Prioritizing hazardous pollutants in two Nigerian water supply schemes: a risk-based approach
Ayotunde T Etchie a, Tunde O Etchie a, Gregory O Adewuyi a, Kannan Krishnamurthi b, S SaravanaDevi b & Satish R Wate b
a. Department of Chemistry (office 8, block B), Faculty of Science, University of Ibadan, Ibadan, Nigeria.
b. National Environmental Engineering Research Institute, Council of Scientific and Industrial Research, Nagpur, India.
Correspondence to Gregory O Adewuyi (email: email@example.com)
(Submitted: 26 November 2012 – Revised version received: 10 April 2013 – Accepted: 10 April 2013 – Published online: 31 May 2013.)
Bulletin of the World Health Organization 2013;91:553-561J. doi: http://dx.doi.org/10.2471/BLT.12.115774 [PDF]
In the fourth edition of the Guidelines for drinking-water quality, the World Health Organization (WHO) reiterates that a risk-based approach should be used to inform management decisions on the safety of drinking-water supplies.1 This approach entails the comprehensive assessment of both the risk to health and risk management and should encompass all stages of the water supply system, from water catchment to human consumption.1–3 In contrast, the concentration-based approach relies solely on determining whether the end product complies with standards that ensure consumer safety.2 Nevertheless, even with the risk-based approach, the concentration of contaminants in water ultimately determines the level of risk. However, in addition to concentration, the risk-based approach also takes into account parameters such as the level and duration of exposure to contaminants, their toxicity and the severity of the diseases they produce in assessing the need for mitigation. Furthermore, since this approach involves estimating the number of disability-adjusted life years (DALYs), it provides a framework for systematically comparing the disease burden associated with different pollutants,4 whether microbial, chemical or radiological.1
In this paper, we used a risk-based approach to identify the pollutants that posed the greatest risk to human health in two Nigerian water supply schemes and which should, therefore, be prioritized for removal.
Two water supply schemes in Nigeria were investigated: the Asejire and Eleyele schemes in Oyo State, which was included in “hydrological area 6” in the WHO and United Nations Children’s Fund (UNICEF) country report for Nigeria.5 The Asejire scheme, which was commissioned in 1972, is located in a suburb of the metropolis of Ibadan, about 30 km east of the city centre; the Eleyele scheme, which was commissioned in 1942, is situated within the metropolis. Ibadan is the capital of Oyo State and covers the largest area of any city in any country in tropical Africa.6 It is also the third most populous city in Nigeria: in 2010, the population was 2 893 137.6
The two water supply schemes are managed by the Water Corporation of Oyo State and together provide an urban piped water supply to around 25% of the people in Ibadan.7,8 Water for the Asejire scheme is collected by a dam on the River Osun and the level is maintained at about 81 m7 throughout the year, thereby ensuring a regular supply. Farming is prohibited in the catchment area7 and trees were planted on the banks of the dam to prevent soil erosion and silting. The Eleyele scheme’s dam collects water from two major rivers: the Ona and Ogunpa, which pass through Ibadan and are often polluted with effluent from unregulated industrial, commercial and residential quarters.7 Water for the treatment works is abstracted using a low-lift pump in the Asejire scheme and by gravity in the Eleyele scheme. Water purification is carried out using the conventional techniques of screening, aeration, coagulation, flocculation, sedimentation, filtration and chlorination. Treated water is delivered to consumers by tankers and through a pipe distribution system, which includes high-lift pumps and booster stations in strategic locations. Piped water is supplied mostly to yard and community taps, except in a few affluent areas where domestic water systems are common. Water is often stored in household containers because the supply is inconsistent. Secondary water treatment in homes is rare. The water supply schemes are unable to recover their operating costs despite government aid. Hence, the water supply is intermittent owing to a lack of chemicals and the high cost of pumping. Moreover, infrastructure maintenance is poor and as much as 40% of water can be lost from the distribution system.7,9
We searched PubMed and Google scholar using the phrase “drinking water of Ibadan” to identify scientific articles published between 2000 and 2010 on relevant hazardous pollutants. We then selected pollutants whose reported concentration exceeded regulatory guideline values. In particular, we looked for chemicals prioritized by WHO10 (i.e. arsenic, fluoride and nitrate) but no study reported a high level. In fact, a project sponsored by WHO and UNICEF in Nigeria in 2004 and 20055 reported that all water from utility pipes and tankers studied complied with guidelines for arsenic, fluoride and nitrate. The hazardous pollutants we identified for inclusion in our investigation were: microbial organisms, cadmium, cobalt, chromium, copper, iron, manganese, nickel, lead and zinc.
