

original cancer site Notably, growth and survival of a tumor require

nourishment, which is provided by new blood vessels near the tumor site

16.5 CLASSIFICATION OF CARCINOGENS

Carcinogens are divided into two groups: Part A and Part B (based on a list

prepared by the U.S National Toxicology Program, see Appendix 3) Part A

refers to those agents that are ‘‘Known to be a human carcinogen,’’ whereas

Part B refers to those that are ‘‘Reasonably anticipated to be a human

carcinogen.’’ Examples of carcinogens belonging to Part A include: aflatoxins,

inorganic arsenic compounds, asbestos, benzene, beryllium, coal tars, dioxin,

diethylstilbestrol, tobacco smoking, steroidal estrogens, nickel compounds,

radon, vinyl chloride, and UV radiation (see Appendix 3, Part A) More than

one hundred agents are included in Part B (see Appendix 3, Part B)

As noted earlier, the basic changes in DNA that can lead to cancer, i.e.,

mutation, can be caused by many agents These agents are generally divided

into four categories: radiation, chemical, biological, and genetic (Table 16.2).3

Although mutation does not necessarily result in cancer, cancer occurs if the

proteins that are produced following mutation affect cellular growth-control

mechanisms The following section discusses in some detail the agents that can

cause DNA damage Emphasis is placed on radiation and chemical agents

16.5.1 RADIATION

The process involved in radiation-induced DNA damage is complex and has

received much attention over many years As noted previously, ionizing

radiation produces a wide variety of DNA lesions, including various base

modifications, strand breaks, and DNA-protein crosslinks.6It was mentioned

in Chapter 15 that absorption of short-wave UV radiation by DNA causes

breakage in its strands, the opening of the rings of its bases, and the formation

of thymine dimers

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UV radiation is the main cause of skin cancer Increased UV radiation

exposure– much of it is caused by sunbathing or tanning under a UV lamp – is

the main contributing factor to the rising incidence of skin cancer worldwide

UV radiation induces formation of free radicals, especially reactive oxygen

radicals Of the three types of UV radiation (UV-A, -B, and -C), UV-B is the

most harmful type UV-B (which has a wavelength of 280 to 320 nm) is

attenuated by the earth’s ozone layer Several other factors modulate the

amount of UV radiation to which people are exposed, including time of day,

season, humidity, and distance from the equator Skin cancer risk is also

affected by skin type; fair skin that freckles or bumps easily is at more risk than

very darkly pigmented skin People who live in sunny climates and have red or

blond hair and blue or light-colored eyes are at especially high risk

Among the photochemical reactions that take place when UV-B penetrates

the skin is mutation of the DNA in skin cells Humans have repair enzymes

that can correct this damage, but mutations accumulate as the individual ages

An individual’s lifestyle may also cause the repair system to eventually become

overtaxed, resulting in skin cancer Most researchers stress that the damage

begins accumulating early – in childhood; by young adulthood about 50% of

lifetime sunlight exposure may have already accumulated

16.5.2 CHEMICALCARCINOGENS

The association between exposure to chemicals and cancer incidence was first

reported in 1775 by the English physician Percivall Pott, following the

observation of scrotal cancer in chimney sweeps.7 With an increase in

European industrial development during the 19th century, high rates of skin

cancer were observed among workers in the shale oil and coal tar industries In

1915, a group of Japanese scientists conducted experiments in which they

painted rabbits with coal tar and induced tumors This led to the knowledge

that the compounds contained in the coal tar could produce cancer in animals

Several groups of organic compounds have now been recognized as

carcinogenic to laboratory animals These include polycyclic aromatic

hydro-carbons (PAHs), aromatic amines, aminoazo dyes, nitroso compounds,

benzene, and vinyl chloride.8

Many chemical agents that may be found in foods are also known to cause

cancer For example, aflatoxin B1, which causes liver cancer in several species

of test animals, is produced by Aspergillus flavus found in contaminated peanut

or cottonseed meal There are also naturally produced substances that are

carcinogenic

A number of inorganic substances have also been shown to induce cancer

These include some salts of arsenic (As), beryllium (Be), cadmium (Cd),

chromium (Cr)(VI), nickel (Ni), and lead (Pb) It should be pointed out that

some of these metals are essential nutrients for humans and animals Trivalent

Cr (Cr3þ) is one of these metals As part of the glucose tolerance factor, Cr

plays an important role in maintaining normal glucose metabolism in

mammals

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Several chlorinated hydrocarbons and other chemicals have been identified

