C H A P T E R
25
Metal Toxicology in Developing Countries
BRUCE A. FOWLER, CANDACE M. PRUSIEWICZ, AND MONICA NORDBERG
ABSTRACT
Environmental health problems associated with
­ etals in developing countries are complex and
m potential public health problems to populations in
­frequently severe. They relate to the mining of min-
eral deposits in these countries, the smelting of
metal-­containing ores, and the secondary smelting of
batteries and electronic waste products transported
into these countries for recycling. Despite efforts in
the international community to promote sustain-
able development, these activities are frequently con-
ducted in developing countries under conditions of
limited health and safety regulation due to the limited
resources available to implement environmental and
occupational health standards in many developing
countries. Poor nutrition and a general lack of food are
also contributory factors that exacerbate susceptibility
to metal toxicity. These issues are further compounded
by metal contamination of food crops through the
utilization of cadmium-containing phosphate fertil-
izers, arsenic in irrigation water from contaminated
groundwater, and other metals or chemicals from
industrial or municipal wastewater sources. The econ-
omies of developing countries are often highly depen-
dent on the mining, smelting, and recycling of metals,
as well as on agricultural products, so tighter regula-
tion of ongoing practices is frequently a secondary
concern. This multiplicity of factors combines to create
an overall situation that frequently places populations
in developing countries at an elevated risk of adverse
public health outcomes from metal exposures. How-
ever, it also should be noted that, given the increased
globalization of industries and the food supply, metal
Handbook on the Toxicology of Metals 4E
http://dx.doi.org/10.1016/B978-0-444-59453-2.00025-1
contamination of the environment in d ­eveloping
countries with ­aeolian transport of metals in the atmo-
sphere, ocean currents, and food may also present
developed countries. For these reasons, the issues dis-
cussed in this chapter are generic and global in nature.
1 INTRODUCTION
This chapter deals with metal toxicology in
­ eveloping countries. Efforts to stimulate sustainable
d
­economic development in countries around the world
were forged by the United Nations (UN) during the
preparation for the 1992 Conference on Environment
and Development in Rio (UNCED, 1992), and resulted
in the Rio declaration signed by EU member states and
several developing countries at that time. S­ ustainable
development requires providing production condi-
tions with high occupational health standards, appli-
cation of a high degree of recycling of materials,
minimizing the use of fossil fuels and high demands
on ­environmental emission control. Such development
has been the goal for the countries that signed the Rio
declaration. One of the principles is that transfer to
other states should be limited of any activities or any
substances that may be harmful to the environment or
human health. The desirability of sustainable devel-
opment has been recognized not only by those who
signed the Rio declaration but by most other UN coun-
tries as confirmed in the Rio+20 declaration of 2012,
signed by EU member states, China, Russia, Japan, and
the United States, in addition to developing countries.
529 Copyright © 2015 Elsevier B.V. All rights reserved.
530 Bruce A. Fowler, Candace M. Prusiewicz, and Monica Nordberg
The term “developing country” is often taken to mean
countries with the lowest economic level, but prob-
lems related to metal toxicology often occur during
the transition phase from low to medium economic
development. Hence, newly industrialized countries
will also be discussed in this chapter.
2  OVERVIEW OF PUBLIC HEALTH
PROBLEM AREAS
Public health problems associated with metals that
were originally identified in the industrialized and cur-
rently highly developed countries have in more recent
years reappeared in developing countries and newly
industrialized countries. The causes are complex and
relate to global geographic shifts from developed to
developing countries of both the production and refin-
ing of metals and the recycling of metal-containing
products, such as batteries and electronic devices. These
activities are frequently conducted under limited safety
conditions because awareness of environmental issues
is low and many developing countries have limited
resources for the implementation of environmental or
occupational health standards. Dietary insufficiencies
are frequently also factors that increase susceptibility to
metal toxicity. The inadequacy of a stable food supply
is sometimes compounded by the utilization of phos-
phate fertilizers that may be contaminated by metals,
such as cadmium, and irrigation water that contains
arsenic from groundwater or other metals/chemicals
in wastewater from industrial or water treatment facili-
ties. The economies of these countries are often highly
dependent on the mining, smelting, and recycling of
metals, but tight environmental regulation is some-
times lacking. There is a growing body of information
that developing countries, such as Africa, are experienc-
ing elevated burdens of cancer rates (­McCormack and
Schüz, 2012), as well as other adverse health outcomes
related to chemical exposures (Nweke and Sanders,
2009; Chatham-Stephens et al., 2013; Caravanos et al.,
2013) associated with industrialization and exposure
to hazardous wastes. ­Caravanos et al. (2013) reported
reduced pediatric IQ scores in seven Asian countries
as a result of lead exposure (from a total of 169 sites).
The IQ reductions ranged from 4.94 to 14.96, which
are clearly major cognitive impacts. Other studies by
­Chatham-Stephens et al. (2013) on waste sites in India,
Indonesia, and the Philippines reported Disability
Adjust Life Year data (DALYs) related to toxic pollut-
ants in total of 373 toxic waste sites in these three coun-
tries. Lead and chromium accounted for over 99% of the
total DALYs, which were in the same calculated range
as outdoor air pollution and malaria in these countries.
The UN Commission on Sustainable Development
in their 18th Session (2010) pointed out that mining in
small island developing states occurs in Jamaica (Al),
Guyana (Bauxite, Au), Suriname (Al, Au), Dominican
Republic (Ni), Cuba (Ni), and Papua New Guinea (Cu,
Au). Artisanal gold mining operations in Guyana, Suri-
name, and Papua New Guinea still use the mercury
amalgamation method, which leads to adverse health
effects among workers and environmental contami-
nation. Moreover, it is estimated that 30% of artisanal
small-scale mining workers in these countries are chil-
dren. Indigenous communities have been particularly
vulnerable to the disruptive effects of mining. Gov-
ernments of these countries are acting to improve the
situation. At the global level, actions are being taken
to improve mining methods. The Dominican Republic,
Jamaica, Papua New Guinea, and Suriname are mem-
bers of the Intergovernmental Forum on Mining, Min-
erals, Metals and Sustainable Development. Global
efforts in controlling mercury pollution have recently
(2013) resulted in approval of the Minamata Conven-
tion on such international controls to be implemented
in the next few years. It includes measures to improve
artisanal gold mining. Fiji and Papua New Guinea
have attempted to formalize artisanal and small-scale
mining through legal frameworks, but enforcement
remains a challenge.
According to the World Health Organization (WHO,
1992), health is “only possible where resources are
available to meet human needs and where the living
and working environment is protected from life threat-
ening pollutants, pathogens and physical hazards.”
When considering health consequences of metal expo-
sure, the use of information regarding the toxicology of
metals is crucial when trying to create a healthy envi-
ronment. The need for implementation of preventive
action based on such information is urgent in many
developing and newly industrialized countries.
Environmental releases of toxic metals into air and
water systems of developing countries are linked to
health impacts on populations. The global movement
of mobilized metals in the jet stream, with release
into local environments via rain/snow or dry deposi-
tion of particles, is well known (Ranville et al., 2010;
­Gallon et al., 2011). In addition, ocean currents may
also transport metal-containing particles over great
distances (Macdonald et al., 2005). Globalization of the
food industry (see Chapter 6) can lead to human and
livestock metal exposures from contaminated fish and
shellfish or plant products, such as rice and other pro-
duce, originating in other countries. Metal releases in
developing countries hence carry health risks to devel-
oped countries. For all of these reasons, it is important
for public health officials worldwide to be aware of
 25  Metal Toxicology in Developing Countries
these issues and to include appropriate risk informa-
tion in their decision-making processes. Agencies, such
as the European Food Safety Authority, the United
States Food and Drug Administration, and the United
States Environmental Protection Agency are among
those with responsibilities in these general areas.
This chapter provides a brief summary of impor-
tant issues related to toxic metals in developing and
newly industrialized countries, and highlights poten-
tial health problems for populations living there and
the need to use existing information on the toxicology
of metals in developing preventive strategies. Each
topic addressed has a voluminous literature, and this
review, of necessity, is only a starting point for appre-
ciating the multiplicity and types of factors impinging
on public health and how such adverse influences can
be prevented.
3  DEVELOPING COUNTRIES AS GLOBAL
SOURCES OF METALS
3.1  Metal Mining Deposits
Anthropogenic mobilization of metals from the
Earth’s crust results from mining and smelting, the
subsequent erosion of mine wastes and tailings into
river systems, and particle releases into the atmo-
sphere. Natural mobilization of metals can result from
volcanic activity. These processes have resulted in sub-
stantial releases of metals, such as copper, zinc, lead,
nickel, and manganese, into the environment. Metal
releases may occur as a result of mining for specific
metals, such as copper and lead, or secondary recov-
ery processes for elements, such as arsenic, antimony,
bismuth, and cadmium. Valuable rare earth elements
(e.g. gold, palladium, gallium, and indium), which
are increasingly used in modern electronic devices,
are routinely recovered. The use of metallic mercury
in gold mining is a special problem area of major
importance for developing countries where artisanal
gold mining, discussed below, is a common practice.
In many cases, the issue of direct human occupational
TABLE 1  Estimated Global Production of Select Metals (1000 Metric Tons/Yr)a
Metal 2006 2007
Arsenic (as trioxide) 60,900 55,400
Cadmium 19,900 19,400
Chromite 19,700,000 22,800,000
Lead 3,630,000 3,720,000
Mercury 1150 1200
aCompiled from U.S. Geological Survey. Minerals Yearbooks (2010), for each metal, U.S. Department of the Interior. Data from 2010 was con-
sidered to be the most comprehensive data available at the time of publication.
531
exposures during the mining process itself is a cen-
tral concern. In addition, irrigation of important food
crops, such as rice, with local river water contaminated
with mine waste runoff containing toxic metals, such
as cadmium, has also been found to have serious pub-
lic health consequences. The United States Geological
Survey Mineral Yearbook (USGS, 2010) provides useful
information on global production trends for a number
of the more important toxic metals and metalloids,
and indicates that many of these metals are mined in
developing countries. Total world production of toxic
metals/metalloids from 2006 through 2010 is shown in
Table 1.
Summary composite tables extracted from a series
of USGS international regional tables for 2010 are
shown in Tables 2-5. Data are presented for the five
countries in each region, except for Mexico, that are the
highest producers of a specific toxic metal. For some
regions, as will be observed, there are fewer than five
countries that produce a given metal. Data for Mexico
are shown with that for South America, but are con-
sidered separately. Data for arsenic and cadmium are
not shown in these regional tables since they are com-
monly recovered as by-products of copper and zinc
smelting, respectively, and can be found in element-
specific USGS 2010 tables.
China is the world’s largest producer of arsenic tri-
oxide (47% of the total), followed by Chile, Morocco,
and Peru. China is also the major producer of refined
cadmium (34% of the total) followed by Korea, Japan,
Kazakhstan, and Mexico. Data for the production of
a selected number of mined important metals in 2010
from the following world regions are presented: Africa
(Table 2), Asia/Pacific (Table 3), Europe/Central Eur-
asia (Table 4), and South America/Mexico (Table 5).
The purpose of these tables is to highlight the impor-
tance of production activities for a number of toxic
metals discussed elsewhere in this book and to include
data from developing and newly industrialized coun-
tries in various regions of the world.
In Africa, South Africa is a major producer of
chromite, lead, and manganese. Namibia and Niger
2008 2009 2010
53,400 54,100 52,800
22,800 20,800 21,100
24,000,000 19,500,000 23,700,00
3,880,000 3,900,000 4,140,000
1820 1960 2250
532 Bruce A. Fowler, Candace M. Prusiewicz, and Monica Nordberg

