Heavy metals research in Nigeria: a review of studies and prioritization of research needs

Nigeria is experiencing continuous economic and industrial transformations, typical of many developing nations. In addition to its well-established oil industry, which is infamous for exuding various kinds of pollutants, there are increased mining operations, indiscriminate disposal and burning of wastes, illegal oil refinery and terroristic insurgency, all poised to increase the levels of heavy metal contaminants in the Nigerian environment. A recent revelation indicates that about 2 million people in South-western Nigeria alone could potentially be poisoned by lead (Pb) and mercury (Hg), emanating from illegal mining operations. This further underscores the importance of investigations of toxic trace metal levels in the country. The current review of 148 research articles was conducted to provide an understanding of the scope of heavy metals research in Nigeria and to prioritize needed research. The review recognized that the scope of heavy metals studies has been wide, covering matrices such as cosmetics, human blood, hair, medicines, foods, beverages, water, air, soil and crude oil. However, important toxic metals, especially mercury (Hg), arsenic (As) and antimony (Sb), are largely under-investigated. Also, there is a need for more studies to be conducted in the northern part of the country. Furthermore, studies need to focus on marine environments rather than the freshwater ecosystems alone. Techniques such as the inductively coupled plasma-optical emission spectrometry (ICP-OES) and particle-induced X-ray emission (PIXE) analyses are herein recommended to bridge the data gap and to overcome limitations in trace metals analyses in the Nigerian total environment.


Introduction
The term 'heavy metals' is used widely to refer to a group of metals and semimetals (metalloids) that have been associated with contamination and potential toxicity to the environment and to various species of organisms. They have specific gravities greater than 5 g/cm 3 or specific gravity at least five times that of water and are known to exist naturally in the Earth's crust (Duffus 2002). More recently, the definition has been broadened to include naturally occurring elements with atomic number greater than 20 (Ali and Khan 2018;Ali et al. 2019).
Heavy metals are broadly grouped into essential and non-essential elements. The essential ones include iron (Fe), manganese (Mn), copper (Cu), zinc (Zn), cobalt (Co), nickel (Ni), molybdenum (Mo) and selenium (Se). They are so-called because they are required by living organisms for fundamental metabolic activities. Many of them serve as cofactors that are functionally and structurally important for enzymes and enzyme-catalysed biochemical reactions, and this is true for many life forms. However, presence of these 'essential' metals above certain levels in organisms results in deleterious physiological effects. The non-essential heavy metals have no known benefits to the living systems and many of them are toxic at low concentrations. Non-essential heavy metals include lead (Pb), cadmium (Cd), mercury (Hg), arsenic (As), tin (Sn), aluminium (Al), silver (Ag), gold (Au), antimony (Sb), bismuth (Bi), palladium (Pd), platinum (Pt), vanadium (V), strontium (Sr), tellurium (Te), titanium (Ti), Uranium (U) and chromium (Cr), particularly the hexavalent form (Cr VI) (Tchounwou et al. 2012). Concerns about heavy metals arise from the fact that they may find their ways into the food chain, through bioaccumulation in plants and animal species, or they may contaminate drinking water sources. The latter is particularly through of developing nations (e.g. Nigeria), where many rural communities depend on open and unprotected surface water sources for drinking, domestic and recreational purposes.
Toxicity effects of heavy metals manifest in various forms. For example, the ability of Cu to change between Cu(I) and Cu(II) oxidation states in living systems enables it to function as cofactor for many oxidative stress-related cuproenzymes such as superoxide dismutase, cytochrome oxidases and ferroxidases. However, this ability to transit between oxidation states also makes Cu toxic, since the process may generate superoxide and hydroxyl radicals (Harvey and McArdle 2008;Stern 2010). Thus, excessive exposure to Cu causes cellular and tissue damages, resulting in Wilson disease in humans (Tchounwou et al. 2012). Pb exerts its toxicity effect by mimicking and inhibiting Ca ions and by interacting with proteins. It therefore affects the central nervous system and vitamin D metabolism and causes reproductive impairments, brain and kidney damages, as well as gastro-intestinal diseases (Flora et al. 2006;Wani et al. 2015).
The vast majority of heavy metals are present naturally in the environment. However, the public and environmental health concerns associated with them stem mainly from the levels introduced by anthropogenic activities. Heavy metals emanate from industrial effluents, mining, smelting of iron, combustion of fossil fuels, waste and biomass burning, manufacturing, use and disposal of electronic gadgets and a host of other human-initiated processes. While many of these activities also go on in the developed nations, as they do in the developing economies, the poor enforcement of environmental laws, coupled with the indiscriminate proliferation of small-scale manufacturing businesses and the lack of efficient recycling programme, makes the environment in developing nations particularly susceptible to heavy metals contamination.
In Nigeria, fairly recent cases of heavy metals poisoning and potential significant pollution by heavy metals make their continuous monitoring worthwhile. The largest known incidence of lead poisoning in history, killing 163 people (including 111 children), took place in Zamfara villages, Northern Nigeria in 2010 (CDC 2016). Unauthorized and illegal mining of gold ores, apparently containing high levels of Pb, caused widespread contamination of soil and drinking water sources with Pb. High concentration of Pb was detected in the blood of children, many of whom had suffered from headaches, vomiting, abdominal pains, seizures and death (Orisakwe et al. 2017). The Pb contamination spread across eight villages, namely Bagega, Dareta, Yargalma, Abare, Tungar Daji, Tungar Guru, Duza and Sunke. More recently, artisanal mining operations, similar to that in Zamfara State have been spreading across the country, and a recent investigation suggests that about two million people in South-western Nigeria may be at risk of Pb and Hg poisoning (Vanguard 2021). Beyond artisanal mining, there is potential for toxic metals emanating from various activities in the country to enter the food chain, leading to significant chronic/long-term human exposure. This necessitated numerous individual studies which determined heavy metals in all kinds of samples. In this review, an attempt is made to summarize investigations into heavy metals in Nigeria over the past 22 years, with a view to understanding the full scope of studies so far and to identify important research gaps.
