Interdisciplinary approach to addressing lead pollution caused by mining activity in Kabwe, The Republic of Zambia

ABSTRACT

Industrial development and economic growth have made human life more convenient. However, the accompanying environmental pollution is a serious problem. The same situation that developed countries have experienced in the past is now being repeated in developing countries, especially in Asia and Africa. Although lead has long been a useful metal in supporting human life, it is highly toxic to living organisms and affects various biological functions, including the kidneys and nervous system. Lead is one of the substances symbolizing the trade-off between industrial and economic development and environmental pollution. Kabwe in the Republic of Zambia, a town that grew out of the discovery and development of lead-zinc deposits, is now known as one of the most lead-polluted areas in the world. While Kabwe is a classic example of the trade-off described above, it is distinct from other polluted areas in that it has been the site of diverse academic research. These include geological survey of the mine, the characterization of mine wastes, monitoring of environmental and animal samples, human health impact studies, understanding of lead dispersion pathways, and development of remediation technologies for contaminated environments. In environmental monitoring, several studies have reported lead concentrations in soil of up to tens of thousands of mg/kg, and lead concentrations in crops exceed international standards by up to 770 times. Extremely high concentrations of lead have also been detected in wildlife, livestock, and humans. Various toxicological studies have been conducted on humans in particular. These studies reveal the contamination status and its effects. However, the elucidation of the diffusion pathways and the development of environmental remediation methods using materials that can be procured locally at low cost pave the way to solving the problem. This review comprehensively outlines these studies in chronological order, as well as the efforts of the Zambian government and future perspectives. This report also provides some guidance on how to promote academic research and problem solving in other polluted areas.

INTRODUCTION

Industrial and socioeconomic development have been rapid since the Industrial Revolution. However, environmental pollution caused by industrial activities is a major issue. For example, in the late 20^th century, Japan achieved rapid economic growth unparalleled in the history of the world. However, simultaneously, the country was affected by some severe diseases including the Itai-itai disease (Tsuchiya, 1969; Inaba et al., 2005) and Minamata disease (Harada, 1995; Ekino et al., 2007), which still linger today. In the 21^st century, developing countries in Asia and Africa are undergoing remarkably rapid economic growth, and it has recently become clear that there is industrially derived environmental pollution in these regions (Pang and Abdullah, 2013; World Health Organization (WHO), 2014; Mia et al., 2019). The Agency for Toxic Substances and Disease Registry (ATSDR) has listed lead (Pb) as the second substance in the Substance Priority List, that was prepared to identify the most significant potential threat to human health (ATSDR, 2017a). In fact, Pb is toxic to living organisms, affecting various functions such as kidney function, reproductive function, and nerve function (Wani et al., 2015; ATSDR, 2017b). One of the key mechanisms of Pb toxicity is the induction of oxidative stress resulting from the production of reactive species and depletion of antioxidant defense systems (Matović et al., 2015). Effects on immune function by disrupting cytokine production and on gene expression levels of metallothionein, a metal-binding protein, have also been reported (Gillis et al., 2012). Moreover, metabolomics and epigenetics-related effects have received more attention in recent years (Park et al., 2017; Eguchi et al., 2018; Wang et al., 2019). According to the WHO, Pb accounts for 0.6% of the global disease burden, which is the highest in developing countries (WHO, 2009). It is also known that low-income communities tend to be more susceptible to pollution (Miranda et al., 2011). Lead is still an extremely useful metal for industry due to its properties. Lead is used in various industrial products, including batteries, and was once widely used as an additive in gasoline, although it has already been phased out worldwide. From this perspective, Pb is a pollutant that symbolizes the trade-off between industrial development and environmental pollution mentioned above, especially in developing countries. Among developing countries, the concern about Pb contamination in Africa has been growing recently (WHO, 2014).

The Republic of Zambia is a landlocked country in Southern Africa (Fig. 1), where the mining industry has been the backbone of the nation since pre-independence. Kabwe, the capital of Central Province, was the site of the discovery of Pb-zinc (Zn) deposits in 1902 and was once a major source of Pb for other countries. The history of the mine, formerly known as the Broken Hill Mine, is indirectly linked to the Industrial and Mineral Revolutions that began in England in the late 17^th century and in South Africa in the late 19^th century (Mufinda, 2015). Raw materials were needed for the Industrial Revolution to succeed; however, as production costs soared in Europe and the United States, and demand outstripped supply, Western countries sought new sources of production. It was against this background that T.G. Davey, an Australian geologist working for the Broken Hill Development Company in Rhodesia, discovered the veins of Pb and Zn at Broken Hill in 1902. Later, the railroad network to South Africa was developed and production equipment could be easily transported; this has led to the start of mining in 1904 and full-scale production from 1906 (Guernsey, 1953; Turner, 1979). As production grew on a larger scale, so did the development of the town, and since then, mining has been central to the history of Kabwe. Since the closure of the mine in 1994, various mining-related industries, such as slag re-smelting, still operate and are important industries in the region.

Fig. 1

Map showing (A) the location of the Republic of Zambia, (B) Kabwe district, and (C) townships in Kabwe district

While the Pb-Zn mines in Kabwe have underpinned the industrial development of the international community and brought enormous socioeconomic benefits to the region and nation, serious Pb contamination in the area has been reported (WHO, 2014). In 2013, Kabwe was listed as one of the 10 most polluted areas in the world (Blacksmith Institute, 2013). Although similar cases can be found in many parts of the world, the Kabwe case is unique in that a wealth of field research and academic studies have been conducted, and various stakeholders are working together to solve the problem.

Environmental pollution caused by various environmental pollutants has been reported worldwide throughout history. In today’s world, sustainability has become important, as symbolized by the SDGs. It is necessary to properly confront environmental pollution and aim for essential solutions, rather than taking shortcuts as if to cover up the destruction. This review provides a chronological overview of the various initiatives in Kabwe. Environmental pollution is an environmental and health issue, but the causes of pollution are traced to human activities, such as those of the industry and economy. In other words, environmental pollution is a social issue caused by humanity itself. In this sense, environmental pollution can and must be solved by mankind. It is strongly hoped that this review will provide a guideline for academia to play a role in environmental pollution issues, and in turn, help to solve environmental pollution worldwide.

METHODOLOGY

A literature review was conducted to review reports of lead contamination in Kabwe. The literature search was completed using keywords including “Lead,” “Zambia,” “Kabwe,” “mine,” “slag,” “geology,” “environment,” “contamination,” “poisoning,” and “remediation.” Data sources included PubMed and Google Scholar. Google search was also carried out to check a gray paper or report. No limit was set on the search data and publication date, but language was limited to English. The retrieved papers and reports were screened for relevance. Subsequently the authors extracted the data. Fig. 2 summarizes the papers reviewed in this review.

Fig. 2

History of Kabwe mine and reporting period of various studies. [1] Dechow and Jensen, [2] Kortman, [3] Unrug, [4] Braithwaite, [5] Kamona, [6] Kamona, [7] Water Management Consultants Ltd., [8] Sracek et al., [9] Ettler et al. (a), [10] Ettler et al. (b), [11] Reilly and Reilly, [12] Clark, [13] Nwankwo and Elinder, [14] ZCCM-IH, [15] Tembo et al., [16] Ikenaka et al., [17] Nakayama et al., [18] Nachiyunde et al., [19] Nakata et al., [20] Uchida et al., [21] Kříbek et al., [22] Mwilola et al., [23] Zingani et al., [24] Mufalo et al., [25] Yabe et al., [26] Ikenaka et al., [27] Nakayama et al., [28] Yabe et al., [29] Nakata et al., [30] Nakayama et al., [31] Doya et al., [32] Toyomaki et al., [33] Yamazaki et al., [34] Kataba et al., [35] Clark, [36] Yabe et al., [37] Mbewe et al., [38] Yabe et al., [39] Bose-O’Reilly et al., [40] Yabe et al., [41] Yamada et al., [42] Yohannes et al., [43] Nakata et al. (a), [44] Nakata et al. (b), [45] Nakata et al. (c), [46] Yohannes et al. (a), [47] Yohannes et al. (b), [48] Toyomaki et al., [49] Nakamura et al., [50] Leteinturier et al., [51] Hamvumba et al., [52] Mwandira et al. (a), [53] Mwandira et al. (b), [54] Mwandira et al., [55] Tabgviroon et al., [56] Mwilola et al., [57] Yoshii et al., [58] Silwamba et al. (a), [59] Silwamba et al. (b), [60] Ettler et al.

MINE AND TAILINGS

GEOLOGICAL CHARACTERISTICS

The Pan-African Lufilian Fold Belt is rich in polymetallic mineralization, mainly composed of copper-cobalt (Cu-Co) and Pb-Zn sulfides. Most of the belt straddles the Democratic Republic of Congo, Angola, and northern Zambia (Copperbelt Province), and Kabwe constitutes the southern end of the belt (Unrug, 1988). The Late Proterozoic rocks contain stratified, vein, and skarn deposits, and they have been an important source of metals for the international community since the 20^th century. The distribution of mineralization types varies among areas and involves three tectonic units. The mineralization type of the Kabwe deposit is vein. The zinc-lead-cadmium (Cd)-silver (Ag) ore contains trace amounts of Co, nickel (Ni), vanadium (V), and Cu (Kortman, 1972). The sulfide core of the orebody contains sphalerite (ZnS), galena (PbS), and pyrite (FeS₂) with a small amount of copper sulfides. These minerals exist in an envelope of oxidized mineralization consisting of silicates, carbonates, and oxides of Pb, Zn, and Fe (Unrug, 1988).

Kamona (1993) indicated that the Kabwe Pb-Zn deposit has produced at least 2.6 Mt of Zn and 0.8 Mt of Pb, with minor amounts of Ag (79 t), fused V₂O₅ (7,820 t), Cd (235 t), and Cu (64 t) during the mine operation period. After the closure of the mine in 1994, the presence of relatively rare trace elements, including germanium (Ge), gallium (Ga), and indium (In) was suggested (Melcher et al., 2006). The Kabwe deposit was formed from high-salinity, high-temperature fluids derived from formation water that equilibrated with sedimentary rocks in a continental tectonic environment. The presence of faults and high geothermal gradients in continental tectonic zones could be a key to providing the necessary conditions for fluid circulation and mineralization in dolomite fault zones. Most of the elements associated with mineralization are confined to the ore body and are not widely dispersed in the parent dolomite (Kamona and Friedrich, 2007). The parent rock of the deposit, dolomite, has the same homogeneous Pb isotope ratio as the galena ore, indicating that the Kabwe dolomite layer was contaminated with Pb from the ore (Kamona et al., 1999). Other findings related to the origin of deposit formation estimated from sulfur isotope ratios (Dechow and Jensen, 1965) and spencerite (Braithwaite, 1988) have been reported.

LEACH PLANT RESIDUE AND SLAG

A photograph of leach plant residue is shown in Fig. 3. The main minerals identified in the wastes of Cu-Co chemical-leaching plants are gypsum (CaSO₄∙2H₂O), mohaucite (Co_0.6Ni_0.3(SO₄)∙6H₂O), broodite (Na₂Mg(SO₄)₂∙4H₂O), starkite (MgSO₄∙4H₂O), chalcantite (CuSO₄∙5H₂O), and cloenite (Na₂Cu(SO₄)₂∙2H₂O). In the dissolution experiment using salts collected from the field, a rapid decrease in pH and a rapid increase in the dissolved concentration due to the rapid dissolution of salts were observed. This result suggested that the beginning of the rainy season could cause serious environmental problems (Sracek et al., 2010).