TABLE 2  Production of Selected Mineral Commodities in 2010: Africa (1000 Metric Tons of Metal Content,
Unless Otherwise Specified)
Manganese
Chromite Cobalt Copper Gold Lead ore Uranium

Metal refined
Mine output Mine Mine Mine U3O8
Country (Gross wt) Mine output Mine output 1° 2° output (kg) output output Content

Botswana – – 28 – – – – – –
Congo – 61,000 440 – – – – –
(Kinshasa)e
Ivory Coaste – – – – – – – 76 –
Gabone – – – – – – – 1,500 –
Ghana – – – – – 76,332 – 420 –
Madagascare 90 700 – – – – – – –
Malawi – – – – – – – 790
Mali – – – – – 36,344 – – –
Mauritania – – 37 – – – – – –
Morocco and – 3,130 – – – 32,461 – –
Western
Sahara
Namibia – – – – – – 10,140 5,473
Nigere – – – – – – – – 4,949
Nigeriae – – – – – – NA – –
South Africa 10,871 400 103 – – 188,701 50,625 2,900 682
Sudan 57 – – – – 26,317 – 186 –
Zambiae – 5,700 820 – – – – –
Zimbabwee 510 – – – – – –
World total 24,000 101,000 15,800 16,400 2,770 2,560,000 4,170,000 14,600 62,100

1°, primary; 2°, secondary; wt, weight.

eEstimated data, U.S. data, and world totals are rounded to no more than three significant digits.

TABLE 3  Production of Selected Mineral Commodities in 2010: Asia and the Pacific (1000 Metric Tons of Metal Content,
Unless Otherwise Specified)
Copper Gold Lead Manganese ore Mercury

Country Mine output Refined 1° Mine output (kg) Mine output Refined 1° Mine output Mine output

Australia 849 417 261,000 625 178 3,100 –

Chinae 1,160 2,950 345,000 1,850 2,840 2,600 1,600
Indiae – 665 – 95 67 1,000 –
Indonesiae 878 – 106,316 – – – –
Japan – 1,334 – – 102 – –
Korea, Northe – – – 13 – – –
Korea, Republic of – 564 – – 198 – –
Mongolia 125 – – – – – –
Pakistane – – – 26 – – –
Papua New Guinea 160p – 62900p – – – –
Philippines – – 40,847 – – – –
Thailand – – – – – 24e –
Vietname – – – – – 4 –
World total 15,800 16,400 2,560,000 4,170 4,560 14,600 1,930

1°, primary. More details are available from USGS (2010).

eestimate,
ppreliminary.
 TABLE 4  Production of Selected Mineral Commodities in 2010: South America and Mexico (1000 Metric Tons of Metal Content,
Unless Otherwise Specified)