Previous reviews on heavy metals studies in Nigeria have been limited in scope. Onakpa et al. (2018) reviewed heavy metals contamination of food crops in Nigeria. Musa et al. (2017) focussed their review on studies that reported the contamination of agricultural soils by heavy metals. Review of contamination of potable water sources and beverages were conducted by Izah et al. (2016) and Izah et al. (2017), respectively. While these reviews have focussed mostly on food items and water, understandably because they are obvious sources of exposure of humans to these toxic substances, they do not provide the full scope of research into heavy metals contamination in Nigeria. This is important to identify knowledge gaps in trace metal investigations in the country and to provide an understanding of the levels reported in other exposure sources (e.g. cosmetics, herbal medicines, orthodox medicines, air) and in human body/fluid samples, which are all covered in this review. The review therefore attempts to exhaustively summarize the investigations of heavy metals in all matrix types and environmental phases reported so far in Nigeria.

Literature search
Literature search for studies on heavy metals in Nigeria was performed in Scopus, Google scholar, PubMed and ResearchGate databases in the month of November in year 2021. Key phrases used in the search were as follows: heavy metal research in Nigeria; heavy metals in the Nigerian environment; heavy metals in the atmosphere/air in Nigeria; heavy metals in cosmetics in Nigeria; heavy metals in human samples in Nigeria; heavy metals in water in Nigeria; heavy metals in foods in Nigeria; heavy metals in soil and sediments in Nigeria; heavy metals in medicine and drugs in Nigeria; heavy metals in aquatic biota in Nigeria; and heavy metals in all matrices in Nigeria. The search was also conducted with the phrase 'heavy metals' replaced with other similar terms such as 'trace elements', 'toxic elements' and 'potentially toxic metals', which are also commonly used in publications. The search was performed independently in each database and the results were compared and collated.

Article selection criteria
Articles that reported concentrations of heavy metals in various matrices in Nigeria were sought for. Article information such as title and abstracts were scrutinized and the irrelevant ones, such as those reporting on phytoremediation of heavy metals, were excluded. Only articles published within the last 22 years (i.e. from years 2000 to 2021) were retained from each database. Furthermore, in order for the final review to reflect the most up-to-date data and information, as well as the latest trend of research on heavy metals in the country, priority was given to articles published within the last three years (up to November, 2021). In instances where two or more papers reported on the same sample types, the latest of the publications was retained in order to keep the total number of the articles for review within a sizable/reasonable amount. After applying the selection criteria and eliminating irrelevant articles, a total of 148 were left from an initial 197 articles obtained via the database search.
The full scheme of selection of the 148 reviewed articles is shown in Fig. 1. The 148 articles were then read in sufficient details during the review and draft preparation (December 2021to March 2022. Apart from the 148 articles that were actually reviewed and analysed, additional 36 articles were cited while discussing the findings of the review under the various subheadings.

Distribution of heavy metals research articles reviewed
Distribution of articles reviewed is considered with respect to the year of publication and the geopolitical zone of Nigeria where the study was conducted. Figure 2 shows the distribution of the journal articles reviewed according to the years of publication. All articles that reported levels of heavy metals in Nigeria and published within the last 4 years (2019-2022) were retained to provide current data and current research trends.
The 78 articles in this category constitute 52.7% of the 148 articles reviewed. These 78 articles were all published after the last review on the subject by Onakpa et al. (2018) which focussed on food contamination aspect only, thereby making this review an important update on heavy metal research in Nigeria. Articles published from years 2000-2004, 2005-2009, 2010-2015 and 2016-2018 represent 1.35%, 7.43%, 18.91% and 19.59% of the reviewed articles, respectively.
Nigeria is divided into six distinct geo-political zones for the purpose of governmental administration. Table 1 presents details of studies that reported heavy metals from the regions and shows a list of the heavy metals that were reported from each region. It should be noted that the summation of the number of articles from the regions shown in Table 1 exceed 148, because some studies determined heavy metals in samples obtained from more than one geopolitical zones.

Heavy metals in cosmetics and personal care products
Manufacturers of cosmetics and skin care products often incorporate substances that could impart substantial amount of heavy metals onto the products. Relevant items to which such substances are incorporated include lip sticks, body creams, sunscreen products, talcum and brown powder, eye shadow, shampoos and concealers. For example, zinc (as the oxide) is widely used in sunscreens, diaper ointments, moisturizers, shampoos and concealers; chromium is used in some products as a colorant; and iron oxides are commonly used as colorants in eye shadows, blushes and concealers .
Despite the prohibition of Pb, As, Cd, Co, Sb, Hg, Ni and Cr in cosmetics, many producers still include compounds that contain these metals at levels above the WHO permissible limits. Table 2 provides a summary of studies that have investigated levels of some heavy metals in cosmetics and personal care products (PCPs) marketed in Nigeria. Usman et al. (2021) determined concentrations of Pb, Co, Cu, Cr and Ni on various kinds of cosmetic products in Nigeria and found high concentrations of Co and Pb in face powders and eye shadows, respectively. The study also found that the concentrations of Cr in eyeshadow, lipstick and face powders were above the USEPA and USFDA permissible limits. Odukudu et al. (2014) investigated the concentration of heavy metals in toothpaste, cosmetics, tissue papers and hair relaxers. Cd and Cr, which are not permitted to be used in personal care products, were present at high concentrations up to 0.68 and 0.76 mg/kg (or ppm), respectively, in the products. Oyekunle et al. (2021) worked on native black soaps and conventional soaps and reported high Hg concentrations of 273.6 and 55.12 µg/g maximum values, respectively, in the soaps. While noting that highly mercuric soaps are effective against fungi and bacteria, the authors cautioned that such products would only be safe if restricted to occasional use by adults and children. Cd, another very toxic metal, was also detected in the soaps, although at much lower concentrations compared to those of Hg. Despite the fact that Zn is an essential element, the study reported values for Zn that raise safety concerns, due to potential cumulative dermal exposure to such high concentrations of the metal.
In addition to studies that investigated the heavy metals directly in cosmetics and PCPs, Eneh (2021a) analysed urine and serum samples of female students in a selected Nigerian population to assess impacts of the use of cosmetics on trace metals absorption into the body. The study found that the mean concentration of Hg (25.9 µg/dL), Pb (17.3 µg/dL) and As (166.0 µg/L) in the urine of students who had consistently used make-up were higher than those who did not wear make-ups. The study points to the negative impact of the use of contaminated cosmetic products on body's burden of these toxic metals.