Fig. 3

Photographs of (A) leach plant residue (left) and efflorescence of zinc sulfate and gypsum (right) and (B) site of small-scale mining. Both photos were taken in October 2021

In a simulated hydrometallurgical extraction of slags from the metallurgical processing of Pb-Zn vanadate ores, Ettler et al., (2020a) observed a higher Zn extraction rate (>72%), compared to the Pb, due to the formation of a large amount of secondary lead sulfate (angleite). This indicates that economic Pb extraction is difficult to achieve using hydrometallurgical methods. The Kabwe slag contains high concentrations of V and has a very high extraction rate (>80%), indicating the potential for future secondary metal recovery (Ettler et al., 2020a). Old slags deposited in an abandoned Kabwe mine represent an important source of metal-containing dust particles. The slag dust fractions contain up to 6.3 wt% Pb, 19 wt% Zn, and 2,610 mg/kg V. The Pb concentrations in the fine slag dust fractions of <48 μm (42,300–51,200 mg/kg for ISF slug and 18,400–47,500 mg/kg for Waelz slag) and <10 μm (57,600–62,700 mg/kg for ISF slag and 23,100–49,100 mg/kg for Waelz slag) were extremely high. Similarly, the levels of Zn and V in the fine slag dust fraction were also higher than those in bulk slag. Additionally, those metals were distributed into soluble phases (metal-rich Mn oxides, slag glasses, hemimorphites, and carbonates) (Ettler et al., 2020b).

CONTAMINATION STATUS IN THE 20^th CENTURY DURING MINING OPERATIONS

LEAD LEVELS IN THE ENVIRONMENT

Several relevant papers were published in the 1970s (Fig. 2). The first report-concerned metal concentrations in soil, plants, and trees (Reilly and Reilly, 1972). The Kabwe surface soil was highly polluted by Pb with a mean concentration of 1,487 mg/kg (dry weight), which was reported to be very high compared with the capital city of Lusaka (14.5 mg/kg) and a rural area (1.1 mg/kg). Lead concentrations in plant leaves were 312–1,427 mg/kg (dry weight), 42–120 mg/kg in tree woods (dry weight), and 401–1,342 mg/kg (dry weight) in tree leaves. All sample types had higher concentrations than those in Lusaka (3.40–14.14 mg/kg for plant leaves, 2.10–3.40 mg/kg for tree woods, and 8.40–23.46 mg/kg for tree leaves) and the rural area (2.96–5.26 mg/kg for plant leaves, 1.74–2.93 mg/kg for tree woods, and 2.43–8.80 mg/kg for tree leaves). These plant and tree samples were washed thoroughly with cold water before extraction and analysis. Washing with organic solvent or acetic acid did not remove most of the Pb, suggesting that the Pb may be chemically bound to the organic matter. In maize, a staple food in Zambia, 28 mg/kg for grain and 77 mg/kg for leaves were recorded after washing with cold water (Reilly and Reilly, 1972).

Lead concentrations in surface soil of 92–2,580 kg/mg (dry weight) were reported by Nwankwo and Elinder (1979) within 5 km west of the mine at Kasanda in 1976–1977. The average soil Pb concentration was 862 mg/kg, which was more than 50 times higher than the average value of 16.1 mg/kg in Lusaka. Maize collected from home gardens within a 3 km radius of the mine showed Pb concentrations of 0.57–1.36 mg/kg (dry weight), with a mean value of 0.90 mg/kg. Lead concentrations in spinach and cabbage ranged from 47.5–322 mg/kg (dry weight) in the west, downwind of the mine, to 20.5–29.4 mg/kg in the north (Nwankwo and Elinder, 1979). Additionally, during the same period, Pb concentrations of 100–9,400 mg/kg (dry weight) were reported in soils sampled from Kasanda and the Chowa area (Fig. 1), which are located at the eastern side of the mine (Clark, 1975). In 1991–1992, just before the closure of the mine, soil samples were analyzed within 0–20 km east, west, north, and south of the mine. Soil Pb concentrations were 0.1–758 mg/kg and were generally higher on the western side of the mine. In all directions, Pb concentrations decreased as the distance from the mine increased (Tembo et al., 2006).

A report prepared by the ZCCM-IH summarized the results of soil Pb concentration surveys conducted between 1975 and 1999 (ZCCM-IH, 2002). The first survey in 1975 recorded Pb concentrations of up to 21,000 mg/kg (dry weight) in soil reaching 0.15 m below the surface in a residential area in Kabwe. The 1994 survey conducted within the mine plant site recorded a maximum concentration of 409,000 mg/kg. Surveys conducted in residential areas showed maximum Pb concentrations of 34,000 mg/kg in 1990 and 15,820 mg/kg in 1999, indicating that severe soil contamination continued into the late 20^th century (ZCCM-IH, 2002).

Atmospheric Pb concentrations have also been reported, with monthly concentrations of 0.002–0.020 mg/m³ in the Kasanda area from April 1973 to July 1974, and 0.001–0.002 mg/m³ recorded in Chowa from May 1974 to July 1975. Both areas in Kabwe exceeded the USEPA standard for the average air Pb concentration for 30 days at that time, which was 0.005 mg/m³. In Kasanda, the concentration in September 1973 was 0.0029 mg/m³, which was much lower than that in the preceding and following months (0.0071 and 0.0090 mg/m³). This phenomenon was due to the temporary shutdown of the Imperial smelter furnace that month. A decrease in Pb concentration was also observed in January and February 1974 (0.002 and 0.005 mg/m³), which the author attributed to wind changes during the rainy season (Clark, 1975), as cited by Nriagu (1992).

A recent interesting study used the rings of pine trees (Pinus montezumae L.) and sedimentary soils as indicators to assess past contamination (Baieta et al., 2021). Although a particularly significant contamination was only found in the topsoil to a depth of about 10 cm, Pb isotope results indicated that the contamination extended to a depth of 40 cm. The Pb concentration in the tree biomass was large, with a maximum of 6.48 mg/kg (dry weight). On the basis of the sequential extraction results, the authors proposed that the Pb was not taken up through the roots, but rather was due to wind-blown particles deposited on the bark and leaves of the trees. Interestingly, trees located away from the mine area contained much higher Pb concentrations than trees closer to the slag dump. The Pb accumulation in pine trees closely reflects the changes in smelter production, showing a significant increase in production in the 1970s (Baieta et al., 2021).

LEAD LEVELS IN HUMANS

While there are no reports of Pb concentrations in wildlife or livestock in the 20^th century, Pb accumulation in the people of Kabwe was reported. In a study of 122 pairs of mothers and their infants living in the Kasanda area within a 3 km western radius of the mine, the venous blood Pb concentration in the mothers was 41.2±14.4 μg/dL, and the cord blood Pb concentration in the infants was 37.0±15.3 μg/dL (Clark, 1977). Blood Pb levels (BLLs) in mothers and children showed a significant positive correlation. BLLs of 14.7 μg/dL in mothers and 11.8 μg/dL in infants were recorded in different directions from Kasanda, i.e., north to northeast, within a radius of 3.3 km from the mine. These results indicated that Pb exposure was greater in the area west of the mine, even though the distance from the mine is comparable. However, there were no significant differences in birth weight, blood hemoglobin concentration, or packed cell volume compared to Lusaka, which is not a Pb-contaminated area (Clark, 1977).

At the same time as the maternal and infant surveys described above, surveys of children up to 16 years of age were conducted in Kasanda and Makululu (west of the mine), and Chowa (east of the mine) (Clark, 1975). Compared with the other areas, BLL was generally higher at Kasanda, with a mean BLL of 103 μg/dL at age 2 years. BLL showed a downward trend with age after an age of 3 years. However, the mean BLL at age 16 years was still high at approximately 40 μg/dL. The other two areas showed a similar trend in that BLL peaked at age 2 years and then gradually declined (Clark, 1975). Findings on human Pb exposure in Africa during the 20^th century are extremely valuable, so the results in Kabwe mentioned above were published in 1997 in a paper that outlined Pb exposure in Africa (Chukwuma 1997).

STUDIES IN THE 21^st century

Although the Kabwe mine was shut down in 1994, various studies on the Pb contamination have been conducted since the beginning of the 21^st century. A wide variety of studies have been reported, such as environmental monitoring, human studies, as well as studies aimed at elucidating the mechanisms of contamination and solutions for the issues. The research teams are also diverse; however, most reports came from a joint team from Japan’s Hokkaido University and the University of Zambia, a Czech team, and Zambian government projects funded by the World Bank.

MINE WASTE CHARACTERIZATION

Mine waste, which is defined to include any material produced by mining or processing activities, is abundant in the Kabwe mine site. Mine wastes are disposed of or stored in piles on the plains. The wastes have diverse compositions due to their diverse origins, including all processes of mining and smelting. It is extremely important to understand the detailed composition and chemical form of mine waste because the degree and mechanism of diffusion to the surrounding environment may vary depending on the form of Pb and mixtures. In this regard, the Copperbelt Environment Project funded by the World Bank and implemented by the Zambian government in the 2000s, provides a detailed summary based on 68 mine waste samples. The materials are resolved into the following four groups (Fig. 4) from a geochemical perspective (Water Management Consultants Ltd, 2005):

Fig. 4

Map showing different mine waste types and their locations at the Kabwe mine dump site (Water Management Consultants Ltd., 2005)

A) Slag waste (including ISF, Waelz Klin, and gray slag wastes)

Concentrations of Pb (1%–9%), Zn (3%–25%) and Mn (generally <2%) are relatively low.

B) Leach plant residue

The Pb concentration is high, with a maximum level of 21%. The Pb/Zn ratio is high because it is produced by a metallurgical process that selectively removes Zn.

C) Washing plant slimes and blue powder wastes

It is mainly composed of high concentrations of residual Zn (22%–31%). The content of most trace metals including Pb is low, and the Pb/Zn ratio is lower than that of leach plant residues.

D) Efflorescent sulfosalt crusts

These wastes are found on the surface of large areas of Kabwe waste and are the result of evaporative concentration. They have low Pb concentrations (often below 1%) and contain enriched Zn (>30%). A significant portion of the mass of these wastes is composed of zinc sulfate, which has lower concentrations of As, Cu, and other trace metals than other types of wastes sampled.

In addition to the approximately 80 ha of ore beneficiation waste above, there is dolomitic waste rock stockpiled adjacent to the Kabwe mine open pit to the north. Metallic deposits were derived from the main canal extending eastward from the mine. During the operation of the mine, the canal was periodically dredged to maintain its capacity. The sediments excavated during this process were allegedly deposited along the banks of the canal, especially in the areas of Chowa and Katondo. Removal of these sediments was initiated by the ZCCM in the 1990s, but several piles (typically 0.5 to 3 m high) remain; the total volume of this material is estimated to be around 50,000 tons in 2005 (Water Management Consultants Ltd., 2005). The same report estimated that some waste materials were deliberately transported from the Kabwe mine site for use as road stones and building materials. Interviews in the field have revealed that this practice remains today. However, there is no knowledge of the exact extent, type, and end use of this removed waste.