For the two water supply schemes, we sampled water from dams, treatment works and consumer taps, which we regarded as the end-point of the distribution system, in 12 communities within the Ibadan metropolis: Apete, Eleyele, Mokola and Sango for the Eleyele scheme and Agodi, Alafara Oje, Basorun, Bere, Beyeruka, Iwo Road, Oduoba and Ojaba for the Asejire scheme. Dam water was sampled where the river enters the dam, in the middle of the dam and at the outlet to the treatment works. After treatment, samples were collected at three different taps within each treatment works. For the Asejire scheme, six different consumer taps were sampled in each community, whereas, for the Eleyele scheme, a variable number of samples was collected because water was not distributed equally at all times to all consumer taps. Before collection, we ran off the tap water for about 20 seconds, which is longer than most people would. Sampling was carried out every two months from April 2010 to December 2011. The Eleyele scheme was shut down temporarily between July 2011 and December 2011 because of flooding, which reduced the number of treated water samples collected at both the treatment works and consumer taps.
For microbiological screening, we collected water samples in aseptic, nonfluorescent 100-ml glass bottles with screw caps. Treated water samples collected at treatment works and consumer taps were dechlorinated using sodium thiosulfate. Within 2 hours of sampling, water was screened for the presence of total coliforms and Escherichia coli using Colilert powder. The bottles were capped and incubated for 24 hours at 35 °C. Yellow coloration indicated the presence of total coliforms and fluorescence at 365 nm indicated the presence of E. coli. Each water sample was screened three times.
For heavy metal analysis, water samples were collected in metal-free, plastic bottles with screw caps and nitric acid was added to achieve a pH below 2. Samples were stored in an ice chest below 4 °C and immediately transferred to a deep freezer on arrival at the laboratory. Metal digestion was carried out using nitric acid within 24 hours and metal concentrations were determined by atomic absorption spectrometry.
We compared the concentrations of hazardous pollutants in water from treatment works and consumer taps with WHO guidelines1 (Table 1, available at: http://www.who.int/bulletin/volumes/91/8/12-115774) and identified those that exceeded guideline limits: they were cadmium, chromium, cobalt, lead and manganese (Table 2). In assessing the risk to health associated with the presence of a particular metal, we adopted the approach used by Crawford-Brown and Crawford-Brown,4 who related the risk of each individual health outcome associated with a particular metal to the probability of that health outcome occurring and the severity of the outcome, expressed in DALYs:
Table 1. Metal and microbial contamination and pH for two water supply schemes, Nigeria, 2010–2011
Table 2. Mean metal concentrations, two water supply schemes, Nigeria, 2010–2011
As a summary measure of biologically relevant exposure to a metal in water, we used the chronic daily intake of the metal, in mg per kg per day, by children and adult females and males, as defined in Equation 3, Equation 4 and Equation 5.13–16
For the oral ingestion of treated water: (3)where CDIo is the oral chronic daily intake, CM is the upper 95% confidence interval (CI) limit for the concentration of the metal in water, IR is the ingestion rate, EF is exposure frequency, ED is exposure duration, BW is body weight and AT is the lifetime averaging time.
For dermal contact with treated water: (4)where CDId is the dermal chronic daily intake, kp is the skin permeability coefficient, tevent is the exposure event duration, EV is the event frequency, SA is the skin surface area involved and ABSGI is the gastrointestinal absorption fraction.