Heavy metals in the atmosphere
Heavy metal presence in atmospheric air may result from combustion of fossil fuel. They could also emanate from non-exhaust sources like wear and tear of vehicle brakes and tyres and from a host of other anthropogenic activities . Metals may exist in form of vapour in the air, thereby increasing the chance of being inhaled by humans. Studies which investigated toxic metals in air in Nigeria have done so relative to metals bound to particulate matters (PM). Uzoekwe et al. (2021) investigated heavy metal presence and levels in particulate matters (PM 10 )   inhalation exposure cancer risks for adults and children, which were well above the acceptable range of 10 −6 to 10 −4 , indicating significant contribution of the industrial activities to the levels of suspended metals in air. The study also reported that Cu and Cr exist in the exchangeable form and would be readily transferred to the human system if the particulate matters were inhaled. Ogundele et al. (2017) investigated nine heavy metals (Pb, Mn, Cd, Zn, Cr, As, Ni, Cu and Fe) in air PM around iron and smelting companies in Ile-Ife, Osun State. Concentrations of Cd, Pb, Mn and Ni in the samples were found to exceed both WHO and USEPA guideline safety limits, resulting in the deterioration status confirmed by various pollution indices. Following months of black soot enveloping the atmosphere in Port-Harcourt, the city of oil and refineries in Southern Nigeria, Kalagbor et al. (2019) determined heavy metals in the soot samples collected from residential areas. Concentrations of all the metals were higher than those in unpolluted control samples, while also exceeding WHO standard limits. In particular, Cd and Pb levels were significantly high and cancer risk assessments suggested that children in the city were at risk of developing various types of cancers (Kalagbor et al. 2019).
There have also been reports of heavy metal presence in the atmosphere in Northern Nigeria. Mafuyai et al. (2014) determined heavy metals (Pb, Cr, Fe, Mn, Cd, Zn, Cu and Ni) in respirable dusts from seven locations within Jos metropolis, Plateau State, over a period of 3 months. Concentrations of Cd, Ni and Mn were found to greatly exceed the WHO recommended limits for the metals in respirable dusts. The study attributed the presence of the metals in the samples to vehicular traffic and wastes incineration in the city (Mafuyai et al. 2014). Ayua et al. (2020) also investigated heavy metals in respirable dust and PM around industrial sites in Kano, Kaduna and Jos. Concentrations of Cd, Ni and Pb were found to be above the WHO set standard limits in some of the areas studied. The study reported strong correlation between PM and the heavy metals, thereby confirming that the contaminants indeed originated from the industrial activities. This finding also gives credence to the use of sampled air-suspended PM for the evaluation of heavy metal levels in air, as reported by most of the studies.

Heavy metals in ground waters, surface waters and aquatic biota species
The review revealed that water is one of the most studied environmental phases, with respect to investigations of heavy metals contamination in Nigeria. Numerous studies have considered this phase from various perspectives and motivated by different reasons. For instance, only about 10% of Nigerians have access to centrally managed clean pipe-borne water; the majority of Nigerian homes depend on underground waters, accessed via hand-dug wells and mechanically drilled borehole facilities (Idowu et al. 2022). Many rural populations also depend on water abstracted from unprotected surface sources such as streams and rivers. This situation, coupled with poor enforcement of environmental laws, which potentially exposes these water resources to contamination by various industrial and municipal wastes, has formed part of the motivation for many studies investigating levels of heavy metals in water samples. Additionally, unprotected and unmanaged streams and rivers often serve as means of recreation (i.e. swimming) to people in rural Nigeria, with the potential hazard of ingesting waters contaminated with toxic metals. Denkok et al. (2021) determined heavy metals in various water samples, including ground water and factorypackaged satchet water, in Jos, Plateau State. The authors found that the levels of Pb, Cd, Cr and Cu were higher than their respective WHO allowable limits in drinking water. Adeyemi and Ojekunle investigated heavy metal concentrations in underground waters (which provide drinking water to people) around industrial estates in Ogun State. High concentrations of Pb, Fe, Ni and Cr were measured in the samples, with the total hazard index (HI) showing high risk across different age groups and particularly for infants. On the other hand, Enuneku et al. (2018) worked on water samples from boreholes sited close to some dumpsites in Benin City, Nigeria. Based on the metals pollution indices and the estimated daily dosage through drinking, it was established that the levels of metals in the boreholes posed no threat to the health of the people. Afolayan (2018) reported heavy pollution of surface waters in Ibadan with Pb, Cd and Fe, due to the presence of a battery waste dumpsite from which these metals leach to the surface water. Odebunmi et al. (2014) worked on various ground and surface water samples from different locations in Osun State and found that the toxic metals (Pb, Hg, As and Cd) were all higher than WHO permissible limit for drinking water. Because many Nigerian homes harvest rainwater for drinking during the rainy season, Olabanji and Adeniyi (2005) investigated heavy metals content of rain water, comparing levels in free-fall rain water to those harvested via roof tops. The study found that the metal concentrations were higher in roof-harvested rain water, with the metals content reflecting the metallic composition of the roofing material. However, levels in both water types were within safe limits and were lower than those determined for the neighbouring surface waters, packaged table waters and vegetation-intercepted rainwater. Ekere et al. (2014) determined levels of As, Cd, Hg, Pb, Cr, Fe and Cu in water samples from streams, lakes/ponds and hand-dug wells in rural parts of South-eastern Nigeria. the result showed that except for Hg, other showed above the permissible limit of drinking water. The total hazard index of the metals, assessed through human oral water consumption, indicated that the water sources were mostly of high risk. As an example of studies that sought to determine seasonal variation of heavy metals in environmental matrices, Achi et al. (2021) investigated levels of Fe, Mn, Zn, Cu, Cd, Cr, Pb and Ni in water samples from Ogbere River, in Ibadan South-western Nigeria. Significant variation was observed for Mn, Fe, Pb, Cr and Cd, with concentrations higher in the dry season samples than in the wet season samples.