CONTAMINATION DIFFUSION PATHWAYS, METEOROLOGICAL FACTOR, AND Pb STABLE-ISOTOPE RATIOS

The extent of wind-induced diffusion in soil and mine waste is expected to depend on the particle size. Analysis of the particle size distribution of soil and Zn-leaching residue showed that 50% of the soil was less than 50 μm in diameter (Mufalo et al., 2021). The dumping site, which is the source of the Pb dispersion simulations, was covered with slag, and 6% of the slag was found to have a particle size smaller than 150 μm (Nakamura et al., 2021). Kabwe tends to have east-southeast winds with an annual frequency of 10.95% (Nakamura et al., 2021). By season, in the rainy season (November to April), the most common wind directions were westerly (11.79%), northerly (10.45%), and east-southeasterly (7.78%). In the dry season (May to October, excluding August due to machine issues), the most common wind directions were east-southeast (14.71%), southeast (14.08%), and south-southeast (11.08%). In terms of other meteorological factors, Kabwe has the following averages: solar radiation of 0.22 kW/m², atmospheric pressure of 872.62 hPa, humidity of 68.65%, and temperature of 23.08°C (Nakamura et al., 2021).

Nakamura et al., (2021) simulated Pb dispersal by wind using three different models depending on the wind speed: a plume model, a weak puff model, and a no-puff model. The results show that Pb dispersal from the Kabwe mine is greatly affected by wind direction and wind speed during the dry season, whereas the effect during the rainy season is limited. In the rainy season, the moisture content of the ground surface is higher, which may make the dispersion more difficult. Hence, there is seasonality in the Pb diffusion pattern. Additionally, the deposition calculated by the simulation decreases with distance from the mining area and is consistent with the measured Pb concentration in soil (Fig. 5). The simulations showed that smaller particles were dispersed further away from the source and vice versa, and smaller particles were easily redispersed according to particle size. Overall, the authors concluded that Pb contamination in soil is mainly due to the dispersion of fine mine wastes (Nakamura et al., 2021).

Fig. 5

Geographical distribution of Pb concentrations in topsoil from the Kabwe area reported by (A) Kříbek et al. (2019) (classed point) and (B) Nakayama et al. (2011) (contour) and Pb concentrations in subsurface soil reported by (A) Kříbek et al. (2019) (contour)

Some studies on Pb pathway tracing have been conducted using Pb stable-isotope ratios as an indicator. Pb exists in nature as four major stable isotopes, with varying abundance ratios depending on the region where the Pb is produced. The combined ratios of these four isotopes, especially ²⁰⁸Pb/²⁰⁶Pb and ²⁰⁷Pb/²⁰⁶Pb, are widely used to estimate the source of contamination because they are relatively easy to analyze precisely and do not change due to physicochemical effects (Bollhöfer and Rosman, 2001; Veysseyre and Bollho, 2001; Charalampides and Manoliadis, 2002). The Pb isotope ratios in various tissues of goats and outdoor-reared chickens near the Kabwe mine were similar to the ratios in soils sampled from near the mine. This suggests that soil is the major source of Pb exposure for animals near the mine and not, for instance, leaded fuel, which was phased out entirely in Zambia in 2008 (Nakata et al., 2016). Furthermore, the soil Pb level averaged 2,300 mg/kg (dry weight), which is well above the standard set by the USEPA (USEPA, 2020). The authors pointed out that ingestion of crops grown in this soil environment, as well as unintentional ingestion of soil on hands and food, may contribute significantly to Pb exposure in the population (Nakata et al., 2016). A study on dogs showed similar results. Blood Pb isotope ratios in dogs near the mine were close to those in Kabwe galena (Kamona et al., 1999), and higher blood Pb levels further approximated galena’s isotope ratios (Toyomaki et al., 2020). There is also one study on Pb stable-isotope ratios in humans. In a study on infant-mother pairs in Kabwe, the isotope ratios in the infants’ blood and feces were nearly identical to those of soil and galena that was previously reported by Kamona et al. (1999) (Toyomaki et al., 2021). This strongly suggested that soil is one of the major sources of Pb exposure for infants, as suggested by the findings from animal samples. The isotope ratios in the blood of mothers and children were also similar, and the authors pointed to the possibility of mother-to-child Pb transfer via breast milk and the placenta (Toyomaki et al., 2021). Additionally, in vivo experiments were performed, in which Wistar rats were kept for one year in cages lined with Pb-contaminated soil from Kabwe. The results showed that the Pb stable-isotope ratio in the lungs was particularly close to that of galena compared with other rat tissues except the kidneys. This suggested respiratory exposure to Pb in small-particle soil via the lungs (Nakayama et al., 2019).

ENVIRONMENTAL POLLUTION STATUS

Soils at 12 sites within 20 km of the mine recorded a maximum of 113,801 mg/kg and a mean of 22,693 mg/kg (Zingani et al., 2020) (Table 1). Other studies reported maximum values in the order of tens of thousands of mg/kg and average values in the order of thousands of mg/kg (Ikenaka et al., 2010; Nakayama et al., 2011; Nakata et al., 2016; Uchida et al., 2017; Kříbek et al., 2019; Mwilola et al., 2020), except for the study by Mufalo et al. (2021), which analyzed playground soils. Soil samples were likely collected from various locations, including residential areas, roadsides, agricultural land, and in the proximity of mines; however, detailed information on the location attributes of the data reported for the Kabwe region was mostly not provided. Therefore, it is difficult to simply compare the Pb levels reported in different papers, although certain similarities in experimental methods, such as sample pretreatment methods are observed. According to the USEPA, the hazard level for Pb in bare soil from residential areas or from areas where children play is 400 mg/kg (dry weight), and 1,200 mg/kg for the rest of the uncovered areas (USEPA, 2001, 2020). The fact that all reports of soil Pb recorded concentrations that exceed the standards by up to several dozen times is a very serious concern.

Table 1 List of papers reporting Pb concentrations in environmental mediums in Kabwe

Sample type	Specification	Collection site	Sample size	Collection period	Sample treatment	Acid used for metal extraction	Analytical method	Pb level (mg/L for water and mg/kg for others)					Reference
								min	max	mean	SD	median
Soil
	Topsoil	within 2 km radius of the mine	3	May and Sep 2008	2 mm shieving, air-dry	H2SO4, HNO3, HClO4, HCl	AAS	880	16,951	7,076	8,644	3,398	Ikenaka et al., 2010
	Topsoil	within 10 km radius of the mine	101	May 2009	2 mm shieving, oven dry (105°C)	HNO3	AAS	9	51,188			282	Nakayama et al., 2011
	Topsoil	within 500 m radius of the mine	19	May 2014	oven dry (50°C)	HNO3, H2O2	ICP-MS	57.67	24,570	2,316	5,460		Nakata et al., 2016
	Topsoil	30 km away from mine	2					14.24	16.10
	Topsoil	within 5 km radius of the mine	14	July 2016	None	None	XRF	20	10,000				Uchida et al., 2017
	Topsoil	within 15 km radius of the mine	116	N/A	air-dry, 2 mm shieving	None	XRF	10	40,692			199	Kříbek et al., 2019
	70-90 cm depth	within 15 km radius of the mine	40					9	39,529			28
	Topsoil	within 20 km radius of the mine	12	Mar 2016	N/A	HNO3, HCl	AAS	24.55	113,801	22,693	41,857	199	Zingani et al., 2020
	0-20 cm depth	within 500 m south of the mine	N/A	2019	air-dry, 2 mm shieving	HNO3, H2O2	AAS			8,810	310		Mwilola et al., 2020
	Playground topsoil	within 10 km radius of the mine	8	2019	air dry	None	XRF	265	3,320	1,521	1,147	1,075	Mufalo et al., 2021
Crops
	Maize	30 km away from mine	1	May 2014	oven dry (50°C)	HNO3, H2O2	ICP-MS	N/D					Nakata et al., 2016
	Maize	within 500 m radius of the mine	3					0.17	2.09	0.92	1.02
	Rape	within 500 m radius of the mine	4					55.20	231	129.46	73.74
	Cabbage	within 500 m radius of the mine	2					1.59	82.07
	Onion	within 500 m radius of the mine	2					N/D	0.35
	Tomato	within 500 m radius of the mine	5					0.01	7.02	2.37	2.94
	Sugar cane	within 500 m radius of the mine	1							335.27
	Maize roots	within 500 m south of the mine	10	2019	oven dry (70°C)	HNO3	AAS			743.3			Mwilola et al., 2020
	Maize stover	within 500 m south of the mine	10							554
	Maize grain	within 500 m south of the mine	10					27.3	29.0
Water
		N/A		Sep-Oct 2011	N/A	N/A	AAS	0	0.094	0.003	0.015		Nachiyunde et al., 2013
		within 500 m radius of the mine	5	May 2014	None	HNO3, H2O2	ICP-MS	0.07	0.69	0.42	0.32		Nakata et al., 2016
		30 km away from mine	2					N/D

Note: AAS=atomic absorption spectrometry, ICP-MS=inductively coupled plasma mass spectrometry, XRF=X-ray fluorescence, N/A=not applicable, N/D=not detected.

Two papers have reported on Pb accumulation in crops. A small study by Nakata et al. (2016) reported Pb levels in edible parts of maize, which a staple food in Zambia, and various vegetables (Table 1). In the Codex standard, the standard values for Pb concentration are 0.3 mg/kg in leafy vegetables, 0.1 mg/kg in bulb vegetables, and 0.05 mg/kg in fruit vegetables (FAO/WHO, 2014). Maximum Pb concentrations of 231 and 82.07 mg/kg (dry weight) were recorded for rape and cabbage grown in home gardens near the mine in Kabwe; these exceeded the standard values for leafy vegetables by approximately 770 and 270 times, respectively. The maximum Pb concentration in the edible part of onion was 0.35 mg/kg (dry weight), which is extremely low compared with the two leafy vegetables, but it exceeds the standard value of 0.1 mg/kg for bulb vegetables. The maximum values of 2.09 and 7.02 mg/kg (dry weight) were recorded in the edible parts of maize and tomato, which are classified as fruit vegetables, and these significantly exceed the standard value of 0.05 mg/kg. Pb exposure from all agricultural crops is a concern, especially maize, which is a staple food in Zambia (Nakata et al., 2016). The consumption of maize by Zambians is probably much higher than the consumption assumed when international standards were set. A detailed site-specific study was conducted on maize grown on a test farm beside a mine. It recorded 27.3–29.0 mg/kg (dry weight) of Pb in the edible grain, although this was much lower than in the roots and stover (Mwilola et al., 2020).

The USEPA has established a standard value of 0.015 mg/L for Pb in drinking water (USEPA, 2021). A survey conducted in 2011 reported a maximum value of 0.094 mg/L and a mean value of 0.003 mg/L, indicating that some samples exceeded the standard (Nachiyunde et al., 2013). Drinking water samples collected from residential areas within 500 m of the mine in 2014 recorded a minimum value of 0.07 mg/L, showing that all of the collected samples exceeded the standard value (Nakata et al., 2016). Hence, it is suggested that Pb contamination occurs in various kinds of environmental samples, including soil, crops, and drinking water, and that the exposure of residents to Pb through ingestion of contaminated crops is extremely high.