Combining these terms, the total chronic daily intake (CDI) is given as:
In calculations, we used exposure data from Adewuyi et al.17 because they reflect typical water usage in Nigeria (Table 3, available at: http://www.who.int/bulletin/volumes/91/8/12-115774).
Crawford-Brown and Crawford-Brown4 and Pennington et al.19 argue that measures of toxicity, such as the reference dose, acceptable daily intake, tolerable daily intake and minimal risk level, were developed for assessing the health risk of individual hazardous substances in a regulatory context, not for comparing hazards. Consequently, Crawford-Brown and Crawford-Brown proposed using the 1% benchmark dose as the metric of toxicity for the noncancerous effects of a substance. This is the dose at which 1% of the population would develop the specified health outcome and is usually expressed in mg per kg per day. Alternatively, Pennington et al. proposed a central estimate of the effect dose, ED10, also expressed in mg per kg per day, which is the dose that results in a 10% increase in the incidence of the specified health outcome relative to the background level. In addition, the health risk can be extrapolated for lower doses using a slope factor, βED10. We used Pennington et al.’s approach for estimating noncancerous effects on health and selected the following algorithms for ED10:
For cadmium and chromium, we estimated ED10 using values for BMD10 obtained from the literature, where BMD10 is the lower 95% confidence limit for the dose that results in a 10% increase in the incidence of the specified health outcome relative to the background level.19 For cobalt and manganese, we used the no-observable-adverse-effect level (NOAEL) and the lowest-observable-adverse-effect level (LOAEL), respectively, both of which are expressed in mg per kg per day. These algorithms all assume a linear relationship between dose and response. Where dose levels were obtained in mice, we used a subchronic-to-chronic conversion factor of 3.3 and an animal-to-human conversion factor of 13 to derive equivalent dose levels in humans, as recommended by Pennington et al.19 We did not use the additional “margin-of-safety” factor of 3 that is generally used for regulatory purposes. We then calculated values for βED10 from the ED10 values for all noncarcinogenic health outcomes associated with these four metals (Table 4, available at: http://www.who.int/bulletin/volumes/91/8/12-115774):
Since we were not able to obtain data on the reference toxic dose for lead in water, we applied WHO’s method for estimating the health risks of lead.29 First, we compared the lead concentrations we observed with the results of a cross-sectional study carried out in the District of Columbia in the United States of America,30,31 which linked levels of lead in water to blood lead levels. That study reported that people who drank water with a lead concentration greater than 0.3 mg per litre, which was comparable to levels observed in our study, had a blood lead level below the level of concern of the United States Centers for Disease Control and Prevention: 10 µg per dl for children aged 6 months to 15 years and 25 µg per dl for adults. Hence, we assumed that the blood lead level corresponding to the lead concentrations in water we observed (Table 1) would fall within the range of 5 to 10 µg per dl and, in calculations, we used a mean of 7.5 µg per dl, which is associated with a mean reduction of 0.65 in intelligence quotient in children and a mean increase of 0.625 mmHg and 0.4 mmHg in systolic blood pressure in adult males and females, respectively.29
The presence of chromium in treated water has been associated with several types of cancer, assuming all species of the metal are oxidized to Cr6+: oral, oesophageal, gastric and small intestine cancer.32,33 To estimate βED10 for the carcinogenic effects of chromium, we adopted the method proposed by Crettaz et al.,34 which relates the cancer slope factor (CSF) for chromium given by the United States Environmental Protection Agency (i.e. 0.5 kg–days per mg) to βED10:
For each health outcome associated with cadmium, cobalt, chromium and manganese contamination, we used the estimates for exposure and toxicity obtained in the previous steps of the calculation to derive the probability of that health outcome: (11)where LPO is the lifetime probability of the outcome.