25  Metal Toxicology in Developing Countries

Antimony Cobalt Copper Gold Lead Manganese ore Mercury Platinum Silver

Metal Metal refined Mine Metal refined Metal Metal Metal refined
Mine refined Mine Mine output Mine Mine refined refined Mine Mine
Country output 2° output output 1° 2° (kg) output 1° 2° output 1° 2° output output 1° 2°

Argentina – 2,200 – 140,001 – 16,000 63,138 22,554 14,245 63,000 – – – – – 723,238 – –

Bolvia 4,980 – – – 895 – – 72,803 310 – – – – – – 1,259,388 – –
Brazilp – – 1,500 213,548 177,800 47,700 62,047 19,650 – 114,887 1,048,000 19,580 1,710 – – – 36,500 32,000
Chile – – – 5,419 1,560 – 39,494 695 – – – – – – – 1,287 – –
Colombia – – – 3,555 – – 53,606 – – – – – – – 997 15,300 – –
Perue – – – 1,094,162 393,638 – 145,085 261,978 – – 200 – – – – 3,640 – –
Venezuela – – – – – – – – – 30,000 – – – – – – – –
Mexico – – – 168,855 272,600 5,000 72,596 92,062 110,980 110,000 174,761 – – 15 – 4,410,749 2,230,024 –
World total 166,000 NR NR 15,800 16,400 2,770 2,560,000 4,170 4,560 4,680 14,600 NR NR 1,930 199,000 30,900 NR NR

1°, primary; 2°, secondary; NR, not recorded; wt, weight. More details are available from USGS (2010).
eestimated,
ppreliminary.

533
 534
TABLE 5  Production of Selected Mineral Commodities in 2010: Europe (1000 Metric Tons of Metal Content Unless Otherwise Specified)
Anti Manganese
mony Chromite Copper Gold Lead ore Mercury Platinum group Silver Uranium

Metal refined Mine Metal refined Refined 10 and 20 (kg)

Mine Mine output Mine output Mine Mine Mine Mine U3O8

Bruce A. Fowler, Candace M. Prusiewicz, and Monica Nordberg

Country output (Gross wt) output 1° 2° (kg) output 1° 2° output output Palladium Platinum output content

Albaniae – 290 – – – – – – – – – – – – –
Armenia – – – – – – – – – – – – – 68 –
Austria – – – – 114 – – – – – – – – – –
Belgiume – – – 370 – – – – 105 – – – – – –
Bulgaria – – 105 – – – – 81 – 11 – – – – –
Czech Republic – – – – – – – – – – – – – – 305
Finlande – 210 – – – – – – – – 6 – 275 – –
Georgiae – – – – – – – – – 116 – – – – –
Germany – – – 402 302 – – 125p 280p – – – 110,000 – –
Greece – 1 – – – – – – – – – – – – –
Ireland – – – – – – 39 – – – – – – – –
Italy – – – – – – – – 134 – – – – – –
Kazakhstan – 3,760 380 323 – 30,272 36 103 – 640 – – – 552 20,995
Kyrgyzstane 10 – – – – 18,300 – – – – 250 – – – –
Macedonia – – – – – – 46 – – – – – – – –
Poland – – 425 547 – – – – – – – 15 25 1,181 –
Russia 3,000 400 703 656 218 189,000 97 89 – 9 50 84,700 25,000 1,356 4,200
Serbiae – – – – – – – – – – – 22 – – –
Spaine – – – – 35 – – – 125 – – – – – –
Swedene – – – – 25 6,300 68 – – – – – – 302 –
Tajikistan 2,000 – – – – – – – – – – – – – –
Ukrainee – – – – – – – – – 540 – – – – 1,000
United Kingdom – – – – – – – 150 144 – – – – – –
Uzbekistane – – 90 – – 90,000 – – – – – – – – 2,830
World total 166,000 24,000 15,800 16,400 2,770 2,560,000 4,170 4,560 4,680 14,600 1,930 199,000 301,000 30,900 62,100