ANIMAL STUDIES

Environmental monitoring using local animals has been widely conducted in the field of environmental chemistry, and wild rats are particularly useful sentinel animals. This is because they share the same living habitat with humans, often feed on crops and household food, share somewhat similar diets to humans, and are versatile enough to inhabit all regions of the world. A study of rats (Rattus rattus and R. tanezumi) conducted in May 2009 showed that rats in Kabwe accumulated significantly higher concentrations of Pb in the liver and kidneys compared with rats collected in Lusaka, the capital city of the Pb-free area (Nakayama et al., 2011). The Pb concentration in the kidneys of Kabwe rats from Lusaka was significantly higher than that in the liver; however, the Pb concentrations in the two organs were significantly correlated. Interestingly, the body weight of the rats and the Pb concentration in the kidneys were significantly different. From these results, the authors suggested that rats in Kabwe are chronically exposed to Pb, which may inhibit their growth (Nakayama et al., 2011). A molecular biological analysis of rats was performed in a study published 2 years later by the same authors (Nakayama et al., 2013). While the Pb levels found in the liver and kidney of Kabwe rats were not extremely high from a toxicological perspective, metallothionein-1 (MT-1) and metallothionein-2 (MT-2) mRNA expression levels were significantly higher than in Lusaka rats. Metallothionein, a low-molecular-weight protein, is a biomarker of metal contamination as it is induced by metal exposure (Marques et al., 2008). MT-1 and MT-2 play a major role in the detoxification of toxic metals, homeostatic regulation of essential metals, and tissue protection from oxidative injury (Haq et al., 2003). A unique study focusing on Pb accumulation in the teeth of rats has also been reported recently. The accumulation of Pb in the crown of the incisor teeth of R. rattus collected from residential areas in different parts of Kabwe showed a significant positive correlation with blood Pb levels (Kataba et al., 2021). Furthermore, teeth Pb levels decreased with increasing distance from the mine. Pb mapping by laser ablation ICP-MS showed an increase in Pb intensity at the tip of the incisor crown with an enamel surface. These results suggested that Pb concentrations in incisor crowns may reflect Pb contamination in rat habitats and may serve as a new monitoring indicator. The most recent report on rodents concerns the effects of Pb exposure on metabolism (Nakata et al., 2022). In this study, metabolomic analysis of plasma was performed using the gas chromatography-mass spectrometry (GC-MS). Phenylalanine and isoleucine were significantly higher in rodents exposed to high levels of Pb living near mines than those in the reference area. Additionally, hydroxybutyric acid was marginally significantly higher, suggesting increased lipid metabolism. Phenylalanine and isoleucine were identified as possible biomarkers in both the interregional least-absolute shrinkage and selection operator (lasso) regression model analysis and the random forest model. Enrichment analysis identified urea circuits and ATP-binding cassette transporter pathways. This is the first time that metabolomic analysis has been performed on Pb-exposed wild terrestrial animals, and some of the results followed previous studies in humans and laboratory animals.

As livestock and poultry are consumed as food, their contamination directly threatens human health. Significantly higher Pb concentrations in the liver (0.42 mg/kg, dry wt) and kidney (0.58 mg/kg) of cattle in Kabwe compared to cattle in cities in other parts of Zambia were reported (Yabe et al., 2011). The detected Pb level is lower than the European reference value for edible organs of 0.5 mg/kg (wet wt), or equivalently 2.32 mg/kg (dry wt) (Regulation Council, 2001). However, cattle liver and kidney are consumed as delicacies in Zambia, and the consumption may be greater than in Europe. The authors noted that significant health risks from consuming large quantities of metal-accumulated bovine offal are of concern (Yabe et al., 2011). Ikenaka et al. (2012) focused on the health effects of the cattle themselves. In addition to blood Pb levels, there were significantly higher levels of MT-2, tumor necrosis factor alpha (TNF-α), interferon-γ (IFN-γ), interleukin-1β (IL-1β), interleukin-6 (IL-6), and inducible nitric oxide synthase (iNOS) in cattle from Kabwe than those from the reference area. Since these genes are involved in the immune system, the possibility of immune system disturbance due to Pb exposure was raised (Ikenaka et al., 2012). As for even-toed ungulates, there is one report on goats. In goats within a few hundred meters of the mine, the mean Pb levels in the liver (1.75 mg/kg wet wt), kidney (1.98 mg/kg), and lung (0.86 mg/kg) exceeded the edible-organ standard of 0.5 mg/kg wet wt (Regulation Council, 2001). For muscle, 60% of the target samples also exceeded the maximum Pb level for human consumption of 0.1 mg/kg (FAO, 2012).

For poultry, there are two studies on chickens. Yabe et al. (2013) compared organ Pb levels in outdoor free-range chickens and commercial broiler chickens raised indoors. The outdoor-raised free-range chickens had significantly higher liver Pb levels than the broilers. The mean Pb concentrations in liver (4.15 mg/kg, wet wt), kidney (7.62 mg/kg, wet wt), and lung (3.34 mg/kg, wet wt) of outdoor-reared chickens significantly exceeded the standard value of 0.5 mg/kg (Regulation Council, 2001). For muscle sample, 59% exceeded the meat standard value of 0.1 mg/kg (FAO, 2012). These results indicated that keeping chickens outdoors increases Pb exposure and risk when consumed as food (Yabe et al., 2013). This is consistent with Regulation Council (2001) who reported that the mean Pb concentrations in the liver (1.25 mg/kg, wet wt), kidney (3.44 mg/kg), lung (1.17 mg/kg), and brain (0.70 mg/kg) in outdoor-raised chickens near the mine were over the edible-organ standard. Muscle also exceeded the meat standards (FAO, 2012) in 20% of the samples (Nakata et al., 2016).

Like rats, companion dogs would be useful as sentinel animals for assessing human Pb exposure because they share a living environment with humans. Blood Pb levels in dogs kept in residential areas near the mine were significantly higher than those in dogs in the reference area (Toyomaki et al., 2020). The blood Pb levels decreased with increasing age and distance from the mine. These results agreed with those obtained in other animal species such as rats and cattle. Alternatively, interestingly, biochemical tests using dog plasma showed that most of the parameters related to liver and kidney functions were within the normal values in most of the samples; no clinical symptoms were observed (Toyomaki et al., 2020). A recent study performed genome-wide DNA methylation analysis on blood samples from these dogs (Yamazaki et al., 2021). It identified 827 CpG regions with differential methylation, and it verified methylation at four CpG sites by bisulfite pyrosequencing. The results showed that abnormal methylation was enhanced in Pb-exposed dogs. This contributed to the knowledge on epigenetic changes caused by Pb exposure.

Lizards live in various environments, including residential areas, green areas, and bare land. Unlike rats, whose main habitat is residential areas, lizards are more generalist in that they do not depend on the attributes of the area. This allows the possible effects of three different land uses (residential, green, and bare land) on Pb contamination levels to be analyzed. Analysis of Pb concentrations in lizards inhabiting three different land attributes revealed that Pb concentrations in lizards on bare land were higher than those further from the mine, and lower than those estimated in green areas (Doya et al., 2020). This suggests that differences in land use can affect pollution levels. As mentioned above, wind dispersal of dust is thought to contribute to Pb diffusion from the mine area, and it is assumed that contamination tends to be lower in green areas, where the amount of dust dispersal is easily reduced. Nineteen percent of the lizards had higher Pb concentrations in the lungs than in the liver. This is a different trend from the results in other animal species. It was suspected that exposure in the respiratory tract through dust inhalation was significant. This paper significantly contributed to the conventional understanding that pollution levels depend on the distance and direction from the source.

SURVEYS OF KABWE RESIDENTS

The first human study of the 21^st century in Kabwe was conducted by Misenge Environmental and Technical Services Ltd. (METS) between 2003 and 2012 (Bose-O’Reilly et al., 2018). Children under 7 years of age, living in residential areas near mines were surveyed. The mean blood Pb level per area was approximately 15–40 μg/dL, with a maximum value of 185.0 μg/dL. Since 2004, a Zambian government project funded by the World Bank has also conducted a survey. The project covered a wide age range. In children, blood Pb levels of up to 65.0 μg/dL have been reported in Chowa, Kasanda, Katondo, Makandanyama, Makululu, Mutwe Wansofu, and Railway (Water Management Consultants Ltd., 2005). Since the CDC’s recently revised reference level is 3.5 μg/dL (Ruckart et al., 2021), the blood Pb levels in children in Kabwe are considered very seriously high. Since 2012, a joint team from Hokkaido University and the University of Zambia has repeatedly conducted surveys. A 2012 survey of children under the age of 7 reported median blood Pb levels of 74.9 μg/dL in Kasanda, 51.1 μg/dL in Makululu, and 39.3 μg/dL in Chowa, and the maximum in all areas was 427.8 μg/dL (Yabe et al., 2015). Five years later, in 2017, the survey was expanded to include all ages including adults and to cover the entire Kabwe district, not just the mining suburbs. The survey revealed that blood Pb levels were higher in children than in adults, and that while Pb levels were particularly high in the vicinity of the mine, blood Pb levels exceeding the CDC reference level were also found in areas over 20 km away (Yabe et al., 2020). In addition to Pb concentration analysis, research topics have expanded to include the effects on hematopoietic and liver functions (Nakata et al., 2021a), effects at the genetic level, such as DNA methylation (Yohannes et al., 2020, 2021a, 2021b), and effects on maternal quality of life due to Pb exposure in children (Nakata et al., 2021b). Moreover, a recent paper evaluated the accuracy of the LeadCare device, which can be used for simple on-site analysis of blood Pb levels (Nakata et al., 2021c).

Another study used socioeconomic statistical analysis methods to calculate representative levels of blood Pb among Kabwe residents (Yamada et al., 2020). This paper highlighted an important potential problem with human surveys commonly conducted in the field of environmental chemistry. Specifically, there may be selection bias in the contaminant concentration data obtained from participants recruited through voluntary research cooperation. For example, Kabwe residents who are aware or concerned about high Pb exposure to themselves, such as people who work in the Pb industry, frequently visit the vicinity of the mine, or have clinical symptoms, could be more willing to participate in the study. The representative blood Pb level of Kabwe residents that was calculated by excluding such biases was 11.9 μg/dL. Furthermore, the authors added location information to the Pb concentration data and mapped it to visually illustrate the blood Pb concentration by region (Fig. 6).

Fig. 6

Geographic distribution of blood Pb levels that were socioeconomically estimated for children (age 16 months) (left) and adults (right) based on surveys in July to September 2017 (Yamada et al., 2020)

ENVIRONMENTAL REMEDIATION TECHNIQUES

Ongoing smelting activities and other related mining industries still play an important role in the national and regional economies. The complete shutdown of mining activities or the complete shielding or removal of economically valuable slag through re-smelting is not a realistic approach. Thus, studies using samples and materials collected from Kabwe have assessed various methods that could be practically implemented. These methods can be broadly classified into three categories: chemical immobilization, biological techniques using microorganisms, and phytoremediation using plants.

Tangviroon et al. (2020) devised a method using dolomite, the base rock of Kabwe, to reduce leaching of Pb. Dolomite is industrially produced in large quantities around Kabwe and can be obtained locally at very low cost. Half-burned dolomite of less than 2 mm in particle size was obtained locally in Zambia and heated at 700°C for 2 h, and then mixed with the residual materials from the Kabwe mine for batch testing. This increased the pH of the leaching solution and precipitated the lead hydroxide, thereby reducing the leaching concentration to below the regulatory limit. Similar results were seen with magnesium oxide, which is commonly used as an immobilizer, but the authors argue that half-burned dolomite is superior in terms of cost and feasibility (Tangviroon et al., 2020). Silwamba et al. (2020a) have proposed a method of adding zero-valent aluminum to leach Zn plant leach residue in a sodium hydrochloric acid-sodium chloride mixture. This induces the dissolved Zn and Pb to be cemented. Through flocculation and sieving of the cement-like material, Zn and Pb could be removed and recovered more efficiently. Processes such as residue washing after smelting is eliminated by this method, and residual Pb in the residue can be economically reduced by performing dissolution and cementation simultaneously. This method is very interesting because of its advantages for both the industrial economy and environmental protection. A similar method has been devised in which microscale zero-valent iron is added to leach Zn plant leach residue in an acid chloride solution (Silwamba et al., 2020b). The Pb cemented to the surface of the zero-valent iron can be easily recovered by magnetic separation. This increases the Pb removal rate. Additionally, it was reported that the toxicity characteristic of the leaching procedure and in vitro solubility and bioavailability research of the treated Zn plant leach residue were greatly improved (Silwamba et al., 2020b).