For lead, we calculated the probability of mild mental retardation (PMMR) associated with a mean reduction of 0.65 in intelligence quotient in children aged 4 years or under using the equation given by Fewtrell et al.:29 (12)where CF is the fraction of consumers aged 4 years or under (Table 5, available at: http://www.who.int/bulletin/volumes/91/8/12-115774) and %MMR is the percentage of consumers that will enter the intelligence quotient range indicating mild mental retardation. The adjustment ratio takes into account mental retardation caused by communicable diseases and iodine deficiency and the higher incidence of mental retardation in developing countries relative to developed countries. Fewtrell et al.29 give a value of 0.24% for %MMR and 2.05 for the regional adjustment ratio.
Table 5. Disease burden associated with lead contamination of water from consumer taps, two water supply schemes combined, Nigeria, 2010–2011
For adults, the probability of cardiovascular disease due to lead (PCVDL) in men and women was calculated using: (13)where CF is the fraction of consumers aged 15 to 54 years who were male or female, respectively, and RR is the corresponding relative risk of cardiovascular disease in men or women (Table 5).
The severity of each health outcome was quantified by obtaining an estimate of the associated degree of disability. For all outcomes other than cancer, we used the value of 0.67 DALYs per affected person attributable to irreversible systemic disease given by Pennington et al.19 Crettaz et al.34 derived the number of DALYs per person due to tumours at various sites using international data reported by Murray and Lopez:35 for oral cavity and oropharyngeal cancer, it was 3.5 DALYs per affected person; for oesophageal cancer, 9.3 DALYs per person; and for gastric cancer, 7.2 DALYs per person. Although these authors did not report a figure for cancer of the small intestine, they suggested a default value of 6.7 DALYs per affected person.34
The total risk to health of each individual metal contaminant (IR), expressed in DALYs per person per year, was calculated by summing the risks for each health outcome associated with that metal: (14)where CF is the fraction of consumers exposed to the health outcome (Table 6 and Table 7, both available at: http://www.who.int/bulletin/volumes/91/8/12-115774), severity is expressed in DALYs per affected person and the average lifespan of Nigerians is 54 years.36
Table 6. Disease burden due to metal contamination of water from treatment works, two water supply schemes, Nigeria, 2010–2011
Table 7. Disease burden due to metal contamination of water from consumer taps, two water supply schemes, Nigeria, 2010–2011
Then we calculated the total risk to the consumer population (RCP) for each water supply scheme, expressed in DALYs per year, from the individual risks associated with all metal contaminants (IRMC) in each scheme, weighted according to observed contaminant levels:
In estimating the consumer population for each water supply scheme, we used information on the distribution capacities of the schemes and the percentage of the population of Ibadan covered by the two schemes. The Asejire scheme provided 82 000 m3 per day and the Eleyele scheme, 27 000 m3 per day, which correspond to 75% and 25% of the total supplied by the two schemes, respectively. In theory, this total should have accounted for 25% of the water supply for the metropolis. However, we assumed a reduction of 5% due to leakage and another reduction of 5% due to political exaggeration; consequently, we assumed these supplies accounted for 15% of the supply to Ibadan. Using population data for 2010, we estimated that the consumer population for the two schemes combined was 433 971: 325 478 for the Asejire scheme (i.e. 75%) and 108 493 for the Eleyele scheme (i.e. 25%).
The results of our analysis of water samples from dams, treatment works and consumer taps are shown in Table 1 for selected pollutants. Although the total coliform and E. coli tests were positive for dam water from both water supply schemes, these contaminants were absent from water from treatment works and consumer taps.
The upper 95% CI limit for the concentrations of cadmium, chromium, lead, manganese, and nickel in dam water exceeded WHO guideline values1 in both wet and dry seasons, whereas the concentrations of copper, iron and zinc were below guideline values. The upper 95% CI limit for the concentration of cobalt in dam water exceeded the maximum contaminant level given by both the environmental media evaluation guide for children11 and health-based groundwater quality criteria12 in the wet season but not in the dry season (Table 1). Although water treatment reduced these concentrations substantially, metal contamination also occurred in the distribution system: levels of cadmium, copper, iron, lead, nickel and zinc were much higher at consumer taps than in water leaving the treatment works. In particular, the upper 95% CI limit for the concentrations of cadmium, chromium, manganese and lead in treated water exceeded WHO guideline values (Table 2).1 Consequently, these four metals were used in the risk assessment. Cobalt was also included because no WHO guideline value was available.