Closely related to studies on surface waters are those examining concentrations of heavy metals in fish and other aquatic fauna. Such studies are important because they reveal the level of exposure of the organisms to toxic trace metals, which may also be passed on to humans through the food chain. Indeed, Nigerians in rural areas freely obtain food resources from many rivers and streams. Also, the use of contaminated waters for fish cultivation may result in the presence of heavy metals in fish species sold and consumed locally. Abalaka et al. (2020) determined concentrations of heavy metals in samples of Clarias gariepinus (common catfish) and Synodontis clarias (mandi) obtained at Kado fish market Abuja (north central) Nigeria. Concentrations of Cr, Fe, Cd and Cu exceeded their permissible limits, while evidence of bioaccumulation in liver was obtained for Zn, Cr, Fe and Cu. Obasohan and Eguavoen (2008) studied heavy metal levels in Erpetoichthys calabaricus (freshwater reed fish) in Ogba River, Benin City. The authors determined and compared dry and rainy season concentrations of Cu, Mn, Zn, Cr, Ni and Pb in the fish. Concentrations of the metals in the fish were all higher than in the river water, pointing to a bioaccumulation effect of metals in this fish species. The study also reported that both dry and rainy season levels of Cu, Mn and Ni exceeded their WHO permissible limits for the metals in food. Bawuro et al. (2018) investigated levels of Zn, Pb, Cd and Cu in fish species from Geriyo Lake in Adamawa State and found high concentrations of Pb, above permissible limit, in Clarias anguillaris and Heterotis niloticus species. Similar studies were conducted by Wegwu and Akaninwor (2006), Oguguah and Ikegwu (2017) and Olayinka-Olagunju et al. (2021) on fish resources in new Calabar River, Lagos Lagoon and Ogbese River (Ondo State), respectively. Wegwu and Akaninwor (2006) further demonstrated that heavy metal presence, even at concentrations below those determined in the Nigerian rivers, caused death of fishes and inhibited hatching of their eggs. A number of studies (for example Aiyesanmi et al. 2010;Anani and Olomukoro 2017;Aduwo and Adeniyi 2018;Ogundele et al. 2019; have also reported levels of heavy metals in river sediments, the bottom layer comprising soil, dead and decayed plant and animal materials, onto which metals are significantly adsorbed and may be resuspended into the water column.

Heavy metals in foods and beverages
Plants growing on contaminated soils may bioaccumulate heavy metals from the soil and translocate it from the root to other parts of the plant. This principle is employed in phytoremediation of lands contaminated with heavy metals. In Nigeria, edible crop plants are sometimes grown on river floodplains, which receive deposits of wastes and contaminants (including heavy metals) during flooding events . Metals from the soil may then transfer to vegetables and food crops growing on the floodplains. Additionally, edible crops and vegetables are found growing around waste dumpsites and factories, with the tendency of toxic metals being transferred from the soil into various plant parts. Apart from these routes, there are other potential routes through which food items may be contaminated by trace metals, and a number of studies have focussed on this subject (Table 3). Akaninwor et al. (2006) compared trace metal concentrations in Nigerian staple food crops (both raw and cooked) from farmlands in Rivers State, an oil-producing area of Nigeria, to those from farmlands in non-oil producing (Ebonyi) state. Metal concentrations were found to be significantly higher in the food crops from the oil-rich region than in the same crops from the non-oil state. This result was attributed to the nature of the soil in the oil-producing area, being high in organic matter content that could chelate metals in the soil and facilitate their transfer into the crop plants. Similar report of comparatively high heavy metals content in crops from oil-producing area was made by Wegwu and Omeodu (2010).
Olutona and Daniel (2020) worked on melon seeds obtained from northern and south-western parts of Nigeria. Heavy metals determined in the samples were of the following order: Pb > Zn > Ni > Co > Cd, with all values higher in seeds from the north than in the south-west. Concentrations of Pb, Cd and Ni were found to be above the WHO permissible limits in samples where they were detected. Samuel and Babatunde (2021) performed health risk assessment, following the determination of heavy metals in food crops grown around an abandoned lead-zinc mining site in Tse-Faga, Benue State. High hazard quotients of 1714 and 1.143 were determined for Pb in Zea mays and Manihot esculenta, respectively. The study indeed indicated that the consumption of food crops growing in the vicinity of the abandoned mining site may cause lead poisoning in humans. Taiwo et al. (2021) investigated heavy metals in sixty samples of snacks and 'fast foods' in Ijebu-ode, South-western Nigeria. The authors found that Fe was most abundant in the samples at concentrations up to 71.3 mg/kg (in cashew nuts). Cancer risk for Co in all the food samples exceeded the acceptable limit of 0.0001, suggesting the possibility of development of cancer by individuals who consume the foods on regular basis. Gaya and Ikechukwu (2016) investigated levels of ten heavy metals in different types of plant-derived spices (seeds, leaves, bulbs, fruit pods and rhizomes), obtained from a market in Kano, Northern Nigeria. The spices all had excessive amounts of Fe and Cu, with maximum levels in ginger (19.4 mg/kg) and African nutmeg (15.3 mg/kg), respectively. Estimated daily intakes of the metals in onion, ginger, alligator pepper, utazi, Ashanti leaves, garlic, castor seeds and shallot were all above the tolerable limits set by FAO/WHO. Apart from plant-based foods, other types of food materials produced in the country have also been investigated. For instance, environmental contamination with toxic metals affects fodder plants, pastures and drinking water sources used for livestock production. In particular, nomadic cattle roaming and rearing in Nigeria depend on waters from unprotected rivers and streams as sources of drinking water for cattle, with the animals directly ingesting water contaminated with toxic metals and other chemical substances. Heavy metal levels in tissues of food animals may therefore provide indication of the degree of meat toxicological safety and the extent of environmental contamination by the metals. Ihedioha and Okoye (2013) investigated heavy metals in various edible organs of cattle and reported high levels of Cr (19.9 ± 2.92 mg/kg) and Zn (529.4 ± 155.3 mg/ kg) in the samples. This finding is highly significant, given the huge amount of beef consumed annually in Nigeria, estimated at 360,000 tonnes (Vanguard 2019). Njoga et al (2021) also determined levels of As, Cd and Pb in 450 edible samples of goat meat, comprising the kidney, liver and muscle, obtained from regular slaughter houses in Enugu State. The study detected at least one toxic metal in 56% of the samples, with the highest mean concentrations of 0.57, 0.82 and 0.06 mg/kg recorded for As, Pb and Cd, respectively. Estimated daily intake for all the metals exceeded recommended safety limits. Because goat meat is commonly consumed in delicacies in eastern part of Nigeria, this study highlighted the significant public health risks that the consumption of goat meats poses to humans in the region. Wegwu and Wigwe (2006) worked on edible meat/ flesh of the African giant snail (Archachatina marginata), sourced from three geopolitical zones of Nigeria -southeast, south-west and south-south. The study quantified Cu, Fe, Zn, Ni, Pb and Cd in the snail samples and reported that the heavy metal concentrations were above the WHO limits, Table 3 Heavy metal concentrations reported in foods (mg/kg) and drinks (mg/L) in Nigeria All recorded values are mean or maximum concentrations determined by the authors. Mercury (Hg) 7.5 and 0.01 mg/kg were reported by Azi et al. (2018) and Bassey et al. (2014), respectively; 0.004 mg/kg of Al was reported by Iwegbue (2010); '-' are metals not determined by the authors or below the quantitation limit  (2006) particularly in samples gotten from highly industrialized environments. Benthic invertebrates such as periwinkle (Tympanotonus fuscatus), mudskipper (Periophthalmus barbarus) and sesarmid crab (Guinearma alberti) constitute an important food (soup) ingredient in Southern parts of the country. Odigie and Olomukoro (2021) determined heavy metals content of these benthic fauna species, collected monthly from a wetland area in Delta State, over a period of 18 months. Apart from assessing the toxicological safety of their consumption, the species are bioindicators that could reveal levels of bioavailable toxic metals or other pollutants present in the rivers and sediments. Notable maximum mean concentrations of the metals measured in the species were 349.8, 3.46, 2.09, 0.41 and 0.19 mg/kg for Fe, Cu, Cd, Pb and Cr, respectively. Such levels of the metals are a cause for concern, given the widespread consumption of the invertebrate species in special delicacies in the area. Study by Azi et al. (2018) provide evidence that heavy metals are leached from raw foods into the cooking water, which is often consumed together with meals in soup preparations.