The reduction of contaminant mobility by microbial biocementation has been reported. Cementation studies with Pararhodobacter sp. on Zn leach plant residue and kiln slag from the Kabwe mine was demonstrated by Mwandira et al. (2019a). Calcium carbonate precipitation by this microorganism was found to reduce the Pb concentration in leachate to below the detection limit (0.001 mg/L). It was also shown that the low water absorption of the cementation material prevented the diffusion of Pb through the water medium. Similar studies using microbially induced calcium carbonate precipitation have also been reported. For instance, Mwandira et al. used Oceanobacillus profundus KBZ 1-3 and O. profundus KBZ 2-5 isolated and extracted from the Kabwe mining area. These Pb-tolerant bacteria contribute to the reduction of metal leaching and have high potential for use as indigenous bacteria (Mwandira et al., 2019b). Another strain of the same species, Oceanobacillus profundus KBZ 3-2, can sequester both Pb and Zn in the extracellular polymeric substance, and it has been shown to remove up to 97% of Pb (Mwandira et al., 2020).

Lemongrass is a hyperaccumulator of Pb and is readily available in Kabwe. Yoshii et al. (2020) showed that growing lemongrass with chicken manure reduced exchangeable Pb in contaminated soil by 70%, demonstrating its usefulness for phytoremediation. A phytogeochemical survey conducted over 20 years ago identified plants in the field that covered 39 taxonomic groups, some of which were found to be metal-resistant (Leteinturier et al., 2001). In this paper, the authors selected Indigofera spicata, Melinis repens, Cynodon dactylon, and Aristida adscencionis as effective species in reducing pollution in Kabwe for their niche formation, stable seed supply, soil stability, erosion control, and suitability for slope planting. Sunflower (Helianthus annuus), sorghum (Sorghum bicolor), and Chinese cabbage (Brassica chinensis) have been studied for more direct phytoremediation, i.e., absorption and removal of Pb by plants (Hamvumba et al., 2014). In this study, plants were grown for 10 weeks in Kabwe soil with different Pb concentrations, and then the dry biomass yield and Pb concentration in the above-ground and below-ground parts were analyzed. The results showed that Pb absorption was higher in Chinese cabbage than in sunflower and sorghum. However, the growth of these plants is poor when the Pb concentration in the soil is high, and issues remain in terms of food safety. The safe production of crops in contaminated soil has been studied by Mwilola et al. (2020). In this experiment, maize, a staple food in Zambia, was grown to maturity in Kabwe soil mixed with chicken manure, triple superphosphate fertilizer, or a mixed fertilizer (consisting of nitrogen, phosphorous, and potassium fertilizer, and composted chicken manure). The results showed that all soil amendments reduced bioavailable soil Pb, and reduced they Pb in maize stover and grain by more than 25%. The hazard quotients for Pb in maize produced without soil amendments were above 1, indicating the need for safer food production using soil amendments. It is necessary to combine the most appropriate methods, considering the characteristics of the target area, land use patterns, and available input costs.

RECENT SITUATION AND FUTURE PERSPECTIVES

Kabwe is facing the serious issue of Pb contamination from over 90 years of mining in the 20^th century and smelting activities that have continued since then. Activities in the region include formal industry activities by operating companies holding official licenses from the government, as well as informal industry activities. Small-scale mining is often an illegal operation carried out by individuals. In these cases, the safety of the miners cannot be guaranteed, and appropriate environmental measures cannot be expected; this may result in further Pb pollution in the surrounding environment. Near the mines, blocks are also being made using soil from vacant land. The blocks made from contaminated soil are thought to contain toxic metals including Pb, and the distribution of these blocks could lead to the spread of secondary pollution.

There has been a recent change in the formal industry areas according to interviews with local communities: in addition to ore mined in Kabwe, ore purchased from other areas such as the Copperbelt province of Zambia and other countries, including the Democratic Republic of the Congo, is also being processed in Kabwe’s smelting facilities. Many of these ores are believed to be copper ores, and the use of ores of different compositions and origins could change the future contamination. Some studies have examined the effects of other toxic metals such as cadmium, or the combined effects of multiple metals, in addition to Pb alone (Nakayama et al., 2011, 2013; Yabe et al., 2018; Nakata et al., 2021a). Geologically, ores and geological formations that contain large amounts of a particular metal usually also contain large amounts of other metal elements. Therefore, further studies on the combined effects of various metals should be conducted.

There are several important positive developments that can help to resolve the contamination issue. First, a new fence surrounding the entire slag dump site was built a few years ago. Previously, there was no physical barrier at all, and residents, including children, were often seen entering the dump site for informal business or for walking. It is extremely risky for people without proper protective equipment to enter the slag site that contains high concentrations of metals. The installation of a fence is expected help prevent this. Additionally, ZMERIP, funded by the World Bank, has been implemented by the Zambian government since 2017 (World Bank, 2021). The project consists of components on health intervention and environmental remediation practices. Program development and technical guidance to local healthcare providers based on the advice from the researchers from Hokkaido University in Japan and the University of Zambia were demonstrated. As a result, more than 10,000 residents have thus far been screened for Pb poisoning, and chelating agent treatment has been provided to those who exceeded the standard level. As for environmental remediation, the ZMERIP is working on a pilot-scale project in some residential areas near the mine.

The commitment of the Zambian government and other relative agencies is essential for the continued development of initiatives that require high costs, such as health intervention and environmental remediation. Even if there is agreement on the importance of efforts to solve environmental pollution, in many cases the cost of such measures would prevent their implementation. This is a common issue in the field of environmental chemistry. One way to address this issue is from a socioeconomic perspective. Specifically, we should quantify the various costs that arise from environmental pollution. Examples of such costs include increased medical costs and decreased labor productivity due to the deteriorating health of the population. It is also desirable to estimate the cost of implementing measures to solve pollution and quantify the expected future benefits of such measures. This cost-benefit analysis allows us to explain the importance of environmental pollution control measures not only from an ethical and moral perspective but also with socioeconomic validity. Such efforts are already underway to address the pollution issues in Kabwe (Japan Science and Technology Agency, 2021). It is hoped that the outputs expected in the future will lead to solutions for the pollution.

Industrial development and economic growth make human life more convenient and affluent. However, environmental pollution threatens human health and has a negative impact on the social economy. In this review, we have presented a typical example of these tradeoffs that mining development brings. In relation to these tradeoffs, we would like to mention some new movements that have emerged in areas other than environmental chemistry, namely, economics, management, and business. One such movement is the concept of creating shared value (CSV), proposed by Porter and Kramer (2019). In CSV, economic value and social value should be compatible, and this compatibility is essential for the sustainability of society and businesses. CSV is bringing about significant changes in society, including the Sustainable Development Goals (SDGs) set up by the United Nations General Assembly (UN-GA) in 2015 (UNDP, 2015). The awareness of environmental issues by the international community has grown rapidly recently, and environmentally friendly industries are required. However, it is also necessary to consider the efforts that should be made in areas that have already been polluted. It is here that environmental chemistry has as important a role to play as ever.

SUMMARY

This review has summarized historical studies and recent developments on Pb contamination in the Kabwe town of Zambia. Kabwe became developed through the discovery of Pb-Zn deposits, and the history of the city in the 20^th century is very closely related to the history of mining. Nearly 30 years after the closure of the mine, mining is still the center of the city’s industry, including smelting activities and informal industrial activities, and it supports the lives of many people. However, we cannot overlook the fact that the city was ranked as one of the 10 most polluted areas in the world. Pb, for better or for worse, is a symbol of this city. This trade-off between the socioeconomic benefits of industrial development and environmental pollution is not unique to Kabwe. Rather, it is a common challenge that can be seen worldwide at both the micro and macro scales.

What distinguishes Kabwe is not the abovementioned tradeoffs, but the fact that various academic studies and field research are actively being conducted. In many polluted areas, especially in developing countries, it is common to find a black box where serious pollution is suspected, but there is no track record of investigation, and the actual status of the pollution is unknown. The research processes described in this paper, i.e., from monitoring of environmental samples to animal studies, followed by elucidating the contamination status and specific health effects in humans, can be used as a reference for other contaminated areas. The quantification of the socioeconomic impact is extremely important for solving social problems, in addition to the assessment of the actual status and impact of pollution in terms of environmental chemistry and medicine. Additionally, academia should provide concrete methods and evidence for solving pollution problems. At this stage, the participation of researchers from different fields, such as engineering and agriculture is essential. The timely implementation of such a comprehensive approach and the active commitment of the Zambian government in Kabwe will assist with solving the problem. This will provide important lessons for stakeholders in the environmental field.

ACKNOWLEDGEMENTS

This research was supported by JST/JICA SATREPS (Science and Technology Research Partnership for Sustainable Development; grant number JPMJSA1501), JST aXis (Accelerating Social Implementation for SDGs Achievement; grant number JPMJAS2001), JSPS KAKENHI Grant Number JP 21HP2003, and Hokkaido University (Sosei Tokutei Research).