Table 5 shows the disease burden due to lead contamination. Table 6 and Table 7 show the estimated disease burden due to cadmium, cobalt, chromium and manganese contamination of the two water supply systems. Table 6 shows the hypothetical disease burden that would result if consumers received water directly from the treatment works. This was used for comparison with the disease burden associated with water from consumer taps (Table 7). Comparison of Table 6 and Table 7 shows that there was no difference in the disease burden due to chromium, manganese or cobalt contamination between water from treatment works and water from consumer taps. In contrast, the estimated number of DALYs per person per year attributable to cadmium contamination was much greater for water from consumer taps. We could not carry out a similar comparison for lead because we estimated the disease burden using a concentration range rather than a mean value.
We also compared our estimates of the disease burden due to water contamination at consumer taps supplied by the two water supply schemes with that associated with WHO’s reference limit and with microbial contamination reported in the literature (Fig. 1). The disease burden due to chromium contamination alone in our study was around 100 000 times that associated with WHO’s reference limit and around 1000 times that due to pathogenic E. coli contamination of treated water in Uganda, which was 0.292 × 10−3 DALYs per person per year.2 Recently, Machdar et al.37 reported that the disease burden, in DALYs per person per year, due to different types of contamination in Ghana was 0.395 for pathogenic E. coli, 0.0813 for Campylobacter spp., 0.026 for rotavirus, 0.025 × 10−3 for Cryptosporidium spp. and 1.4 × 10−3 for Ascaris spp.
Fig. 1. Disease burden of water supply scheme contamination in Nigeria compared with literature values, 2010–2011
Table 8 shows the total disease burden due to each metal contaminant among consumers supplied by the two water supply schemes. Chromium had the largest effect on human health in both schemes, followed in decreasing order by cadmium, lead, manganese and cobalt. The total number of DALYs per year attributable to metal contamination of the Asejire and Eleyele water supply schemes was 46 000 and 9500, respectively. This is equivalent to 0.14 and 0.088 DALYs per person per year, respectively: both values are much higher than the WHO reference limit of 1 × 10−6 DALYs per person per year but lower than the 0.5 DALYs per person per year reported for microbial contaminants in Ghana.37
Table 8. Disease burden due to metal contamination of consumer tap water in populations using two water supply schemes, Nigeria, 2010–2011
Our risk-based approach to identifying the pollutants in two Nigerian water supply schemes that posed the greatest risk to human health showed that the most important were chromium, cadmium, lead, manganese and cobalt, in decreasing order of their effect on health. The estimated disease burden due to each metal contaminant far exceeded reference limits and was comparable with the results of African studies of the disease burden of microbial contamination. In contrast, total coliforms and E. coli were not present in consumer tap water in the Nigerian water supply schemes, which indicates that treatment was effective in removing microbial contaminants present in dam water. Nevertheless, given the large number of pathogens that could be present in water, this negative finding should be taken with some degree of caution.
Metal contamination also occurred in the distribution system and, in particular, post-treatment contamination was substantial for cadmium and lead. However, most of the disease burden associated with these two contaminants appeared to be due to contaminated dam water and ineffective treatment. Consequently, reducing the disease burden could best be achieved by protecting water catchment and upgrading water treatment systems. Several studies have shown that electrocoagulation can reduce the quantity of metal ions in water to a very low level.38–41 The technique could be particularly effective when used before conventional chemical treatment. Further, comparison of the disease burden due to metal contamination observed in our study and that due to microbial contamination in other African studies indicates that chemical contaminants could be as important as microbial contaminants in piped water supplies.
This study was made possible by the World Academy of Sciences (TWAS) in Trieste and the Council of Scientific and Industrial Research in New Delhi, which awarded a doctoral fellowship to Tunde O Etchie.
- Guidelines for drinking water quality. 4th edition. Geneva: World Health Organization; 2011.