1°, primary; 2°, secondary; wt, weight. Numbers in italics are estimates. More details are available from USGS (2010).
eestimate;
ppreliminary
 25  Metal Toxicology in Developing Countries
are major producers of uranium, while the Congo,
Morocco/Western Sahara, and Zambia are major
producers of cobalt. Morocco/Western Sahara and
Namibia are also major producers of lead. Gold is
mined in South Africa, Gabon, Tanzania, Mali, and
Sudan.
In the Asia/Pacific region, China is a major pro-
ducer of lead, manganese, and mercury. Australia and
India are also major producers of manganese. Gold
is extensively mined in Australia, China, Indonesia,
Papua New Guinea, and the Philippines.
In Europe and Central Asia, Kazakhstan and Russia
are major producers of uranium. Russia is also a major
producer of antimony, platinum group metals, and sil-
ver. Germany is a major refiner of platinum. Russia,
Uzbekistan, Kazakhstan, and Kyrgyzstan are major
producers of gold.
In South America and Mexico, Bolivia is a major
producer of antimony, while Brazil is a major pro-
ducer of cobalt. Peru, Mexico, Bolivia, and Brazil are
the major producers of lead. Brazil is also the major
producer of manganese. Silver is extensively mined in
Mexico, Bolivia, and Argentina. Peru, Mexico, Argen-
tina, Brazil, and Colombia are the major producers of
gold in this region.
It is clear from these tables that significant quanti-
ties of both toxic and precious metals are mined in a
number of developing and newly industrialized coun-
tries in various regions of the world. This industrial
activity has positive economic benefits but also poten-
tially negative consequences for occupational and
environmental health if adequate protective resources
are not in place (described in Chapter 24). Environ-
mental consequences are not limited to persons living
in those countries; those in developed countries are
also affected. Adverse health effects to persons living
in developed countries may occur due to secondary
smelter activities, atmospheric and oceanic transport
of toxic metallics released by mining and smelting
activities in developing countries, and use of goods
and consumption of food stuffs produced in develop-
ing countries via increasing globalization of the food
supply (see Chapter 6).
The UN Commission on Sustainable Development
monitors the progress of sustainable development in
UN countries. In some developing and nearly indus-
trialized countries, however, there are difficulties in
developing efficient administrative legislation system
to reach these goals. Dissemination of toxic metals,
such as lead, cadmium, mercury, and the metalloid
arsenic, may occur via atmospheric transport or water
systems. Such transport is highly dependent on local
soil and sediment compositions. For example, elevated
concentrations of elements, such as lead, cadmium,
535
arsenic, zinc, and copper, have been reported in soils
and river sediments at sampling sites proximate to a
mining area in Zambia, with lower concentrations at
more distant sites (Ikenaka et al., 2010). Similar soil
contamination findings for copper, lead, zinc, and
cadmium have been reported by Qin et al. (2012) in
agricultural soils near an abandoned copper mine in
eastern China. They reported that 18.4% of the soils
sampled were in the moderately to heavily contami-
nated category according to Chinese Agricultural Stan-
dards for edible agricultural products.
Similar accumulations of arsenic in edible plants,
fish, shellfish, meats from livestock, and dairy prod-
ucts in mining areas of Latin America (Bundschuh
et al., 2012) and in plants grown in a coal mining area
of India have been reported. Transfer of cadmium into
edible plants such as carrots, parsley, and dill grown
in soils near a lead smelter in Baia Mare, Romania,
exceeding EU-stipulated limits has also been reported
(Mihali et al., 2012). Future land use of old mining
areas for growing crops is an important consideration
in developing countries where sufficient food produc-
tion is an issue.
3.2  Primary and Secondary Smelting
Operations
Primary and secondary smelting operations as well
as unregulated coal-fired power plants have a long his-
tory of dispersing toxic elements, such as lead (Gallon
et al., 2011), silver, and selenium (Ranville et al., 2010)
over wide areas of the Earth, including across the North
Pacific. Atmospheric deposition of metals, such as
lead, cadmium, aluminum, and cobalt, has been exten-
sively studied by a number of investigators (­Wallace
et al., 1977; Jickells et al., 1994; Jickells, 1995; Morel and
Price, 2003). Deposited metals are generally associated
with organic material, such as phytoplankton, in the
water column. The physical and chemical processes
involved in the sorption of metals on to particles in the
marine environment have been reviewed by Brown
and Parks (2001). In the case of cadmium, the metal is
complexed with phytochelatins in the plankton (Morel
and Price, 2003). Binding to the organic component is
pH dependent, with increasing solubility of metals,
such as lead, at low pH values (Jickells, 1995). Stud-
ies of radioactive isotopes of thorium, radium, lead,
and beryllium support the binding of these elements
to particles in the water column but suggest that it is
a dynamic process that shows seasonal (Baskaran and
Santschi, 1993) and depth (Cochran and Masque, 2003)
variations. It is important to note here that river inputs
of metals bound to sediments, such as mineral mining
particles or fertilizers, as discussed below, are also an
536 Bruce A. Fowler, Candace M. Prusiewicz, and Monica Nordberg
important source of toxic metals into embayments and
the oceans. A review by Dagg et al. (2004) noted that
deposition rates of dissolved and particulate materi-
als on the continental shelves were strongly influenced
by plume processes of large rivers that drained exten-
sive land areas. The largest of these rivers in terms of
water volume, such as the Amazon, Zaire, Orinoco,
Ganges-Brahmaputra, and Yangtze, are in developing
countries. Hence, metal contamination of these water
sources is important with regard to oceanic inputs of
metals for the potential accumulation by edible biota.
China is one of the countries in the world where
industrialization is most intense. Considerable efforts
have been made in China to control emissions to the
environment, but there have been difficulties in the
past to avoid pollution. In an area of Zhejiang prov-
ince, cadmium from a zinc and lead smelter was
released into irrigation water used to irrigate rice fields.
Very high daily intake of cadmium (up to 1850 μg/
day) was estimated for farmers and their families
consuming locally grown rice (Nordberg et al., 1997),
and a related increased occurrence of adverse kidney
and bone effects was shown (Nordberg et al., 2002;
Wang et al., 2003). When these adverse effects became
known to the local health authorities, the consump-
tion of cadmium-contaminated rice was stopped from
1996 onwards. The beneficial effect of lower exposure
has been documented in terms of lower cadmium con-
centrations in blood and urine and a reversal of some
of the kidney effects in this population (Liang et al.,
2012). This example further demonstrates the value
of research into health effects in raising awareness of
pollution problems in local communities, resulting in
effective preventive action.
Primary smelting operations process mineral-­
containing ores, while secondary smelting recovers
metals from scrap materials (Blacksmith Institute,
2013). Both types of smelting contribute to global
atmospheric emissions of a number of toxic metallics.
It has been estimated (Yanez et al., 2002) that 60% of
smelters in the world are located in developing coun-
tries. Hylander and Herbert (2008) estimated that the
largest quantities of mercury were emitted by copper,
lead, and zinc smelters, with China being the largest
emitter followed by the Russian Federation, India, and
South Korea. Coal-fired power plants are also major
emission sources of toxic trace elements and the major
global source for mercury emissions. Mercury released
into the environment may be deposited in water bod-
ies, where it can be methylated to form methylmer-
cury, which bioaccumulates in the aquatic food chain
and thus into fish species consumed by humans. This
is a particular concern in developing countries, where
subsistence fishing is an important food source. Other
toxic elements, such as lead, cadmium, and arsenic,
may contaminate local soils used to grow food crops,
including cocoa, rice, and leafy vegetables, as well as
tobacco plants (Rankin et al., 2005). This pattern leads to
increased human exposure to these toxic elements via
the diet (see Chapter 3 for a more detailed discussion
of metals in food). The addition of particulate “scrub-
bers,” which trap particle and other fugitive emissions,
to smelter stacks has the potential to greatly reduce
subsequent human exposures to these elements from
smelters and coal-fired power plants (Hylander and
Herbert, 2008). Elevated soil concentrations of mercury
have been reported in the vicinity of secondary cop-
per smelters in China (Yin et al., 2009). High concentra-
tions of toxic elements, such as arsenic, cadmium, and
lead, have also been reported near smelters in Mexico
(Benin et al., 1999) and the Congo (Narendrula et al.,
2012). The costs of installing and maintaining devices
that trap emissions may be regarded as particularly
great in developing countries but may be worthwhile
in terms of reducing public health outcomes from
elevated exposures to toxic metals over time. A recent
report on lead poisoning among children living near a
smelter in Torreon, Mexico (Soto-Jimenez and Flegal,
2011), indicated that lead exposures in children were
predominately from the smelter despite the installation
of control systems to reduce atmospheric emissions
from this facility. These data suggest that exposures
may occur from the historical deposition of lead dust
in this kind of environment and will take some time to
be reduced without further remediation.
3.3  Recycling of Metal-Containing Products
Recycling of metals under health protective occupa-
tional and environmental conditions is desirable and
an important component of sustainable development.
However, protective measures vary among countries
and adverse human health effects have occurred in
some developing and newly industrialized countries
that lack adequate regulations, equipment, or educa-
tion for persons handling recycled materials.
3.3.1  Battery Recycling (Lead, Cadmium, and Nickel)
Recycling of both lead-acid storage batteries and
more recently nickel-cadmium (NiCad) batteries
takes place in both developed and developing coun-
tries. Few countries have restrictions for export and
recycling in developing countries is a well-known
public health issue since these activities are often
conducted in homes or small workshops with little
or no occupational protections. Children may also be