Few studies have investigated levels of toxic metals in beverages. Iwegbue (2010) analysed various brands of canned beers in Nigeria and reported that Pb, Cd, Cr and Ni were above permissible maximum levels for the metals in drinking water, while Co, Al, Cu and Zn were within the limits. Iwegbue et al. (2014) investigated heavy metal concentrations in locally produced alcoholic beverages, including raphia palm wine, oil palm wine, ogogoro, pito and burukutu, mostly consumed in rural communities in Southern Nigeria. In contrast to the result obtained for canned alcoholic (beer) drinks, the concentrations of all the metals were below permissible limits. The high concentrations of toxic trace metals in canned beers may be due to the industrial nature of the production process, which typically involves the intermediate liquors and finished products coming in contact with metallic equipment and machineries, unlike the production of traditional alcoholic drinks, which employs local wooden utensils. The packaging and storage of beers in metallic cans may also be contributing to the impartation of trace metals onto the drinks. Olutona and Livingstone (2018) investigated heavy metal concentration of non-alcoholic (malt) drinks obtained from various markets in Ibadan, South-western Nigeria. Concentrations of Pb, Ni and Cr were found to be above their respective WHO limits for drinking water.

Heavy metals in medicine and human fluid samples
Medicines, being substances ingested to cure or lessen the effects of diseases and ailments, are normally manufactured under hygienic conditions. They are also expected to be of high-purity standards, with the absence or non-detectable levels of extraneous chemical substances. In Nigeria, as it is in many developing African nations, people use orthodox/ modern medicines as well as local medicines, produced from herbs and made in form of tablets or mixed bottle concoctions. Aigberua and Izah (2019) investigated levels of heavy metals in some liquid herbal medicines sold in Portharcout, Southern Nigeria. Ni, Zn, Co and Fe were determined in the concoctions at maximum concentrations of 0.07, 0.03, 0.18 and 27.1 mg/L, respectively (Fe was found in 100% of the samples). The study noted that some of the herbal medicines were not approved by the government agency regulating the production and sales of foods and drugs in Nigeria. This points to the inadequacy of surveillance and inadequacy of enforcement of relevant laws by the concerned national agencies. Similarly, Nduka et al. (2020) determined carcinogenic heavy metals (Cd, Hg, As, Cr, Pb and Ni) in 30 brands of locally manufactured painkiller medicines, randomly sourced from pharmaceutical stores in Anambra State. The metals were detected in various combinations in the samples, while Ni was found in all the painkiller samples. The study estimated total cancer risk (TCR) and total non-cancer risk (TNCR) for the heavy metals to range from 7.21 × 10 −13 to 1.25 × 10 −10 and 1.51 × 10 −7 to 5.56 × 10 −5 , respectively, noting that the continuous consumption of these painkiller medicines puts people at risk of heavy metal toxicity. Nnaneme (2021) worked on orthodox analgesic syrups from pharmaceutical shops in Ibadan, Oyo State. The mean maximum concentrations reported by the study were 4.12, 3.5, 0.49, 0.67, 0.7 and 0.91 mg/L for Ni, Cd, Cr, Zn, Pb and Hg, respectively (Table 4). These values are highly worrisome and cast some doubts on the correctness of the analytical procedure and processing of the ensuing data. For instance, the maximum values reported for Ni and Cd in the syrups are 58 times and 1166 times higher than the authentic WHO guideline limits for these metals (WHO 2017). On the other hand (though very unlikely), the results may mean that the pharmaceutical syrups indeed contain such high levels of toxic trace metals, raising even more concerns for the health and safety of the Nigerian unsuspecting public.
The presence of heavy metals in medicines and in other samples such as cosmetics, foods and water (as discussed in 'Heavy metals in cosmetics and personal care products', 'Heavy metals in foods and beverages' and 'Heavy metals in ground waters, surface waters and aquatic biota species', respectively) provide good premise and justification for studies, which investigated toxic trace metals in human samples. Adekola et al. (2001) investigated heavy metals (Cd, Pb, Zn and Cu) in scalp hair samples of 900 individuals aged between 1 and 40 years, living in Ibadan or Ilorin, Nigeria. Varying concentrations of the metals were detected in the hair samples. The values range from 28 mg/kg for Cu to 1047 mg/kg for Zn. However, a most profound outcome of the study is the generally higher concentrations of Pb and Cd, found in hair samples of older people (16-40 years) than in hair samples of younger ones, irrespective of the location.