- Howard G, Pedley S, Tibatemwa S. Quantitative microbial risk assessment to estimate health risks attributable to water supply: can the technique be applied in developing countries with limited data? J Water Health 2006; 4: 49-65 pmid: 16604838.
- Bartram J, Corrales L, Davison A, Deere D, Drury D, Gordon B et al. Water safety plan manual: step-by-step risk management for drinking-water suppliers. Geneva: World Health Organization; 2009. Available from: http://whqlibdoc.who.int/publications/2009/9789241562638_eng_print.pdf [accessed 20 March 2013].
- Crawford-Brown D, Crawford-Brown S. Cumulative risk assessment framework for waterborne contaminants. J Environ Protect 2012; 3: 400-13 http://dx.doi.org/10.4236/jep.2012.35050.
- Ince M, Basir D, Oni OOO, Awe EO, Ogbechie V, Korve K et al. Rapid assessment of drinking-water quality in the Federal Republic of Nigeria: country report of the pilot project implementation in 2004–2005. Geneva & New York: World Health Organization & United Nations Children’s Fund; 2010.
- Ajayi O, Agbola SB, Olokesusi BF, Wahab B, Taiwo OJ, Gbadegesin M et al. Flood management in an urban setting: a case study of Ibadan metropolis. In: Martins O, Idowu OA, Mbajiorgu CC, Jimoh OD, Oluwasanya GO, editors. Hydrology for disaster management. Nsukka: Nigerian Association of Hydrological Sciences; 2012:65-81. Available from: http://journal.unaab.edu.ng/index.php/NAHS/article/download/914/882 [accessed 21 May 2013].
- African Development Bank Group [Internet]. Project: urban water supply and sanitation for Oyo and Taraba States. Country: Nigeria. Project appraisal report. Available from: http://www.afdb.org/fileadmin/uploads/afdb/Documents/Project-and-Operations/AR%20Nigeria002En.pdf [accessed 21 May 2013].
- Oyo State [Internet]. Oyo State Water Corporation launches urban water supply. Oyo State Press/News 6 November 2012. Available from: http://www.oyostate.gov.ng/oyo-state-water-corporation-launches-urban-water-supply [accessed 15 April 2013].
- African Development Bank Group [Internet]. Nigeria: project completion report, Ibadan Water Supply II Project. Abidjan: ADBG, Infrastructure Department, Central and West Region; 2004. Available from: http://www.afdb.org/en/documents/project-operations/projectprogramme-completion-reports/2/ [accessed 17 May 2013].
- Thompson T, Fawell J, Kunikane S, Jackson D, Appleyard S, Callen P et al. Chemical safety of drinking-water: assessing priorities for risk management. Geneva: World Health Organization; 2007. Available from: http://whqlibdoc.who.int/publications/2007/9789241546768_eng.pdf [accessed 15 April 2013].
- California Department of Public Health. Evaluation of potential exposure to contaminants in private well water: Cloverdale, Sonoma County, California. Atlanta: United States Department of Health and Human Services, Agency for Toxic Substances and Disease Registry; 2009. Available from: http://www.ehib.org/projects/PrivateWellCloverdaleHC_121009.pdf [accessed 15 April 2013].
- Site remediation and waste management program, New Jersey Department of Environmental Protection. Development of site-specific impact to ground water soil remediation standards using the soil-water partition equation. Trenton: New Jersey Department of Environmental Protection; 2008. Available from: http://www.nj.gov/dep/srp/guidance/rs/partition_equation.pdf [accessed 15 April 2031].
- Risk assessment guidance for Superfund. Volume 1. Human health evaluation manual (Part A). Interim final. Washington: United States Environmental Protection Agency; 1989 (EPA/540/1−89/002). Available from: http://www.epa.gov/oswer/riskassessment/ragsa/index.htm [accessed 15 April 2013].