present and even working in these environments or
 25  Metal Toxicology in Developing Countries
directly involved in the manual recycling activities,
leading to elevated metal exposures at an early and
sensitive life stage. The unsafe recycling of used lead-
acid batteries is one of the oldest and largest p ­ ublic
health issues in developing countries, with docu-
mented exposures of not only adults but also children
(Blacksmith Institute, 2013). Underscoring the danger-
ous health effects linked with lead battery recycling are
the reported deaths of 18 children in Dakar, Senegal,
from November 2007 through March 2008. The fatali-
ties were linked with acute lead dust and soil exposure
from local lead battery recycling operations. Average
blood lead levels of children living in the areas were
more than 12-fold higher than the U.S. Centers for Dis-
ease Control and Prevention action level of 10 μg/dL
(100 μg/L) (­Haefliger et al., 2009).
Recycling of NiCad batteries is an issue of growing
public health concern in developing countries, such as
Iran (Zand and Abduli, 2008) and Egypt (Rabah et al.,
2008). Zand and Abduli (2008) noted that 9800 metric
tons of household batteries were imported into Iran in a
recent decade and that there was no available recycling
program; hence, most of these batteries were ­discarded
via municipal waste into sanitary landfills. As noted
elsewhere in this chapter, such batteries undergo bac-
terial breakdown, and exposure to rain may result in
the leaching of toxic metals, such as nickel and cad-
mium, into groundwater and surface waters.
3.4  E-Waste (Gallium Indium, Gold, and
Arsenic)
Electronic waste, referred to as e-waste, is a growing
global waste problem. Legislation is in place in some
developed countries, for example the EU Regulation
of Waste Electrical and Electronic Equipment (WEEE
Directive 2012/19/EU), promoting the recycling and
restricting the export of such waste, particularly to
developing countries. Despite such efforts, the global
industry of e-waste recycling continues to expand and
presents a number of complex economic and public
health challenges. E-waste includes discarded cath-
ode ray tubes (CRTs), televisions, VCRs, DVD players,
stereo equipment, desktop computers, laptop comput-
ers, CRT monitors, liquid crystal display monitors,
cell phones, keyboards, computer mice, printers, and
copiers. Rapid advancements in information and com-
munication technologies diminish the lifespan of elec-
tronic equipment as individuals continually upgrade
their computers and cell phones. It is estimated that
20-50 million tons of e-waste are generated annually
worldwide, with the largest volumes of waste being
produced by the United States, Europe, China, Japan,
and Australia. Significant amounts of e-waste from
537
industrialized countries are exported to less devel-
oped countries, where labor costs and occupational
and environmental regulations are less restrictive. The
United Nations Environmental Program (UNEP) esti-
mates that e-waste volumes will increase significantly
in developing countries by 2020. Computer-related
e-waste is expected to increase by 200 and 500% in
South Africa and India, respectively while cell-phone
e-waste is expected to increase by 1800% in India dur-
ing the next decade (UNEP, 2009).
In some cases, the recycling stream is initiated by
their collection in developed countries and then their
being shipped overseas via container ships to develop-
ing countries. In the developing countries, small-scale
disassembly can be done by family network members
who melt the electronic components and recycle the
generated raw materials in a largely unregulated or ille-
gal manner (International Labor Organization, 2012).
Valuable metals, such as gallium, indium, and gold,
are resold for reuse in electronics. Other common met-
als, such as copper, zinc, lead, and the metalloid arse-
nic, are also recovered and resold to variable degrees.
It should be noted that other toxic chemicals, for exam-
ple, polychlorinated biphenyls and flame retardants,
such as the polybrominated diphenyl ethers (PBDEs),
may also be released during the process of recovering
metals (e.g. copper from insulated wiring), thus creat-
ing chemical mixture exposure situations (Robinson,
2009). The chemical interactions between toxic metals
and persistent organic chemicals released in the recy-
cling process is a relatively unstudied area of poten-
tial public health concern, particularly in developing
countries (Yanez et al., 2002).
E-waste recycling in countries such as China is
associated with exposures to lead (Zheng et al., 2008;
Wang et al., 2012), cadmium (Zheng et al., 2008), and a
number of other toxic metals (Wu et al., 2008), and has
generated research into the associated human health
effects. Chromosomal alterations and other manifesta-
tions of DNA damage have been reported in human
populations exposed to e-waste (Jiu et al., 2009).
Blood lead and cadmium levels were 50-60% higher in
1-6-year-old children living near an e-waste recycling
center in Guiyu, China (Zheng et al., 2008), where
factors such as whether the father’s work related to
e-waste, the proximity of residence to e-waste center,
and time spent playing outdoors were linked with
elevated metal blood levels (Zheng et al., 2008). Devel-
opmental neurotoxic effects have also been reported
in children exposed to e-waste materials in China
(Chen et al., 2011).
In Nigeria (Nnorom et al., 2010; Onwughara et al.,
2010), the release of lead from CRT computer moni-
tors, other computer components, and other electronic
538 Bruce A. Fowler, Candace M. Prusiewicz, and Monica Nordberg
devices is also well known and has been studied for a
number of years. The profitability of the lead-recycling
industry has led to the expansion of this industry into
many developing countries, including Malaysia, Bra-
zil, South Korea, Vietnam, India, Pakistan, and Mexico
(Arora, 2008).
Codisposal of e-waste in municipal solid waste
(MSW) landfill facilities is a common practice in some
developing countries. Visvanathan et al. (2010) stud-
ied the mobility of metals in MSW bioreactor land-
fills in Thailand using a lysimeter approach, and
demonstrated that the mobility of metals, such as
lead, increased with long-term deposition in the site.
The release of these metals is undoubtedly related to
the action of acid-producing bacteria on the e-waste
materials.
It should be noted here that exposure to toxic ­metals/
metalloids, as well as to related organic chemicals (e.g.
PBDEs), in both developed and developing countries
usually occurs as mixtures of these agents. This impor-
tant topic area is taken up in more detail in Chapter 11,
but the implications of additive or synergistic interac-
tions among toxic elements and related organic chemi-
cals are of particular concern in developing countries,
where dietary nutrition may be inadequate and high
birth rates lead to societies with large numbers of
children at risk of developmental toxicity from metal
exposures. As noted below, the issue at e-waste sites
of potential interactions between toxic metals/metal-
loids and toxic organic chemicals also found in elec-
tronic devices is in need of further research. The UNEP
(2009) as part of its Sustainable Innovation Technol-
ogy Transfer Industrial Sector Studies (STEP) program
published a report that details production, price, and
value for some toxic metallics related to the e-waste
problem in developing countries.
These are in addition to the lead in leaded glass in
CRTs, mercury in switches, and nickel and cadmium
in batteries already mentioned. Table 6 provides infor-
mation on 12 metals/metalloids that are incorporated
into various components of major types of electric and
electronic devices. Many of these are toxic.
UNEP estimates of the number of new and used
electronic devices put on the market in selected devel-
oping countries are shown in Table 7.
Data included in this publication also estimate that
thousands of metric tons of older electronic devices
per year arrive in a selected number of African, Asian
(India and China), and Latin American countries from
developed countries for recycling or reuse via both
legal and nonlegal means. Although these data are dif-
ficult to quantify reliably, even reasonable estimates
indicate that the numbers of metal-containing devices
are enormous and suggest that the total quantities of
toxic metals present must also be very large. The quan-
tities of e-waste generated within selected developing
countries in thousands of metric tons per year may also
be large (as shown in Table 8), with China and India
producing the largest quantities followed by Brazil,
Mexico, Morocco, Uganda, Kenya, and South Africa.
Recycling of e-waste brings economical resources to
developing countries. However, it must be performed
under well-controlled occupational and environmen-
tal conditions.
4  ARTISANAL GOLD MINING
(MERCURY—OCCUPATIONAL EXPOSURES/
SUBSISTENCE FISHING)
Artisanal gold mining is another usually small
industry that is estimated to involve approximately
20 million persons worldwide (Blacksmith Institute,
2013). The mining process utilizes metallic mercury to
form gold-mercury amalgams by running river water
containing alluvial gold particles through sluices
coated with mercury and then recovering the gold by
burning off the mercury with propane torches. Arti-
sanal gold miners are estimated to be the second larg-
est source of mercury released into the atmosphere
after coal-fired power plants. It is important to note
that the miners usually do not work under occupation-
ally or environmentally safe conditions and frequently
entire families are engaged in this activity. This means
that even children are directly exposed to mercury
vapor fumes and to further exposure from local water
and local food sources, such as fish caught by subsis-
tence fishing, which may be contaminated with meth-
ylmercury produced by the methylation of inorganic
mercury wastes.
Passos and Mergler (2008) reported elevated con-
centrations of mercury in the hair of adults and chil-
dren (mean values > 15 μg/g) living in the Amazon
basin. These concentrations were associated with a
number of neurobehavioral deficits, immune system
alterations, cardiovascular system effects, and cyto-
genetic damage. These data indicate that the clear
adverse health effects and costs associated with use of
mercury for the mining of gold in this region. Similar
adverse clinical effects were observed in children liv-
ing near a gold processing and refining plant in Davao
del Norte, the Philippines (Akagi et al., 2000). ­Elevated
concentrations of total and methylmercury were
observed in three species of local fish (1.07-438.8 and
0.71-377.18 ng/g respectively) and in hair samples of
the study subjects (0.278-20.393 and 0.191-18.469 μg/g,
respectively). The study subjects exhibited decreased
stature and weight, gingival discoloration, adenopathy,
 25  Metal Toxicology in Developing Countries 539