as carcinogenic These include 2,4-D, DDE, hexachlorocyclohexane,

poly-chlorinated biphenyls (PCBs), and polychlorinated dibenzo-p-dioxins

(PCDDs) (see Chapter 13)

16.6 METABOLISM OF CHEMICAL CARCINOGENS

As shown in Figure 16.1, chemical carcinogens are divided into two broad

classes: direct carcinogens and procarcinogens Direct carcinogens are usually

electrophiles, such as Hþ

, Cþ , Nþ , and can react readily with nucleophiles, such as proteins and nucleic acids The main sites in these molecules where such

reactions can occur are S, ¼N–, –C–OH, or –P–OH Examples of cellular

nucleophiles include some amino acids, such as methionine, cysteine, histidine,

tryptophan, and tyrosine, and nucleic acid bases, such as adenine (N-1, N-3)

and guanine (C-8, N-7, O-6) Procarcinogens are those agents that require

biologic activation before becoming ultimate carcinogens Compared with

direct carcinogens, procarcinogens are relatively stable, and so many people

may be environmentally or occupationally exposed to them It is possible for

people to ingest or absorb some procarcinogens, after which enzymes in the

liver, lungs, or other organs convert them to their activated metabolites

It is thought that most, and probably all, chemical carcinogens are

converted by metabolism into electrophilic reactants that exert their biological

effects by covalent interaction with DNA Some examples of these reactants are

shown inFigure 16.2.Several of these chemicals are discussed in some detail in

the following sections The discussion will focus on free radicals, DDT, vinyl

chloride, nitrosamine, benzo[a]pyrene, and halogenated aromatic

hydrocar-bons

16.6.1 FREERADICALS

Reactive oxygen species, such as hydroxyl radicals (OH), are produced during

the enzymatic and chemical reactions of molecular oxygen in cells Hydroxyl

radicals are also produced when cells are exposed to ionizing radiation, tumor

promoters, and chemical carcinogens As mentioned earlier, reactive oxygen

species can cause various lesions in DNA, by inducing damage to nucleic acids

and altering their structures and function Oxygen-induced lesions of nucleic

acids include strand breaks9and base modification products Alternatively, the

OH free radical, formed through the reaction between superoxide free radical

(O2  

) and H2O2 (Reaction 16.1), is unique and can induce breaks in the phosphodiester bonds Both single- and double-strand breaks can occur In

addition, the free radical can abstract H-atoms from the DNA helix.10

O2 þH2O2!O2þHOþHO ð16:1Þ

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16.6.2 DDT

DDT is one of the several pesticides that have been added to the long list of

cancer-causing agents present in the environment According to a report by the

National Cancer Institute, women with high exposures to DDT may have a

greater risk of developing breast cancer Researchers at Mt Sinai Hospital in

New York City have found that women with blood levels of DDE (see Chapter

13) of 19 ng/ml have four times the risk of breast cancer compared with women

with levels of 2 ng/ml

It is suggested that DDE may cause breast cancer in two ways: it may

induce cytochrome P450 enzymes, thereby altering the metabolism of

toxicants, or it may act as an estrogen mimic and as such may disrupt

the endocrine system through interaction with estrogen receptors (see

Chapter 14)

F IGURE 16.2 Some examples of chemical carcinogens.