- Risk assessment guidance for Superfund. Volume I: human health evaluation manual (Part E: supplemental guidance for dermal risk assessment). Final. Washington: United States Environmental Protection Agency; 2004 (EPA/540/99/005). Available from: http://www.epa.gov/oswer/riskassessment/ragse/pdf/part_e_final_revision_10-03-07.pdf [accessed 21 May 2013].
- Dermal exposure assessment: a summary of EPA approaches. Washington: Environmental Protection Agency; 2007 (EPA/600/R-07/040F). Available from: http://cfpub.epa.gov/ncea/cfm/recordisplay.cfm?deid=183584 [accessed 15 April 2013].
- WHO human health risk assessment toolkit: chemical hazards. Geneva: World Health Organization; 2010. Available from: http://libdoc.who.int/publications/2010/9789241548076_eng.pdf [accessed 30 March 2013].
- Adewuyi GO, Etchie AT, Etchie TO. Health risk assessment of exposure to metals in a Nigerian water supply. Hum Ecol Risk Assess 2012.
- Ebersole KE, Dugas LR, Durazo-Arvizu RA, Adeyemo AA, Tayo BO, Omotade OO, et al., et al. Energy expenditure and adiposity in Nigerian and African-American women. Obesity (Silver Spring) 2008; 16: 2148-54 http://dx.doi.org/10.1038/oby.2008.330 pmid: 19186335.
- Pennington D, Crettaz P, Tauxe A, Rhomberg L, Brand K. Assessing human health response in life cycle assessment using ED10s and DALYs: Part 2 – noncancer effects. Risk Anal 2002; 22: 947-63 http://dx.doi.org/10.1111/1539-6924.00263 pmid: 12442991.
- Suwazono Y, Nogawa K, Uetani M, Miura K, Sakata K, Okayama A, et al., et al. Application of hybrid approach for estimating the benchmark dose of urinary cadmium for adverse renal effects in the general population of Japan. J Appl Toxicol 2011; 31: 89-93 http://dx.doi.org/10.1002/jat.1582 pmid: 20836141.
- Gallagher CM, Kovach JS, Meliker JR. Urinary cadmium and osteoporosis in US women > or = 50 years of age: NHANES 1988-1994 and 1999-2004. Environ Health Perspect 2008; 116: 1338-43 http://dx.doi.org/10.1289/ehp.11452 pmid: 18941575.
- Akesson A, Vahter M. Health effects of cadmium in Sweden. Stockholm: Karolinska Institutet; 2011. Available from: http://ki.se/content/1/c6/12/28/21/bilaga3.pdf [accessed 15 April 2013].
- Engström A, Michaelsson K, Suwazono Y, Wolk A, Vahter M, Akesson A. Long-term cadmium exposure and the association with bone mineral density and fractures in a population-based study among women. J Bone Miner Res 2011; 26: 486-95 http://dx.doi.org/10.1002/jbmr.224 pmid: 20734452.
- Stopford W. Re: comments concerning your draft toxicology profile for cobalt. Durham: Duke University Medical Center; 2002. Available from: http://duketox.mc.duke.edu/atsdrcobaltcomments1.pdf [accessed 15 April 2013].
- Agency for Toxic Substances and Disease Registry. Toxicological profile for chromium. Atlanta: United States Department of Health and Human Services; 2012. Available from: http://www.atsdr.cdc.gov/toxprofiles/tp7.pdf [accessed 15 April 2013].
- Wasserman GA, Liu X, Parvez F, Factor-Litvak P, Ahsan H, Levy D, et al., et al. Arsenic and manganese exposure and children’s intellectual function. Neurotoxicology 2011; 32: 450-7 http://dx.doi.org/10.1016/j.neuro.2011.03.009 pmid: 21453724.
- Agency for Toxic Substances and Disease Registry. Toxicological profile for manganese. Atlanta: United States Department of Health and Human Services; 2012. Available from: http://www.atsdr.cdc.gov/toxprofiles/tp151.pdf [accessed 15 April 2013].