TABLE 6  Important Metals Used for Electric and Electronic Equipment (Based on Demand in 2006)
Primary production By-product Demand for EEE Demand/ Value in EEE
Metal (Tons/Year) from (Tons/Year) Production (%) Pricea (USD/kg) (106USD) Main applications

Ag 20,000 Pb, Zn 6,000 30 430 2.6 Contacts, switches, solders

Au 2500 Cu 300 12 22,280 6.7 Bonding wire, contacts,
integrated circuits
Bi 5600 Pb, W, Zn 900 16 31 0.03 Solders, capacitor, heat sink
Co 58,000 Ni, Cu 11,000 19 62 0.7 Rechargeable batteries
Cu 15,000,000 – 4,500,000 30 7 32.1 Cable wire, connectors
In 480 Zn, Pb 380 79 682 0.3 LCD glass, solder, semiconductor
Pd 230 PGM 33 14 11,413 0.4 Multilayer capacitors, connectors
Pt 210 PGM 13 6 41,957 0.5 Hard disk, thermocouple, fuel cell
Ru 32 PGM 27 84 18,647 0.5 Hard disk, plasma displays
Sb 130,000 – 65,000 50 6 0.4 Flame retardant, CRT glass
Se 1400 Cu 240 17 72 0.02 Electro-optic, copier, solar cell
Sn 275,000 90,000 33 15 1.3 Solders
Total – – 4,670,000 – – 45.4 –

EEC, Electric and electronic equipment; LCD, liquid crystal display; PGM, platinum group metals.
aUsing the average price in 2007

Source: Adapted from UNEP (2009).

TABLE 7  Quantity of EEE Put onto the Market (in Metric Tons/Year)
Country Assessment date PCs Printers Mobile phones TVs Refrigerators

China 2007 419,100 NR 15,000 1,170,000 771,700

Colombia 2008 13,600 NR NR NR NR
India 2007 140,800 12,000 9300 450,000 211,500
Kenya 2007 5200 NR 150 NR NR
Mexico 2003 63,700 NR NR 224,100 NR
Morocco 2007 15,100 NR 1700 16,800 NR
Peru 2006 7000 NR NR NR NR
Senegal 2007 1100 NR 140 4200 NR
South Africa 2007 32,000 6800 1900 35,800 22,300
Uganda 2007 700 NR NR NR NR

EEE, electric and electronic equipment; NR, not reported.

Source: UNEP (2009).

TABLE 8  Quantity of E-Waste Generated in Metric Tons/Year for Selected Developing Countries
Country Assessment date PCs Printers Mobile phones TVs Refrigerators

Brazil 2005 96,800 17,200 2200 137,000 115,100

China 2007 300,000 60,000 7000 1,350,000 495,000
Colombia 2006 6,500 1300 1200 18,300 8800
India 2007 56,300 4700 1700 275,000 101,300
Kenya 2007 2500 500 150 2800 1400
Mexico 2006 47,500 9500 1100 166,500 44,700
Morocco 2007 13,500 2700 1700 15,100 5200
Peru 2006 6,000 1200 220 11,500 5500
Senegal 2007 900 180 100 1900 650
South Africa 2007 19,400 4300 850 23,700 11,400
Uganda 2007 1300 250 40 1900 900

Source: UNEP 2009.