REFERENCES

• Agency for Toxic Substances and Disease Registry (ATSDR), 2017a. Substance priority list. https://www.atsdr.cdc.gov/SPL/#2017spl (accessed 31 December 2021)
• Agency for Toxic Substances and Disease Registry, 2017b. Lead toxicity. What are possible health effects from Pb exposure? http://atsdr.cdc.gov/csem/Pb/docs/csem-Pb_toxicity_508.pdf (accessed 15 December 2021)
•  Baieta,  R.,  Mihaljevič,  M.,  Ettler,  V.,  Vaněk,  A.,  Penížek,  V.,  Trubač,  J.,  Kříbek,  B.,  Ježek,  J.,  Svoboda,  M.,  Sracek,  O.,  Nyambe,  I., 2021. Depicting the historical pollution in a Pb-Zn mining/smelting site in Kabwe (Zambia) using tree rings. J. Afr. Earth Sci. 181, 104246. doi: 10.1016/j.jafrearsci.2021.104246.
• Blacksmith Institute, 2013. The World’s worst 2013: The top ten toxic threats, Blacksmith Institute, New York. https://www.worstpolluted.org/docs/TopTenThreats2013.pdf (accessed 15 December 2021)
•  Bollhöfer,  A.,  Rosman,  K.L.R., 2001. Isotopic source signatures for atmospheric Pb: The Northern Hemisphere. Geochim. Cosmochim. Acta 65(11), 1727–1740. doi: 10.1016/S0016-7037(00)00630-X.
•  Bose-O’Reilly,  S.,  Yabe,  J.,  Makumba,  J.,  Schutzmeier,  P.,  Ericson,  B.,  Caravanos,  J., 2018. Lead intoxicated children in Kabwe, Zambia. Environ. Res. 165, 420–424. doi: 10.1016/j.envres.2017.10.024.
•  Braithwaite,  R.S.W., 1988. Spencerite from Kabwe, Zambia, and the infrared spectroscopy of the Kabwe zinc phosphates. Mineral. Mag. 52(364), 126–129. doi: 10.1180/minmag.1988.052.364.13.
•  Charalampides,  G.,  Manoliadis,  O., 2002. Sr and Pb isotopes as environmental indicators in environmental studies. Environ. Int. 28(3), 147–151. doi: 10.1016/S0160-4120(02)00020-X.
•  Chukwuma, Sr.,  C., 1997. Environmental Pb exposure in Africa. Ambio- J. Hum. Environ. 399–403.
•  Clark,  A.R., 1975. The sources of Pb pollution and its effects on children living in the mining community of Kabwe, Zambia. University of London, London.
•  Clark,  A.R., 1977. Placental transfer of Pb and its effects on the newborn. Postgrad. Med. J. 53(625), 674–678.
•  Dechow,  E.,  Jensen,  M.L., 1965. Sulfur isotopes of some Central African sulfide deposits. Econ. Geol. 60(5), 894–941. doi: 10.2113/gsecongeo.60.5.894.
•  Doya,  R.,  Nakayama,  S.M.M.,  Nakata,  H.,  Toyomaki,  H.,  Yabe,  J.,  Muzandu,  K.,  Yohannes,  Y.B.,  Kataba,  A.,  Zyambo,  G.,  Ogawa,  T.,  Uchida,  Y.,  Ikenaka,  Y.,  Ishizuka,  M., 2020. Land use in habitats affects metal concentrations in wild lizards around a former Pb mining site. Environ. Sci. Technol. 54(22), 14474–14481. doi: 10.1021/acs.est.0c00150.
•  Eguchi,  A.,  Nomiyama,  K.,  Sakurai,  K.,  Kim Trang,  P.T.K.,  Viet,  P.H.,  Takahashi,  S.,  Iwata,  H.,  Tanabe,  S.,  Todaka,  E.,  Mori,  C., 2018. Alterations in urinary metabolomic profiles due to lead exposure from a lead-acid battery recycling site. Environ. Pollut. 242(A), 98–105. doi: 10.1016/j.envpol.2018.06.071.
•  Ekino,  S.,  Susa,  M.,  Ninomiya,  T.,  Imamura,  K.,  Kitamura,  T., 2007. Minamata disease revisited: An update on the acute and chronic manifestations of methyl mercury poisoning. J. Neurol. Sci. 262(1–2), 131–144. doi: 10.1016/j.jns.2007.06.036.
•  Ettler,  V.,  Jarošíková,  A.,  Mihaljevič,  M.,  Kříbek,  B.,  Nyambe,  I.,  Kamona,  F.,  Mapani,  B., 2020a. Vanadium in slags from smelting of African Pb-Zn vanadate ores: Mineralogy, extractability and potential recovery. J. Geochem. Explor. 218, 106631. doi: 10.1016/j.gexplo.2020.106631.
•  Ettler,  V.,  Štěpánek,  D.,  Mihaljevič,  M.,  Drahota,  P.,  Jedlicka,  R.,  Kříbek,  B.,  Vaněk,  A.,  Penížek,  V.,  Sracek,  O.,  Nyambe,  I., 2020b. Slag dusts from Kabwe (Zambia): Contaminant mineralogy and oral bioaccessibility. Chemosphere 260, 127642. doi: 10.1016/j.chemosphere.2020.127642.
• Food and Agriculture Organization of the United Nations (FAO), 2012. Joint FAO/WHO food standards programme, codex committee on contaminants in foods. Sixth session. CF/6 INF/1, pp. 1–94, Codex Alimentarius Commission, Maastricht.
• FAO/WHO, 2014. General standards for contaminants and toxins in food and feed (CODEX STAN 193–1995), Codex Alimentarius Commission.
•  Gillis,  B.S.,  Arbieva,  Z.,  Gavin,  I.M., 2012. Analysis of lead toxicity in human cells. BMC Genom. 13(1), 344. doi: 10.1186/1471-2164-13-344.
•  Guernsey,  T.D., 1953. Summary of early prospecting in northern Rhodesia. Trans. Inst. Min. Metall. 63, 1–8.
•  Hamvumba,  R.,  Mataa,  M.,  Mweetwa,  A.M., 2014. Evaluation of sunflower (Helianthus annuus L.), sorghum (Sorghum bicolor L.) and Chinese cabbage (Brassica chinensis) for phytoremediation of Pb contaminated soils. Environ. Pollut. 3(2), 65. doi: 10.5539/ep.v3n2p65.
•  Haq,  F.,  Mahoney,  M.,  Koropatnick,  J., 2003. Signaling events for metallothionein induction. Mutat. Res. 533(1–2), 211–226. doi: 10.1016/j.mrfmmm.2003.07.014.
•  Harada,  M., 1995. Minamata disease: Methylmercury poisoning in Japan caused by environmental pollution. Crit. Rev. Toxicol. 25(1), 1–24. doi: 10.3109/10408449509089885.
•  Ikenaka,  Y.,  Nakayama,  S.M.,  Muzandu,  K.,  Choongo,  K.,  Teraoka,  H.,  Mizuno,  N.,  Ishizuka,  M., 2010. Heavy metal contamination of soil and sediment in Zambia. Afr. J. Environ. Sci. Technol. 4(11), 729–739.
•  Ikenaka,  Y.,  Nakayama,  S.M.,  Muroya,  T.,  Yabe,  J.,  Konnai,  S.,  Darwish,  W.S.,  Muzandu,  K.,  Choongo,  K.,  Mainda,  G.,  Teraoka,  H.,  Umemura,  T.,  Ishizuka,  M., 2012. Effects of environmental Pb contamination on cattle in a Pb/zinc mining area: Changes in cattle immune systems on exposure to Pb in vivo and in vitro. Environ. Toxicol. Chem. 31(10), 2300–2305. doi: 10.1002/etc.1951.
•  Inaba,  T.,  Kobayashi,  E.,  Suwazono,  Y.,  Uetani,  M.,  Oishi,  M.,  Nakagawa,  H.,  Nogawa,  K., 2005. Estimation of cumulative cadmium intake causing Itai-itai disease. Toxicol. Lett. 159(2), 192–201. doi: 10.1016/j.toxlet.2005.05.011.
• Japan Science and Technology Agency, 2021. Sustainable development goals aXis. https://www.jst.go.jp/global/axis/en/field/a_01_ishizuka.html (accessed 15 December 2021)
•  Kamona,  F., 1993. The carbonate hosted Kabwe Pb-Zn deposit, central Zambia: Ph. D (Doctoral dissertation, Rheinisch-Westfalischen Technischen Hoschschule, Aachen, Germany)
•  Kamona,  A.F.,  Lévêque,  J.,  Friedrich,  G.,  Haack,  U., 1999. Lead isotopes of the carbonate-hosted Kabwe, Tsumeb, and Kipushi Pb-Zn-Cu sulphide deposits in relation to Pan African orogenesis in the Damaran-Lufilian fold belt of Central Africa. Miner. Deposita 34(3), 273–283. doi: 10.1007/s001260050203.
•  Kamona,  A.F.,  Friedrich,  G.H., 2007. Geology, mineralogy and stable isotope geochemistry of the Kabwe carbonate-hosted Pb-Zn deposit, Central Zambia. Ore Geol. Rev. 30(3–4), 217–243.
•  Kataba,  A.,  Nakayama,  S.M.M.,  Nakata,  H.,  Toyomaki,  H.,  Yohannes,  Y.B.,  Yabe,  J.,  Muzandu,  K.,  Zyambo,  G.,  Kubota,  A.,  Matsukawa,  T.,  Yokoyama,  K.,  Ikenaka,  Y.,  Ishizuka,  M., 2021. An investigation of the wild rat crown incisor as an indicator of lead (Pb) exposure using inductively couple plasma mass spectrometry (ICP-MS) and laser ablation ICP-MS. Int. J. Environ. Res. Public Health 18(2), 767. doi: 10.3390/ijerph18020767.
•  Kortman,  C.R., 1972. The geology of the Zambia Broken Hill Mine, Kabwe. Geol. Mijnb. 51(3), 347–356.
•  Kříbek,  B.,  Nyambe,  I.,  Majer,  V.,  Knésl,  I.,  Mihaljevič,  M.,  Ettler,  V.,  Vaněk,  A.,  Penížek,  V.,  Sracek,  O., 2019. Soil contamination near the Kabwe Pb-Zn smelter in Zambia: Environmental impacts and remediation measures proposal. J. Geochem. Explor. 197, 159–173. doi: 10.1016/j.gexplo.2018.11.018.
•  Leteinturier,  B.,  Laroche,  J.,  Matera,  J.,  Malaisse,  F., 2001. Reclamation of Pb/zinc processing wastes at Kabwe, Zambia: A phytogeochemical approach. South Afr. J. Sci. 97(11), 624–627.
•  Marques,  C.C.,  Gabriel,  S.I.,  Pinheiro,  T.,  Viegas-Crespo,  A.M.,  da Luz Mathias,  M.,  Bebianno,  M.J., 2008. Metallothionein levels in Algerian mice (Mus spretus) exposed to elemental pollution: An ecophysiological approach. Chemosphere 71(7), 1340–1347. doi: 10.1016/j.chemosphere.2007.11.024.
•  Matović,  V.,  Buha,  A.,  Ðukić-Ćosić,  D.,  Bulat,  Z., 2015. Insight into the oxidative stress induced by lead and/or cadmium in blood, liver and kidneys. Food Chem. Toxicol.: Int. J. Publ. Br. Ind. Biol. Res. Assoc. 78, 130–140. doi: 10.1016/j.fct.2015.02.011.
•  Melcher,  F.,  Oberthür,  T.,  Rammlmair,  D., 2006. Geochemical and mineralogical distribution of germanium in the Khusib Springs Cu-Zn-Pb-Ag sulfide deposit, Otavi Mountain Land, Namibia. Ore Geol. Rev. 28(1), 32–56. doi: 10.1016/j.oregeorev.2005.04.006.