- United States Environmental Protection Agency [Internet]. Regional screening level (RSL) tapwater supporting table November 2012. Washington: EPA; 2012. Available from: http://www.epa.gov/reg3hwmd/risk/human/rb-concentration_table/Generic_Tables/pdf/restap_sl_table_bwrun_NOV2012.pdf [accessed 21 May 2013].
- Fewtrell L, Kaufmann R, Prüss-Üstün A. Lead: assessing the environmental burden of disease at national and local levels. Geneva: World Health Organization; 2003 (WHO Environmental Burden of Disease Series, No. 2). Available from: http://www.who.int/quantifying_ehimpacts/publications/en/leadebd2.pdf [accessed 15 April 2013].
- Centers for Disease Control and Prevention. Blood lead levels in residents of homes with elevated lead in tap water – District of Columbia. MMWR Morb Mortal Wkly Rep 2004; 53: 268-70 pmid: 15057194.
- Centers for Disease Control and Prevention. Notice to readers. Examining the effect of previously missing blood lead surveillance data on results reported in MMWR. MMWR Morb Mortal Wkly Rep 2010; 59: 592-3.
- Snow ET. Scientific review of public health goal for hexavalent chromium in drinking water. Launceston: University of Tasmania, School of Human Life Sciences; 2010. Available from: http://oehha.ca.gov/water/phg/pdf/092010SnowReview.pdf [accessed 15 April 2013].
- Analysis of oral, esophageal and stomach cancer incidence near chromium-contaminated sites in Jersey City. Trenton: New Jersey Department of Health and Senior Services and New Jersey Department of Environmental Protection; 2010. Available from: http://www.state.nj.us/health/eoh/cehsweb/documents/hudson_co_chromium_hc.pdf [accessed 15 April 2013].
- Crettaz P, Pennington D, Rhomberg L, Brand K, Jolliet O. Assessing human health response in life cycle assessment using ED10s and DALYs: Part 1 – cancer effects. Risk Anal 2002; 22: 931-46 http://dx.doi.org/10.1111/1539-6924.00262 pmid: 12442990.
- Murray C, Lopez A. The global burden of disease: a comprehensive assessment of mortality and disability from disease, injuries, and risk factors in 1990 and projected to 2020. Cambridge: Harvard School of Public Health; 1996 (Global Burden of Disease and Injury Series, vols. I & II).
- World Health Organization [Internet]. Nigeria: health profile Geneva: WHO; 2012. Available from: http://www.who.int/gho/countries/nga.pdf [accessed 15 April 2013].
- Machdar E, van der Steen NP, Raschid-Sally L, Lens PNL. Application of quantitative microbial risk assessment to analyze the public health risk from poor drinking water quality in a low income area in Accra, Ghana. Sci Total Environ 2013; 449: 134-42 http://dx.doi.org/10.1016/j.scitotenv.2013.01.048 pmid: 23416990.
- Adhoum N, Monser L, Bellakhal N, Belgaied J-E. Treatment of electroplating wastewater containing Cu2+, Zn2+ and Cr(VI) by electrocoagulation. J Hazard Mater 2004; 112: 207-13 http://dx.doi.org/10.1016/j.jhazmat.2004.04.018 pmid: 15302441.
- Orescanin V, Kollar R, Nad K. The application of the ozonation/electrocoagulation treatment process of the boat pressure washing wastewater. J Environ Sci Health A Tox Hazard Subst Environ Eng 2011; 46: 1338-45 http://dx.doi.org/10.1080/10934529.2011.606423 pmid: 21929469.
- Yadav AK, Singh L, Mohanty A, Satya S, Sreekrishnan TR. Removal of various pollutants from wastewater by electrocoagulation using iron and aluminium electrode. Desalination Water Treat 2012; 46: 352-8 http://dx.doi.org/10.1080/19443994.2012.677560.
- Barrera-Díaz CE, Lugo-Lugo V, Bilyeu B. A review of chemical, electrochemical and biological methods for aqueous Cr(VI) reduction. J Hazard Mater 2012; 223-224: 1-12 http://dx.doi.org/10.1016/j.jhazmat.2012.04.054 pmid: 22608208.