540 Bruce A. Fowler, Candace M. Prusiewicz, and Monica Nordberg
and skin abnormalities. Studies by ­Bose-O’Reilly et al.
(2008a) reported mercury in the breast milk of moth-
ers living in gold mining areas as a hazard to infants
in Zimbabwe, Indonesia, and Tanzania. Subsequent
studies by this group in Indonesia (Bose-O’Reilly et al.,
2010a) on artisanal gold miners showed a high degree
of mercury poisoning in not only workers in the amal-
gam smelters but also mineral processors and the gen-
eral population living in these areas. Similar studies
in Tanzania (Bose-O’Reilly et al., 2010b) reported that
only the amalgam burner group showed evidence of
mercury poisoning.
A recent publication by Caravanos et al. (2013)
examined environmental health risks created by min-
ing operations in selected case studies in low- and
moderate-income countries. The authors used data
from the Blacksmith Institute Toxic Sites Identifica-
tion Program, which used an initial site-screening tool.
They reported results on 131 artisanal/small-scale sites
in gold mining areas and 275 industrial mining sites in
a total of 45 countries. These data provide useful infor-
mation on the international scope of mercury releases
from these mining practices in developing countries.
Summary estimates by de Lacerda (2003) indicate that
about 20% of the total anthropogenic atmospheric mer-
cury emissions originate from small-scale gold mining.
From his estimates, a number of countries in South and
Central America, Russia, China, and Africa, as well as
the Philippines and Indonesia, are major contributors
to global mercury emissions.
Environmental and health hazard assessments
have been conducted in a number of these mining
areas, such as Tanzania (Taylor et al., 2005), Kenya
(Ogola et al., 2002), Indonesia (Castilhos et al., 2006;
­Bose-O’Reilly et al., 2008b, 2010a,b), Zimbabwe (Bose-
O’Reilly et al., 2008a,b), and Peru (Yard et al., 2012).
The economic forces driving artisanal gold mining in
developing countries are complex, and both political
(Spiegel and Veiga, 2005; Veiga et al., 2006; Spiegel,
2012) and technical changes such as the use of ball mill
leaching (Veiga et al., 2009; Shandro et al., 2009) and
of magnets (Drace et al., 2012) have been evaluated as
a means of reducing the use of mercury in small-scale
gold mining operations (Figure 1). However, such
methods sometimes involve substitution of cyanide in
the process (Veiga et al., 2009), which may carry other
environmental and health risks. As noted by Shandro
et al. (2009), artisanal gold miners in countries, such
as Mozambique, are also struggling with major pub-
lic health issues like malaria and human immunode-
ficiency virus/acquired immunodeficiency syndrome
so there are competing health problems for limited
societal resources. In summary, artisanal gold min-
ing is a widespread international practice that brings
needed financial resources to impoverished popula-
tions in developing countries but has clear environ-
mental and public health impacts on both a local and a
more global level associated with the global movement
of mercury in the atmosphere and its accumulation in
fishery products. This latter aspect is likely to become
more problematic with the continued globalization of
the food industry.
5  URANIUM MINING
Developing countries are major sources of ura-
nium for the nuclear industry. According to the World
Nuclear Association, Kazakhstan was the largest
uranium-producing country in 2010, with the African
nations of Namibia and Niger in fourth and fifth posi-
tion behind the developed countries of Canada and
Australia. Uzbekistan and China are also major pro-
ducers, but with lower productions.
Aside from occupational radiation exposure of the
miners, the main concerns in many of these countries
are centered on the contamination of local soils with
various uranium-related radioactive isotopes, which
varies with soil pH (Tserenpil et al., 2013). Environ-
mental modeling studies of isotopic uptake by plants,
mollusks, crustaceans and fish using the ERICA tool
(Oughton et al., 2013) have reported accumulation dif-
ferences among these various nonmammalian biota.
In addition, indoor workplace radon exposure studies
near an in situ leach mining site in Pakistan (­Matiullah,
2012) reported exposure levels above established
action limits proposed by a number of world health
organizations.
FIGURE 1  Artisanal gold miner burning off mercury from a Au-
Hg amalgam in Thailand. Source: Blacksmith Institute (2008).
 25  Metal Toxicology in Developing Countries
Uranium exposures from the mining and refining of
uranium ore and uranium in drinking water are poten-
tially important routes of exposure in some countries,
but data on toxicity are limited (Brugge et al., 2005).
The main reported health outcomes from uranium
in drinking water involve the skeleton (Kurttio et al.,
2005) and kidney and occur in a dose-dependent man-
ner (Kurttio et al., 2002, 2005, 2006; Zamora et al.,
1998). In vitro studies (Prat et al., 2005) examining the
transcriptomic and proteomic responses of human kid-
ney HEK 293 cells exposed to uranium demonstrated
concentration-dependent responses between adapta-
tion and cellular toxicity in this cell line.
As with many toxic metals, uranium production in
developing countries has economic benefits, but con-
sideration must be given to long-term environmental
and human health consequences both with regard to
radiation effects from the long-lived isotopes of ura-
nium and the chemical toxicity of the uranium ions.
See Chapter 45 for more details.
6  AGRICULTURAL FERTILIZERS
In many developing countries, there is not enough
food to sustain the indigenous population and to pro-
vide surplus food crops for sale or export. A common
approach for increasing food production is through the
use of superphosphate fertilizers. One problem that
has arisen from this practice stems from the presence of
cadmium in some phosphate fertilizers. Some plants,
such as rice, some grains, and leafy green vegetables,
actively accumulate cadmium from soils, leading to the
increased presence of this metal in staple food crops,
and rice in particular. In addition to point sources, such
as power plants, smelters, and mining operations, toxic
metals and metalloids, such as cadmium, arsenic, and
lead, may also be released into croplands as contami-
nants of phosphate fertilizers. Once in the soil, these
elements may be taken up by various food crops.
There is a large and growing body of literature on
this general problem and a great deal of basic scientific
information has been developed on soil characteristics,
such as type and pH of soil, that may influence metal
bioavailability to plants, as well as differences in metal
uptake between plants. In addition, there is a growing
body of molecular information on the molecules (phy-
tochelatins) responsible for the accumulation of metals
like cadmium in specific plant components. Genetic
studies on metal transporters in the roots of Arabidopsis
thaliana by Thomine et al. (2000) pointed to the homol-
ogy of these transporters with Nramp genes in other
species and highlighted their importance in cadmium
uptake in this plant species. Studies by Jiao et al. (2012)
541
noted the importance of fertilizer application rates, as
well as soil and plant parameters.
Wang et al. (2008) examined the impact of three dif-
ferent phosphate fertilizer types on the bioavailability
of lead, cadmium, and zinc to cabbages. They also noted
that cadmium uptake by the cabbages was negatively
associated with soil pH. Fang et al. (2012) studied the
effects of phosphorous amendments on plant growth
and the bioavailability of lead, copper, and zinc in
metal-contaminated soils and found that phosphorous
was effective in immobilizing lead. They also observed
that metal-sensitive plants were more responsive to
the phosphorous treatments than were metal-resistant
plants. Other studies by Cao et al. (2013) focused on
the mobility of lead, copper, and zinc in contaminated
soils using simulated landfill and rainfall conditions
in a model system. The authors concluded that the
mobility of these metals varied by the type of phos-
phate source, and that some of these metals may be
immobilized while others showed increased mobility.
They also cautioned against elevated releases of phos-
phorous, which may produce eutrophication.
Studies from India by Gill et al. (2013) reviewed
the importance of nitric oxide in mediating cadmium-
induced oxidative stress in plant crops, since cadmium
is also phytotoxic and produces wilting, chlorosis,
reduced growth, and plant death. Studies from Mexico
(Mendoza-Cozatl et al., 2005) reported on cadmium-
induced oxidative stress in a number of phyla, includ-
ing plants, in relation to sulfur assimilation and the
synthesis of glutathione and phytochelatins. It was
concluded that cadmium is an effective activator of
phytochelatin synthetase. Other studies from Argen-
tina (Bianucci et al., 2012) reported the importance of
phytochelatins in producing tolerance to cadmium in
peanut plants and noted that peanut roots were able to
produce a number of different types of phytochelatins
that may play roles in protecting the plants from cad-
mium-induced oxidative stress. Studies from Middle
Eastern countries such as Jordan (Al-Jundi et al., 2008),
Lebanon (Aoun et al., 2010; Kassir et al., 2012), Iran
(Jafarnejadi et al., 2012; Cheraghi et al., 2012), and Saudi
Arabia (Khater, 2012) have reported contamination of