•  Mia,  R.,  Selim,  M.,  Shamim,  A.M.,  Chowdhury,  M.,  Sultana,  S.,  Armin,  M.,  Hossain,  M.,  Akter,  R.,  Dey,  S.,  Naznin,  H., 2019. Review on various types of pollution problem in textile dyeing & printing industries of Bangladesh and recommandation for mitigation. J. Text. Eng. Fash. Technol. 5(4), 220–226. doi: 10.15406/jteft.2019.05.00205.
•  Miranda,  M.L.,  Edwards,  S.E.,  Keating,  M.H.,  Paul,  C.J., 2011. Making the environmental justice grade: The relative burden of air pollution exposure in the United States. Int. J. Environ. Res. Public Health 8(6), 1755–1771. doi: 10.3390/ijerph8061755.
•  Mufalo,  W.,  Tangviroon,  P.,  Igarashi,  T.,  Ito,  M.,  Sato,  T.,  Chirwa,  M.,  Nyambe,  I.,  Nakata,  H.,  Nakayama,  S.,  Ishizuka,  M., 2021. Solid-phase partitioning and leaching behavior of Pb and Zn from playground soils in Kabwe, Zambia. Toxics 9(10), 248. doi: 10.3390/toxics9100248.
•  Mufinda,  B., 2015. A history of mining in Broken Hill (Kabwe): 1902–1929 (Doctoral dissertation, University of the Free State, South Africa)
•  Mwandira,  W.,  Nakashima,  K.,  Kawasaki,  S.,  Ito,  M.,  Sato,  T.,  Igarashi,  T.,  Banda,  K.,  Chirwa,  M.,  Nyambe,  I.,  Nakayama,  S.,  Ishizuka,  M., 2019a. Efficacy of biocementation of Pb mine waste from the Kabwe Mine site evaluated using Pararhodobacter sp. Environ. Sci. Pollut. Res. Int. 26(15), 15653–15664. doi: 10.1007/s11356-019-04984-8.
•  Mwandira,  W.,  Nakashima,  K.,  Kawasaki,  S.,  Ito,  M.,  Sato,  T.,  Igarashi,  T.,  Chirwa,  M.,  Banda,  K.,  Nyambe,  I.,  Nakayama,  S.,  Nakata,  H.,  Ishizuka,  M., 2019b. Solidification of sand by Pb (II). Chemosphere 228, 17–25. doi: 10.1016/j.chemosphere.2019.04.107.
•  Mwandira,  W.,  Nakashima,  K.,  Kawasaki,  S.,  Arabelo,  A.,  Banda,  K.,  Nyambe,  I.,  Chirwa,  M.,  Ito,  M.,  Sato,  T.,  Igarashi,  T.,  Nakata,  H.,  Nakayama,  S.,  Ishizuka,  M., 2020. Biosorption of Pb (II) and Zn (II) from aqueous solution by Oceanobacillus profundus isolated from an abandoned mine. Sci. Rep. 10(1), 21189. doi: 10.1038/s41598-020-78187-4.
•  Mwilola,  P.N.,  Mukumbuta,  I.,  Shitumbanuma,  V.,  Chishala,  B.H.,  Uchida,  Y.,  Nakata,  H.,  Nakayama,  S.,  Ishizuka,  M., 2020. Lead, zinc and cadmium accumulation, and associated health risks, in maize grown near the Kabwe Mine in Zambia in response to organic and inorganic soil amendments. Int. J. Environ. Res. Public Health 17(23), 9038. doi: 10.3390/ijerph17239038.
•  Nachiyunde,  K.,  Ikeda,  H.,  Okuda,  T.,  Nishijima,  W., 2013. Assessment of dissolved heavy metal pollution in five provinces of Zambia. J. Environ. Prot. 4(01), 80–85. doi: 10.4236/jep.2013.41B015.
•  Nakamura,  S.,  Igarashi,  T.,  Uchida,  Y.,  Ito,  M.,  Hirose,  K.,  Sato,  T.,  Mufalo,  W.,  Chirwa,  M.,  Nyambe,  I.,  Nakata,  H.,  Nakayama,  S.,  Ishizuka,  M., 2021. Evaluation of dispersion of lead-bearing mine wastes in Kabwe District, Zambia. Minerals 11(8), 901. doi: 10.3390/min11080901.
•  Nakata,  H.,  Nakayama,  S.M.,  Yabe,  J.,  Liazambi,  A.,  Mizukawa,  H.,  Darwish,  W.S.,  Ikenaka,  Y.,  Ishizuka,  M., 2016. Reliability of stable Pb isotopes to identify Pb sources and verifying biological fractionation of Pb isotopes in goats and chickens. Environ. Pollut. 208(B), 395–403. doi: 10.1016/j.envpol.2015.10.006.
•  Nakata,  H.,  Nakayama,  S.M.M.,  Yabe,  J.,  Muzandu,  K.,  Toyomaki,  H.,  Yohannes,  Y.B.,  Kataba,  A.,  Zyambo,  G.,  Ikenaka,  Y.,  Choongo,  K.,  Ishizuka,  M., 2021a. Clinical biochemical parameters associated with the exposure to multiple environmental metals in residents from Kabwe, Zambia. Chemosphere 262, 127788. doi: 10.1016/j.chemosphere.2020.127788.
•  Nakata,  H.,  Tohyama,  H.,  Fujita,  W.,  Nakayama,  S.M.M.,  Ishizuka,  M.,  Yabe,  J.,  Munyinda,  N.S.,  Sakala,  D.,  Choongo,  K.,  Yamasaki,  S.,  Nagai,  N.,  Yoshida,  T.,  Saito,  T., 2021b. The impact of elevated blood Pb levels in children on maternal health-related quality of life. Chemosphere 279, 130490. doi: 10.1016/j.chemosphere.2021.130490.
•  Nakata,  H.,  Nakayama,  S.M.M.,  Yabe,  J.,  Muzandu,  K.,  Toyomaki,  H.,  Yohannes,  Y.B.,  Kataba,  A.,  Zyambo,  G.,  Ikenaka,  Y.,  Choongo,  K.,  Ishizuka,  M., 2021c. Assessment of LeadCare^® II analysis for testing of a wide range of blood lead levels in comparison with ICP-MS analysis. Chemosphere 271, 129832. doi: 10.1016/j.chemosphere.2021.129832.
•  Nakata,  H.,  Eguchi,  A.,  Nakayama,  S.M.M.,  Yabe,  J.,  Muzandu,  K.,  Ikenaka,  Y.,  Mori,  C.,  Ishizuka,  M., 2022. Metabolomic alteration in the plasma of wild rodents environmentally exposed to lead: A preliminary study. Int. J. Environ. Res. Public Health 19(1), 541. doi: 10.3390/ijerph19010541.
•  Nakayama,  S.M.M.,  Ikenaka,  Y.,  Hamada,  K.,  Muzandu,  K.,  Choongo,  K.,  Teraoka,  H.,  Mizuno,  N.,  Ishizuka,  M., 2011. Metal and metalloid contamination in roadside soil and wild rats around a Pb-Zn mine in Kabwe, Zambia. Environ. Pollut. 159(1), 175–181. doi: 10.1016/j.envpol.2010.09.007.
•  Nakayama,  S.M.,  Ikenaka,  Y.,  Hamada,  K.,  Muzandu,  K.,  Choongo,  K.,  Yabe,  J.,  Umemura,  T.,  Ishizuka,  M., 2013. Accumulation and biological effects of metals in wild rats in mining areas of Zambia. Environ. Monit. Assess. 185(6), 4907–4918. doi: 10.1007/s10661-012-2912-6.
•  Nakayama,  S.M.M.,  Nakata,  H.,  Ikenaka,  Y.,  Yabe,  J.,  Oroszlany,  B.,  Yohannes,  Y.B.,  Bortey-Sam,  N.,  Muzandu,  K.,  Choongo,  K.,  Kuritani,  T.,  Nakagawa,  M.,  Ishizuka,  M., 2019. One year exposure to Cd- and Pb-contaminated soil causes metal accumulation and alteration of global DNA methylation in rats. Environ. Pollut. 252(B), 1267–1276. doi: 10.1016/j.envpol.2019.05.038.
•  Nriagu,  J.O., 1992. Toxic metal pollution in Africa. Sci. Total Environ. 121, 1–37. doi: 10.1016/0048-9697(92)90304-B.
•  Nwankwo,  J.N.,  Elinder,  C.G., 1979. Cadmium, lead, and zinc concentrations in soils and in food grown near a zinc and lead smelter in Zambia. Bull. Environ. Contam. Toxicol. 22(4–5), 625–631. doi: 10.1007/BF02026998.
•  Pang,  Y.L.,  Abdullah,  A.Z., 2013. Current status of textile industry wastewater management and research progress in Malaysia: A review. CLEAN-Soil, Air, Water 41(8), 751–764. doi: 10.1002/clen.201000318.
•  Park,  S.S.,  Skaar,  D.A.,  Jirtle,  R.L.,  Hoyo,  C., 2017. Epigenetics, obesity and early-life cadmium or lead exposure. Epigenomics 9(1), 57–75. doi: 10.2217/epi-2016-0047.
•  Porter,  M.E.,  Kramer,  M.R., 2019. Creating shared value, In: Managing sustainable business, pp. 323–346, Springer, Dordrecht.
• Regulation Council, 2001. No 2375/2001 of 29 November 2001 amending Commission Regulation (EC) No 466/2001 setting maximum levels for certain contaminants in foodstuffs. Off. J. Eur. Commun. L. 321(1), 6–12.
•  Reilly,  A.,  Reilly,  C., 1972. Patterns of Pb pollution in the Zambian environment. Med. J. Zambia;(Zambia), 125–127. doi: 10.1007/978-94-024-1144-7_16.
•  Ruckart,  P.Z.,  Jones,  R.L.,  Courtney,  J.G.,  LeBlanc,  T.T.,  Jackson,  W.,  Karwowski,  M.P.,  Cheng,  P.Y.,  Allwood,  P.,  Svendsen,  E.R.,  Breysse,  P.N., 2021. Update of the blood lead reference value–United States, 2021. MMWR. Morb. Mortal. Wkly Rep. 70(43), 1509–1512.
•  Silwamba,  M.,  Ito,  M.,  Hiroyoshi,  N.,  Tabelin,  C.B.,  Hashizume,  R.,  Fukushima,  T.,  Park,  I.,  Jeon,  S.,  Igarashi,  T.,  Sato,  T.,  Chirwa,  M.,  Banda,  K.,  Nyambe,  I.,  Nakata,  H.,  Nakayama,  S.,  Ishizuka,  M., 2020a. Recovery of Pb and zinc from zinc plant leach residues by concurrent dissolution-cementation using zero-valent aluminum in chloride medium. Metals 10(4), 531. doi: 10.3390/met10040531.
•  Silwamba,  M.,  Ito,  M.,  Hiroyoshi,  N.,  Tabelin,  C.B.,  Fukushima,  T.,  Park,  I.,  Jeon,  S.,  Igarashi,  T.,  Sato,  T.,  Nyambe,  I.,  Chirwa,  M.,  Banda,  K.,  Nakata,  H.,  Nakayama,  S.,  Ishizuka,  M., 2020b. Detoxification of Pb-bearing zinc plant leach residues from Kabwe, Zambia by coupled extraction-cementation method. J. Environ. Chem. Eng. 8(4), 104197. doi: 10.1016/j.jece.2020.104197.
•  Sracek,  O.,  Veselovský,  F.,  Kříbek,  B.,  Malec,  J.,  Jehlička,  J., 2010. Geochemistry, mineralogy and environmental impact of precipitated efflorescent salts at the Kabwe Cu-Co chemical leaching plant in Zambia. Appl. Geochem. 25(12), 1815–1824. doi: 10.1016/j.apgeochem.2010.09.008.
•  Tangviroon,  P.,  Noto,  K.,  Igarashi,  T.,  Kawashima,  T.,  Ito,  M.,  Sato,  T.,  Mufalo,  W.,  Chirwa,  M.,  Nyambe,  I.,  Nakata,  H.,  Nakayama,  S.,  Ishizuka,  M., 2020. Immobilization of Pb and zinc leached from mining residual materials in Kabwe, Zambia: Possibility of Chemical Immobilization by dolomite, calcined dolomite, and magnesium oxide. Minerals 10(9), 763. doi: 10.3390/min10090763.