This result provides strong indication of bioaccumulation of heavy metals in human body, through ingestion and other exposure routes. The fact that the hair samples were thoroughly and repeatedly washed with solvents and water prior digestion  excludes the possibility that the heavy metals were merely adsorbed on the surface of the hair samples. Accumulation of toxic trace metals in human body systems in Nigeria was also corroborated by findings of Akan et al. (2014), who determined Ni, Cd, Pb and As in blood and urine of patients at the University of Maiduguri Teaching Hospital (UMTH), Borno State. The authors found that the concentrations of metals increased with the age of people, being lowest in the 1-10-year group and highest in the 51-60-year age group. Furthermore, levels of the metals in blood and urine were above those in drinking water sources in Maiduguri Metropolis, where the patients reside (Akan et al. 2014). Verla et al. (2019) also investigated levels of heavy metals in urine and blood samples of 60 children in Owerri Metropolis, Eastern Nigeria. The study found Pb, Cd, Ni, Mn and Cr in both the urine and blood samples, with concentrations in blood being higher than those of urine samples. Indeed, the authors noted that the maximum concentrations of the metals in blood were higher than the maximum values specified by the American Academy of Pediatrics. Mn levels up to 16.2 and 4.57 mg/kg were measured in the blood and urine samples, respectively (Verla et al. 2019). Eneh (2021b) investigated toxic heavy metal concentrations in blood and urine samples of a cohort of 100 hairdressers in Enugu, believed to have been exposed to the metals through regular use of hairdressing cosmetics. Exposure to Pb was implied from a high mean blood Pb concentration of 17.47 µg/dL. The study also reported mean blood Hg level of 25.06 ng/mL, which was above the expected normal range of 10-20 ng/mL. Mean concentration of Ni (0.49 µg/dL) was found to be above the reliable value of 0.2 µg/dL. These Ni levels were noted to be possibly responsible for carcinogenic effects, which impaired the quality of life of the subjects, as indicated by the rates of dizziness, nausea, vomiting, sleeplessness and headaches that were recorded among the workers (Eneh 2021b).

Heavy metals in soils
Soil could be imparted with trace metals through weathering and mineralization of parent rock materials, as well as anthropogenic influences such as industrialization, mining, indiscriminate waste dumping and automobile emissions. Particular areas of soil prone to receiving high concentrations of heavy metals in Nigeria are the waste dumpsites, serving as receptacle for all forms of solid and liquid wastes and are mostly unregulated by the authorities. The majority of studies investigating heavy metals in soil have focussed on dumpsite soils (Table 5). Aiyesanmi and Idowu (2012) reported high concentrations of heavy metals in soils of three dumpsites in Akure, South-western Nigeria. Order of concentration of the metals was the same in the three dumpsite soils and followed the pattern: Cu > Ni > Pb > Zn > Cr > Cd > Co. High concentrations of all the metals were also detected in edible leafy vegetables (Amaranthus spinosus and Talinum triangulae) found growing around the waste dumpsites. Eze et al. (2020) investigated heavy metal levels in four major dumpsites in South-eastern Nigeria and performed an assessment of human health risks associated with metals at the dumpsites. The study revealed that children were at the highest risk of exposure to As, Pb and Ni, with the ingestion exposure pathway being the major contributor to both the cancer and non-cancer risks. Electronic wastes, particularly the cathode and anode of batteries used in many portable devices, contain substantial amount of heavy metals and rare earth elements after their useful life (Odegbemi et al. 2021). Studies by Ofudje et al. (2014) and Ibe et al. (2018) on electronics workshops and electronic wastes dumpsites in Nigeria have demonstrated the release of heavy metals from these materials. Investigation of heavy metals in soil near a battery waste dumpsite in Ibadan, Oyo State, by Afolayan (2018) revealed soil contamination factor above 6.0 for Cd, Pb and Fe, indicating excessive and severe pollution of the soil with the metals. Furthermore, the toxic metals, Cd and Pb, were found at concentrations above 2.80 and 40.0 mg/kg, respectively, in maize plants grown near the battery dumpsite. Accumulation of metals in vegetables growing around dumpsites is a major cause for concern, as unsuspecting individuals may fetch them for consumption and/or for sales in open markets. In addition to being a source of heavy metals entering the soil environment, dumpsites are also associated with the release of radioactive elements. A study by Oladejo et al. (2021) determined heavy metals and radionuclides ( 232 Th, 238 U and 40 K) in soil around a dumpsite in Osogbo, South-western Nigeria. The reported mean activity concentrations and the absorbed dose rate values of the radionuclides exceeded recommended safe limits, indicating a risk of exposure to humans and animals around the dumpsites.
Soils in the proximity of industrial sites have also attracted some attention. Two recent studies ; Laniyan and Adewumi 2020) investigated heavy metal levels of soils around different cement factories in Southwestern Nigeria. Heavy metal concentrations were higher in the soil samples, compared to the appropriate reference samples analysed in the studies. Considerable pollution and potential ecological risk from Cd, Cr, Ni and Pb were   observed by Olatunde et al. (2020) for soil samples around Ibese cement factory. In addition to the proximal soil pollution with heavy metals at the Ewekoro factory, Laniyan and Adewumi (2020) detected Cu, Pb, Cr, Co and Ni in vegetables and root crops, at concentrations above international maximum safe limits. Ogundele et al. (2021) worked on soil samples from both active and abandoned artisanal gold mining sites in Ile-Ife, South-western Nigeria. While various metals were detected in the samples, concentration of Pb was particularly high and an assessment of contamination status via geoaccumulation indices revealed that the soils were indeed contaminated with Pb. In Northern Nigeria, Orisakwe et al. (2018) investigated the concentrations of Cu, Cr, Cd, Zn, Ni and Se in soil and edible vegetable samples in Dilimi, Bukuru and Barkin Ladi communities, where artisanal mining activities are prevalent. Estimated total hazard quotient and hazard index, based on metal concentration in the vegetables, were both above unity, indicating potential health risk from consumption of the vegetables. Floodplain soils (adjacent to rivers) are commonly used in Nigeria for cultivation of food crops and vegetables, due to their alluvial nature and the availability of water for irrigation purposes. A number of recent studies have been focussing on the metals content of floodplain soils, which potentially derive from materials deposited by overflowing rivers, themselves contaminated with toxic trace metals. Maduawuchi et al. (2019) investigated levels of Pb, Co and Cr in three floodplains in Southwestern Nigeria. The study found that fluvial deposition contributed more significantly to Pb and Co contents of the floodplains, with percentage contribution ranging from 79.3-99% and 67.2-85.7%, respectively. These two metals were also detected in an edible vegetable (Amaranthus hydridus) harvested from the floodplains. Another study by Aiyesanmi et al. (2020) determined the speciation of metals in the floodplain of Onukun River, Ondo State. Cu was found to be associated with the soil organic fraction; Pb and Zn exists in reducible fractions, while Cr and Fe are associated with the residual fraction. The findings suggest that Cu, Pb and Zn were mostly contributed by fluvial deposition to the floodplains, whereas Cr and Fe determined in the soils were more of geogenic or lithologic origin. Association of Pb with reducible soil fraction and attribution to anthropogenic activities was also reported by Ebong et al. (2019). In relation to agriculture, soils of vegetable farms irrigated with wastewater have showed higher levels of heavy metals than similar soils with no wastewater applied (Abdu et al. 2011). A recent investigation of heavy metals in floodplain soils and edible vegetables by Oguntade et al. (2020) found dangerous levels of accumulation of Cd (0.46 mg/kg) and Pb (49.30 mg/kg) in Celosia argentea and Corchorus olitorius, respectively.