phosphate fertilizers with a number of toxic trace ele-
ments including transuranic elements such as uranium
and 210polonium. These data suggest that public health
metal pollution problems related to the application of
phosphate fertilizers may be greater than just concerns
about metals, such as cadmium, depending on the geo-
logical sources of the phosphate. Monitoring of other
toxic elements and radioactive elements from specific
deposits would seem to be a prudent course of action
prior to the widespread application of phosphate fer-
tilizers from those deposits.
542 Bruce A. Fowler, Candace M. Prusiewicz, and Monica Nordberg
Contaminated groundwater sources are another
evolving public health issue in developing countries,
such as India, Pakistan, and Bangladesh, due to the
presence of arsenic in groundwater derived from
geological formations. Arsenic in drinking water has
received extensive attention, but uptake of this ele-
ment by plants, such as rice, due to use of these water
sources for irrigation practices in developing countries
has only been recognized more recently (Smith et al.,
2006; Pal et al.,2009).
Contamination of food crops, such as rice, from
the use of arsenic-contaminated groundwater and
cadmium-contaminated fertilizers creates several
­
problems for developing countries. In an effort to
increase essential agricultural food production in these
developing countries to support economic growth,
food crops may become contaminated with these toxic
elements and (1) produce major public health problems
for the local populations and (2) render the produce
unacceptable for export or sale. Some of the human
exposure to arsenic and cadmium in rice can be miti-
gated by cooking practices that involve discarding the
cooking water (Carbonell-Barrachina et al., 2009; Khan
et al., 2010). Studies by Khan et al. (2010) reported that
discarding cooking water of rice reduced exposures
to arsenic but not to cadmium. This is most likely the
result of cadmium being complexed with phytochela-
tins in the rice matrix.
Studies from China (Dou et al., 2013) reported
enrichment of zinc, chromium, lead, cadmium, and
copper in surface sediments of eastern Beibu Bay in
the South China Sea. They attributed the increased
cadmium concentrations to use of phosphate fertiliz-
ers and transport of this element into the bay by local
rivers. The potential importance of this is that cad-
mium carried into embayments by river runoff from
croplands could also lead to cadmium contamination
of local shellfish.
An additional related problem is the use of indus-
trial wastewater from mining, industrial uses, and
municipal sewage treatment plants (Abdu et al., 2011)
for the irrigation of crops. These practices have also led
to large-scale contamination of crops, such as rice and
vegetables, with cadmium and arsenic in a number
of countries including Japan, Thailand, India, and Sri
Lanka. The limited availability of water in many coun-
tries, particularly clean water, has also led to the use
of reclaimed water for agricultural purposes. It must
be noted that water treatments from sewage treatment
plants are largely focused on removing microorgan-
isms and not the removal of chemicals, such as toxic
metals, pharmaceuticals, and organic chemicals. The
use of such water sources for food production may
hence create similar problems to those noted above as
sources of available clean water become limited and
the populations of many developing countries con-
tinue to grow.
In addition to food crops, plants used for medicinal
purposes in developing countries such as Botswana
(Okatch et al., 2012), South Africa (Street, 2012), India
(Sarma et al., 2011), and China (Harris et al., 2011) may
also accumulate toxic metals. This is a potential public
health issue for both the developing country of origin
and developed countries if dietary supplements or
pharmaceutical products derived from these plants are
exported.
7  METHODS FOR THE REMOVAL OF TOXIC
METALS FROM WASTEWATER STREAMS IN
DEVELOPING COUNTRIES
It is important to note that in a number of develop-
ing countries there has been considerable progress in
engineering relatively low-to-moderate cost, innova-
tive methods for the removal of toxic metal ions from
wastewater and groundwater. Some of these rely on
man-made (Alvarez-Ayuso et al., 2003; Choi et al.,
2006; Akgul et al., 2006; Johnson and Worrall, 2007) or
natural zeolites (Erdem et al., 2004). Copolymer hydro-
gels have also been synthesized and tested for remov-
ing metals from water (Ali et al. 2003). ­Orescanin et al.
(2011) reported that electrocoagulation with advanced
oxidation treatment of groundwater from the city of
Osijek in eastern Croatia was highly effective in remov-
ing a number of toxic elements including arsenic,
nickel, vanadium, chromium, manganese, iron, cop-
per, zinc, and lead. This is another promising technical
approach for removal of toxic metallics from water in
addition to more traditional adsorptive methods using
iron-based technologies (Cundy et al., 2008)
Other approaches have used more biological
methods such as shells from peanuts (Periasamy and
Namasivayam, 1996; Salam et al., 2011), hazelnuts,
­
orange peels, jackfruit, and soybean hulls (Kurniawan
et al., 2006), algae/bacterial biofilters (Loutseti et al.,
2009), and chitosan (Chauhan et al., 2012). Salam et al.
(2011) compared peanut shells, fly ash, charcoal, and
natural zeolites and reported that all of these adsor-
bent matrices were effective in removing metals from
wastewater. Phytoremediation using nonfood plants,
such as herbs (Tang et al., 1999), ornamental sunflow-
ers (Hao et al., 2012; Cassina et al., 2012), or Indian
mustard (Cassina et al., 2012), is another low-cost and
effective approach for removing toxic metals such as
cadmium from irrigation water system-contaminated
soils. Bech et al. (2012) reported lead and zinc accumula-
tion in two plant species grown on mine wastes in Peru
 25  Metal Toxicology in Developing Countries
and noted their potential application for phytoreme-
diation. ­Ghaderian et al. (2012) reported the results of
similar studies on copper, lead, and zinc accumulation
in several native plant species grown in a copper min-
ing area of Iran. Similar findings have been reported
for copper, lead, and zinc in a mining area of northern
Tunisia (Zribi et al., 2012) and in Spain (­Garcia-Salgado
et al., 2012). An interesting variation of this approach
has been published by Carcamo et al. (2012), who
studied the effects of increasing soil pH by the addi-
tion of seashell grit to aid the phytostabilization of
copper, zinc, and arsenic in soils surrounding a copper
smelter in the Puchuncavi Valley in central Chile. They
reported positive findings for this approach as a cost-
effective management option. Aquatic plants such as
the water hyacinth (Jayaweera et al., 2006) have been
effectively used to remove cadmium, lead, chromium,
and zinc from wastewater in constructed wetlands in
Sri Lanka. Similar findings have been reported in Por-
tugal for the removal of arsenic from water systems by
a number of water plants (Favas et al., 2012) and alu-
minum in a mesocosm in Canada (Goulet et al., 2005).
Clearly, significant progress has been made in develop-
ing countries in producing cost-effective methods for
the removal of toxic metals from water systems such
that the water may be used for drinking or agriculture.
These studies suggest that problem areas described in
the above sections regarding metal contamination of
drinking and agricultural water systems, while major,
need not be intractable. A combination of innovative
recycling methods and low-cost methods for attenu-
ating the release and removal of toxic elements from
these water systems seems feasible.
8  NEEDED PREVENTIVE ACTION AND
RESEARCH INTO THE TOXICITY OF
METALS IN HUMANS
It should be clear from the above discussion that
developing countries are at especial risk of a num-
ber of adverse environmental and human health
effects from toxic metals and metalloids. This is due
to a confluence of factors including, but not limited
to, the presence of rich mineral resources, low-cost
labor, weak environmental and public health infra-
structure, high reproductive rates, nutritional defi-
ciencies, and the prevalence of health problems that
consume limited public health resources. Many of
these problems can be addressed using our existing
knowledge and efforts are made by the international
community to stimulate sustainable development
in all countries. The lack of resources in develop-
ing countries is a challenge: technologies used in
543
developed countries for waste treatment and efflu-
ent control have to be adapted to the local situation
and in addition there may be a need for new low-
cost, innovative solutions. Given this general back-
ground, there is also a pressing need for research
to address the metal toxicology issues summarized
above. The local impact of research into the health
effects of metal pollution in stimulating societal
action to stop exposures can sometimes be consid-
erable and such research thus has a dual effect. It
is important to note, given the documented global
movement of toxic metals such as lead, that these
issues are also of importance to developed countries
since some fraction of these metals will be trans-
ported between continents and deposited by rain,
snow, and dry depositional fallout.
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