•  Tembo,  B.D.,  Sichilongo,  K.,  Cernak,  J., 2006. Distribution of copper, lead, cadmium and zinc concentrations in soils around Kabwe town in Zambia. Chemosphere 63(3), 497–501. doi: 10.1016/j.chemosphere.2005.08.002.
•  Toyomaki,  H.,  Yabe,  J.,  Nakayama,  S.M.M.,  Yohannes,  Y.B.,  Muzandu,  K.,  Liazambi,  A.,  Ikenaka,  Y.,  Kuritani,  T.,  Nakagawa,  M.,  Ishizuka,  M., 2020. Factors associated with Pb (Pb) exposure on dogs around a Pb mining area, Kabwe, Zambia. Chemosphere 247, 125884. doi: 10.1016/j.chemosphere.2020.125884.
•  Toyomaki,  H.,  Yabe,  J.,  Nakayama,  S.M.M.,  Yohannes,  Y.B.,  Muzandu,  K.,  Mufune,  T.,  Nakata,  H.,  Ikenaka,  Y.,  Kuritani,  T.,  Nakagawa,  M.,  Choongo,  K.,  Ishizuka,  M., 2021. Lead concentrations and isotope ratios in blood, breastmilk and feces: Contribution of both lactation and soil/dust exposure to infants in a Pb mining area, Kabwe, Zambia. Environ. Pollut. 286, 117456. doi: 10.1016/j.envpol.2021.117456.
•  Tsuchiya,  K., 1969. Causation of Ouch-Ouch disease (Itai-Itai Byo)-An introductory review-Part I. Nature of the disease. Keio J. Med. 18(4), 181–194.
•  Turner,  A., 1979, Ph.D thesis. A socio-economic history of Kabwe 1902–1966. University of California, USA.
•  Uchida,  Y.,  Banda,  K.,  Nyambe,  I.,  Hamamoto,  T.,  Yoshii,  Y.,  Munthali,  K.,  Mwansa,  M.,  Mukula,  M.,  Mutale,  M.,  Yabe,  J.,  Toyomaki,  H.,  Beyene,  Y.B.,  Nakayama,  S.M.,  Naruse,  N.,  Ishizuka,  M.,  Takahashi,  Y., 2017. Multidisciplinary field research in Kabwe, Zambia, towards better understanding of lead contamination of the city-A short report from a field survey. bioRxiv, 096164. doi: 10.1101/096164.
• United Nations Development Programme (UNDP), 2015. Sustainable development goals, UNDP, USA. https://www.undp.org/content/dam/undp/library/corporate/brochure/SDGs_Booklet_Web_En.pdf (accessed 15 December 2021)
•  Unrug,  R., 1988. Mineralization controls and source of metals in the Lufilian fold belt, Shaba (Zaire), Zambia, and Angola. Econ. Geol. 83(6), 1247–1258. doi: 10.2113/gsecongeo.83.6.1247.
• US Environmental Protection Agency (USEPA), 2001. Lead, Identification of Dangerous Levels; Final Rule (40 CFR Part 745), USEPA, USA. https://www.federalregister.gov/documents/2001/01/05/01-84/Pb-identification-of-dangerous-levels-of-Pb (accessed 15 December 2021)
• US Environmental Protection Agency, 2020. Lead in soil, USEPA, USA. https://www.epa.gov/sites/default/files/2020-10/documents/Pb-in-soil-aug2020.pdf (accessed 15 December 2021)
• US Environmental Protection Agency, 2021. Monitoring requirements for Pb and copper in tap water (40 CFR 141.86), USEPA, USA. https://www.federalregister.gov/documents/2021/01/15/2020-28691/national-primary-drinking-water-regulations-Pb-and-copper-rule-revisions (accessed 15 December 2021)
•  Veysseyre,  A.M.,  Bollho,  A.F., 2001. Tracing the origin of pollution in French alpine snow and aerosols using Pb isotopic ratios. Environ. Sci. Technol. 35(22), 4463e4469. doi: 10.1021/es0105717.
•  Wang,  Z.,  Xu,  X.,  He,  B.,  Guo,  J.,  Zhao,  B.,  Zhang,  Y.,  Zhou,  Z.,  Zhou,  X.,  Zhang,  R.,  Abliz,  Z., 2019. The impact of chronic environmental metal and benzene exposure on human urinary metabolome among Chinese children and the elderly population. Ecotoxicol. Environ. Saf. 169, 232–239. doi: 10.1016/j.ecoenv.2018.11.016.
•  Wani,  A.L.,  Ara,  A.,  Usmani,  J.A., 2015. Lead toxicity: A review. Interdiscip. Toxicol. 8(2), 55–64. doi: 10.1515/intox-2015-0009.
• Water Management Consultants Ltd., 2005. Copperbelt Environment Project, Kabwe scoping and design study phase 2 report: Geochemical hazard screening and human risk analysis, Water Management Consultants Ltd, UK.
• World Bank, 2021. Zambia, Mining and Environmental Remediation and Improvement Project. https://projects.worldbank.org/en/projects-operations/project-detail/P154683 (accessed 15 December 2021)
• World Health Organization (WHO), 2009. Global health risks: Mortality and burden of disease attributable to selected major risks, WHO, Switzerland. http://whqlibdoc.who.int/publications/2009/9789241563871_eng.pdf (accessed 31 December 2021)
• World Health Organization, 2014. Chemicals of public health concern in the African Region and their management: Regional Assessment Report, WHO, Switzerland. https://www.afro.who.int/sites/default/files/2017-06/9789290232810.pdf (accessed 15 December 2021)
•  Yabe,  J.,  Nakayama,  S.M.,  Ikenaka,  Y.,  Muzandu,  K.,  Ishizuka,  M.,  Umemura,  T., 2011. Uptake of Pb, cadmium, and other metals in the liver and kidneys of cattle near a Pb-zinc mine in Kabwe, Zambia. Environ. Toxicol. Chem. 30(8), 1892–1897. doi: 10.1002/etc.580.
•  Yabe,  J.,  Nakayama,  S.M.,  Ikenaka,  Y.,  Muzandu,  K.,  Choongo,  K.,  Mainda,  G.,  Kabeta,  M.,  Ishizuka,  M.,  Umemura,  T., 2013. Metal distribution in tissues of free-range chickens near a Pb-zinc mine in Kabwe, Zambia. Environ. Toxicol. Chem. 32(1), 189–192. doi: 10.1002/etc.2029.
•  Yabe,  J.,  Nakayama,  S.M.M.,  Ikenaka,  Y.,  Yohannes,  Y.B.,  Bortey-Sam,  N.,  Oroszlany,  B.,  Muzandu,  K.,  Choongo,  K.,  Kabalo,  A.N.,  Ntapisha,  J.,  Mweene,  A.,  Umemura,  T.,  Ishizuka,  M., 2015. Lead poisoning in children from townships in the vicinity of a Pb-zinc mine in Kabwe, Zambia. Chemosphere 119, 941–947. doi: 10.1016/j.chemosphere.2014.09.028.
•  Yabe,  J.,  Nakayama,  S.M.M.,  Ikenaka,  Y.,  Yohannes,  Y.B.,  Bortey-Sam,  N.,  Kabalo,  A.N.,  Ntapisha,  J.,  Mizukawa,  H.,  Umemura,  T.,  Ishizuka,  M., 2018. Lead and cadmium excretion in feces and urine of children from polluted townships near a Pb-zinc mine in Kabwe, Zambia. Chemosphere 202, 48–55. doi: 10.1016/j.chemosphere.2018.03.079.
•  Yabe,  J.,  Nakayama,  S.M.,  Nakata,  H.,  Toyomaki,  H.,  Yohannes,  Y.B.,  Muzandu,  K.,  Kataba,  A.,  Zyambo,  G.,  Hiwatari,  M.,  Narita,  D.,  Yamada,  D.,  Hangoma,  P.,  Munyinda,  N.S.,  Mufune,  T.,  Ikenaka,  Y.,  Choongo,  K.,  Ishizuka,  M., 2020. Current trends of blood Pb levels, distribution patterns and exposure variations among household members in Kabwe, Zambia. Chemosphere 243, 125412. doi: 10.1016/j.chemosphere.2019.125412.
•  Yamada,  D.,  Hiwatari,  M.,  Hangoma,  P.,  Narita,  D.,  Mphuka,  C.,  Chitah,  B.,  Yabe,  J.,  Nakayama,  S.M.M.,  Nakata,  H.,  Choongo,  K.,  Ishizuka,  M., 2020. Assessing the population-wide exposure to Pb pollution in Kabwe, Zambia: An econometric estimation based on survey data. Sci. Rep. 10(1), 15092. doi: 10.1038/s41598-020-71998-5.
•  Yamazaki,  J.,  Toyomaki,  H.,  Nakayama,  S.M.M.,  Yabe,  J.,  Muzandu,  K.,  Jelinek,  J.,  Yokoyama,  S.,  Ikenaka,  Y.,  Takiguchi,  M.,  Ishizuka,  M., 2021. Genome-wide DNA methylation analysis of dogs with high Pb exposure living near a Pb mining area in Kabwe, Zambia. Environ. Pollut. 286, 117229. doi: 10.1016/j.envpol.2021.117229.
•  Yohannes,  Y.B.,  Nakayama,  S.M.,  Yabe,  J.,  Nakata,  H.,  Toyomaki,  H.,  Kataba,  A.,  Muzandu,  K.,  Ikenaka,  Y.,  Choongo,  K.,  Ishizuka,  M., 2020. Blood Pb levels and aberrant DNA methylation of the ALAD and p16 gene promoters in children exposed to environmental-Pb. Environ. Res. 188, 109759. doi: 10.1016/j.envres.2020.109759.
•  Yohannes,  Y.B.,  Nakayama,  S.M.,  Yabe,  J.,  Toyomaki,  H.,  Kataba,  A.,  Nakata,  H.,  Muzandu,  K.,  Ikenaka,  Y.,  Choongo,  K.,  Ishizuka,  M., 2021a. Glutathione S-transferase gene polymorphisms in association with susceptibility to Pb toxicity in Pb- and cadmium-exposed children near an abandoned Pb-zinc mining area in Kabwe, Zambia. Environ. Sci. Pollut. Res. 1–11. doi: 10.1007/s11356-021-16098-1.
•  Yohannes,  Y.B.,  Nakayama,  S.M.M.,  Yabe,  J.,  Toyomaki,  H.,  Kataba,  A.,  Nakata,  H.,  Muzandu,  K.,  Ikenaka,  Y.,  Choongo,  K.,  Ishizuka,  M., 2021b. Delta-aminolevulinic acid dehydratase (ALAD) and vitamin D receptor (VDR) genes polymorphisms in children residing in an abandoned Pb-zinc mine area in Kabwe, Zambia. Meta Gene 27, 100838. doi: 10.1016/j.mgene.2020.100838.
•  Yoshii,  Y.,  von Rein,  I.,  Munthali,  K.,  Mwansa,  M.,  Nakata,  H.,  Nakayama,  S.,  Ishizuka,  M.,  Uchida,  Y., 2020. Evaluation of phytoremediation effects of chicken manure, urea and lemongrass on remediating a Pb contaminated soil in Kabwe, Zambia. South Afr. J. Plant Soil 37(5), 351–360. doi: 10.1080/02571862.2020.1772386.
• Zambia copper and Cobalt Mining-Investment Holding Plc. (ZCCM-IH), 2002. Environmental Assessment of the Copperbelt and Kabwe area, ZCCM-IH, Zambia. https://documents1.worldbank.org/curated/en/468161468764056541/pdf/E5390vol-2.pdf (accessed 15 December 2021)
•  Zingani,  E.,  Ndhlovu,  G.,  Chiluba,  B.C., 2020. Assessment of lead content in soil samples obtained from four different sites of Kabwe, Central Province of Zambia. Int. J. Environ. Sustain. Soc. Sci. 1(1), 41–46.