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16.6.3 VINYLCHLORIDE

Vinyl chloride, the common name for monochloroethene (CH2¼CHCl), is

one of the most widely manufactured organic chemicals in the U.S Vinyl

chloride is a gas at ambient temperature, with a boiling point of 14C, and

exhibits a low solubility in water While the vinyl chloride monomer itself is

rarely used, it is polymerized with itself and other organic compounds to

form many products, making it a very important chemical to industry and to

consumers

Among the many polymers that are derived from vinyl chloride, polyvinyl

chloride (PVC) is the most common PVC, as a solid material, is extremely

adaptable and cost effective, and is used in numerous construction materials,

home furnishings, packaging materials, automobile products, etc Some

examples of the products made of PVC are water pipes, raincoats, credit

cards, wire coatings, and food packaging

PVC production involves three stages: synthesis of vinyl chloride monomer

from petrochemicals and chlorine, polymerization of vinyl chloride into PVC

resin, and PVC fabrication Environmental contamination occurs from these

processes, although the extent of it varies with each stage The contamination

includes emission of vinyl chloride into the atmosphere, and surface and

groundwater contamination resulting from sludge and wastewater discharge

Vinyl chloride has been shown to be both mutagenic and carcinogenic It is

classified as a Part 1 carcinogen because sufficient evidence exists that the

compound is carcinogenic to humans This is highly important because only

about 40 chemicals or chemical mixtures are classified as such.11Vinyl chloride

causes liver cancer in both humans and laboratory animals However,

laboratory experiments with mice showed induction of not only liver cancer

but also cancers of bone, skin, lung, brain, nephron, and mammary tissues.11,12

In humans, vinyl chloride exposure may occur both occupationally and

non-occupationally

Vinyl chloride is metabolized by the hepatic cytochrome P450 enzymes to

the carcinogenic epoxide form Studies show that this metabolite is an ultimate

carcinogen It reacts with DNA, causing it to change its function In the liver,

the active epoxide may be further converted to chloroethane aldehyde A

molecule of glutathione can conjugate the aldehyde and the resultant conjugate

may then be excreted (Figure 16.3)

16.6.4 ALKYLATINGAGENTS

As noted in Chapter 15, alkylating agents are those chemicals that can react

with DNA to produce alkylated DNA adducts Several groups of organic

compounds can be metabolized to alkylating agents An example is N-nitroso

compounds, which consist of nitrosamines and nitrosamides Nitroso

com-pounds are found in various types of food, particularly meat and meat

products (e.g., fried and cured meat products) and cheese Small amounts of

the compounds have been shown to occur in beer, and tobacco smoke contains

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varying amounts Industrial exposure to N-nitrosamines accounts for another

environmental source Occupation or industrial activities that may lead to

exposure include metal cutting and rolling, leather tanning, rubber

manufac-ture, handling of hydraulic fluids, and producing or using amines in the

chemicals industry In these activities, exposure is mostly via air and skin.13

The importance of nitrosamines as environmental carcinogens was first

postulated in 1962 Subsequent studies demonstrated the endogenous

forma-tion of such compounds from precursor amines and nitrite in vivo The

endogenous formation of N-nitroso compounds from precursor amines and

nitrosating agents, particularly nitrite, is unique among the various chemical

carcinogens Nitrosatable amine precursors, such as secondary and tertiary

amines, are natural constituents of food or contaminants of food, such as some

pesticides that can be nitrosated Nitrite is the most important nitrosating

agent and is present in some food products However, nitrite can also be

formed from nitrate in saliva and possibly in the intestines The pathway

leading to the formation of an alkylating agent from dimethylamine is

presented in Figure 16.4 The first step is nitrosation in which dimethylamine

reacts with nitrite to form dimethylnitrosamine, a nitroso compound

Metabolism of dimethylnitrosamine leads to the formation of a CH3þradical,

which can react with DNA, resulting in methylated DNA

F IGURE 16.3 Metabolism of vinyl chloride by the cytochrome P450 system.

F IGURE 16.4 Activation mechanism of dimethylamine.

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