Heavy metals in crude oil and oil-contaminated sites
Hydrocarbons and various heavy metals are common components of crude oil, bitumen, oil-bearing rocks and other valuable earth resources. A number of studies have determined heavy metals in crude oil in Nigeria, to provide indication of the suitability of crude for refining, in terms of the tendency to cause corrosion or poison catalysts used in refinery operations Adebiyi and Adebiyi 2015). The heavy metals present in Nigerian crude oil are mainly Cu, Mn, Fe, Zn, Pb, Co, Ni, Cd and Cr (Chinedu and Chukwuemeka 2018). Of greater relevance to this review, however, are studies which examined heavy metals in oil sands and oil-spillage sites. An estimated 3.1 million barrels of crude oil is believed to have spilled in the Niger Delta, the oilendowed region of Nigeria, from 1976 to 2014 (Chinedu and Chukwuemeka 2018). Osuji and Onojake (2004) worked on soil samples from oil-polluted lands in Obiobi and Obrikom, Niger Delta. The study confirmed higher levels of Pb, Ni and Cu in all surface soils (0-15 cm) from oil-contaminated lands, compared to nearby ones which did not receive oil spills. Similarly, Nwaichi et al. (2016) determined heavy metals in farm soils and crops grown on 4-year-old crude oil-impacted lands in Uduvwoku and Ekore, Delta State, compared to non-oil-impacted lands in the same area. The study found much higher levels of Cd and Cr in oil-impacted farmlands than in the controls. Also, edible cassava tubers grown on the contaminated lands contained Cd and Cr at average concentrations of 0.24 and 1.33 mg/kg, respectively, exceeding WHO set limits for these metals in food, whereas the same metals were not detected in cassava from non-oilimpacted farmlands. This study exemplifies the exposure of humans in Nigeria to heavy metals, through consumption of food crops cultivated on contaminated soil environments. Similar results of elevated metals content in crops from oilprospecting areas of Rivers State were earlier reported by Hart et al. (2005). Adebiyi and Ore (2020) determined heavy metals in sand residues (tailings) of the Nigerian bituminous sand field. Various heavy metals, including Cu, Fe, Sc, Nb, As, V, Mn, Ti, Sr and Ni, were detected at high concentrations, ranging from 81.75 µg/g (As) to 9453 µg/g (Fe). Indeed, assessment of contamination revealed very high ecological risks by the level of metals present in the tailings.

Identified gaps and recommendations for research priority
The review revealed that very few studies have been conducted in the northern part of Nigeria, especially, the northeastern and north-western geopolitical zones, with only 5 and 7 published articles, respectively (Table 1). The fact that these zones are educationally and technically less developed may have contributed to the little research being conducted in the region. The over-a-decade-long terroristic insurgency and associated violent activities in the north-east, which in itself may contribute to high environmental levels of heavy metals, have also limited scientific studies in the region. To avoid incidents similar to the Zamfara Pb poisoning in 2010 (Orisakwe et al. 2017), there is the need for Researchers in the north to collaborate more with their southern counterparts on heavy metal investigations in Northern Nigeria.
One of the key reasons for investigating heavy metal concentrations in matrices is to identify sources of toxic elements that may potentially injure the health of humans and affect animals and biodiversity. This review revealed that some important toxic metals are not being investigated in most studies. For instance, the summary presented in Table 1 showed that less toxic metals such as iron (Fe) and zinc (Zn) are being investigated and reported in all the six geopolitical zones, whereas the more toxic elements such as arsenic (As) and mercury (Hg) are scarcely investigated. From the set of studies reviewed (the bulk of which were conducted in the last ten years), As has been reported by mainly three zones, while Hg is reported from only one (south-east) out of the six geopolitical zones. Although As is included for the north-east zone in Table 1, it is noteworthy that only one study from the region (Akan et al. 2014) determined this metal. Furthermore, it could be seen from summaries provided in Table 3 (For foods) and Table 5 (for soil samples) that little attention is being given to As, compared to Zn and Fe. This same pattern is prevalent in studies of heavy metals in the entire sub-Saharan Africa. A compilation of 35 studies , cutting across 11 countries in the sub-Sahara, showed that As was reported by only 4 of the studies, while Hg was not determined by all. The poor reportage of Hg may be due to the special requirement of a cold vapour atomic absorption spectrometry (CVAAS), which is needed for its accurate detection and quantification. Although the majority of the studies in the current review employed the AAS instrumentation for analyses, the cold vapour facility is lacking in the laboratories from which the studies emanated; hence, the inability of these studies to include Hg in their investigations. It is noteworthy that only three studies (Ekere et al. 2014;Eneh 2021) out five that reported Hg levels in the south-eastern zone employed the CVAAS variant, while the remaining three studies used the flame AAS technique. This implies that the levels reported for Hg by some of the studies may be lower than are actually present in the samples. The gap in data availability for Hg (and the perceived inaccuracy in the concentrations being reported) can be effectively remedied by turning to the inductively coupled plasma-optical emission spectrometry/mass spectrometry (ICP-OES and ICP-MS), capable of providing limits of detection up to 0.001 µg/L for the metal (Passariello et al. 1996), while determining it alongside other heavy metals. Similar to Hg, researchers in Nigeria may also deploy ICP versatility and sensitivity to bridge the data gap for As. Indeed, there is a need to investigate Hg and As levels of many environmental matrices in Nigeria, including phases and ecosystems for which levels of other heavy metals were previously reported.
This review recognized that investigations of heavy metals in Nigeria have been broad in scope, in terms of the different sample matrices studied. However, the scope is limited from the perspective of the various heavy metals being investigated. Apart from data gap relating to Hg and As levels highlighted above, there are other elements categorized as toxic metals, but are not regularly investigated and monitored by Researchers in Nigeria. As an indication, the WHO (2017) guideline for drinking water quality provides maximum limit for 13 metals and metalloids (Table 6). This review indicates that five of the elements (Ba, Se, U, Sb and Mo) are not routinely investigated in environmental studies in Nigeria. Indeed, some of these elements have confirmed toxicity effects, just as others (e.g. Cd, Pb) that are often investigated and reported. For instance, Ba is a potent non-specific inhibitor of the inward rectifier channel (IRCs), causing blockade of potassium conducting pores. Exposure manifests in the form of gastrointestinal diarrhea, cardiac arrhythmias, hypokalemia, muscle weakness and paralysis (Bhoelan et al. 2014). Also, exposure to high levels of molybdenum (although an essential nutrient metal) may cause kidney damage, decreases in sperm count, anemia and loss of body weight in animals and humans (Todd 2020). Implication of non-investigation of these metals/ metalloids is that they may be present at dangerous levels in the environment and in the food chain, while attention is not yet given to their determination. The ICP facilities and the proton/particle-induced X-ray emission (PIXE) analyses (Ishii 2019), now available in the country, may be effectively deployed for the determination of these elements. As well as investigating heavy metal presence and levels in foods, beverages, drugs, cosmetics and other commodities that are of direct use to humans, there is clear evidence of awareness of the potential impacts of toxic heavy metal levels to the natural environment. A good number of the studies reviewed (74 out of 148) investigated and reported metal concentrations in natural environments such as streams, lakes, rivers and soil, which serve as habitats for species of organisms. However, such studies appear to be limited to the freshwater ecosystems alone and data are scarce regarding trace metal concentrations of the Nigerian marine ecosystems, which is very important to the country's fish resources. The situation also obscures the understanding of the nation's contribution to toxic metal levels in the world's interconnected ocean system. Possible reason for the dearth of studies on heavy metal levels in the Nigerian marine environment may be the more difficult logistics of obtaining samples from such environments, compared to the fresh water areas which are readily accessible. This review serves to recognize the need for groups of researchers in the country to pool resources together, to investigate and monitor levels of toxic heavy metals in the Nigerian marine ecosystems.
Also important for the marine environment is the association of heavy metals with plastic pollution. Heavy metals have been demonstrated to adsorb on plastic fragments (Oz et al. 2019;Cao et al. 2021), which may then carry them to far locations and into the bellies of organisms in water environments. Nigeria is one of the five countries in Africa, estimated to contribute the most to global marine plastic pollution, the other countries being Algeria, Egypt, Morocco and South Africa (Babayemi et al. 2019). In addition to serving as vectors for toxic heavy metal transport, plastics themselves are sources of metals in the aquatic environment. This is because their production processes involve the incorporation of certain metals, especially lead (Pb), cadmium (Cd), mercury (Hg), tin (Sn), antimony (Sb) and arsenic (As), to function as catalysts, biocides and heat stabilizers (Hahladakis et al. 2018), and during plastic degradation processes, these metals are also released into the environment. As plastics and microplastic research are starting to develop in Nigeria (Alimi et al. 2021), the extent of association of toxic heavy metals with plastic pollutants (both as vectors and as sources) need to be studied, especially under the prevailing tropical environmental conditions.
As governments now seek to diversify the economy through solid mineral development, resulting in increased mining activities across the country, there is a need to monitor levels of toxic metals, particularly Cd, Pb, Hg, As, Co, Ni, Cr, Se, Ba and U which are usually associated with geogenic sources (WHO, 2017;Ungureanu et al. 2017;Horvart and Kotnik 2019;Sodango et al. 2021) and will potentially be released more into the environment, particularly surface waters, as mining activities increase.

Concluding notes
This review has provided a state-of-the-art summary of heavy metals research in Nigeria. It reports on the levels of various metals determined for all sample types, including human body fluids, cosmetics, medicines, beverages, foods, drinking water, surface water, biota, soil and atmosphere. Identified sources of human exposure to heavy metals include the use cosmetics and personal care products (PCPs), consumption of food crops grown on lands with history of oil-spillage, consumption of crops grown in industrialized areas, consumption of aquatic resources from contaminated rivers, irrigation of farmlands with wastewaters, as well as the use of locally made herbal medicines. This review revealed that heavy metal concentrations in human body are increasing with age of individuals in Nigeria. As these toxic elements can typically induce organ damage and cancers, it remains to be demonstrated whether there is correlation between metal level in human body and increasing number of deaths from non-communicable kidney/heart failure and cancers in Nigeria (Olanrewaju et al. 2020;Idris et al. 2020). In the meantime, the review underscores the need for relevant food and drug agencies to pay more attention to locally made medicines in the country, with a view to prohibiting the sales and distribution of heavy metal-laden concoctions. The proliferation of such local medicines as well as cosmetics also calls for the establishment of trace metals limits, upon which such products could be benchmarked.
The review reveals that the scope of heavy metals studies has been sufficiently wide, with respect to various kinds of samples and matrices analysed. It shows that the latest trend in heavy metal research in Nigeria is the focus on cosmetics, electronic waste sites, herbal medicines, air samples and artisanal mining sites. However, it recognized the dearth of data regarding levels of some metals and metalloids, especially Hg, As, Ba, Se, U and Sb. There is also a general lack of data on heavy metals contamination of the marine ecosystems in Nigeria. Reduction of toxic metals' entrance into the food chain may be achieved by locating farmlands away from industrial areas and dumpsites and from oil-contaminated sites. Policies should be put in place to eradicate street hawking and display of food items, acts that expose the materials to air-borne toxic metals, emanating from diverse anthropogenic sources.