THE HEALTH EFFECTS OF ARSENIC AND OTHER TOXIC METALS IN BANGLADESH’S DRINKING WATER
The recent transition in Bangladesh from drinking surface water to drinking tubewell water has significantly reduced deaths from water-borne pathogens; however, disease and death from As in groundwater is affecting large areas of the country. In addition, the finding of small children with melanosis and keratosis, which are typical symptoms of arsenic poisoning in adults, and the observation of an analytical interference for the measurement of iron raised the question of other metals magnifying the toxic effects of As (Sarkar, 1998; Frisbie, Maynard, and Hoque, 1999).
In this evaluation, the areal and vertical distribution of As and 29 other inorganic chemicals in groundwater were determined throughout Bangladesh. This study of 30 analytes per sample suggests the most significant health risk from drinking Bangladesh’s tubewell water is chronic arsenic poisoning. The As concentration ranged from <0.0007 to 0.64 mg/L with 48% of samples above the 0.01 mg/L World Health Organization drinking water guideline.
Furthermore it reveals unsafe levels of Mn, Pb, Ni and Cr. Our survey also suggests that groundwater with unsafe levels of As, Mn, Pb, Ni and Cr may extend beyond Bangladesh’s border into the 4 adjacent and densely populated states in India. In addition to the health risks from individual toxins, possible multimetal synergistic and inhibitory effects are considered. Antimony was detected in 98% of the samples from this study and magnifies the toxic effects of As. In contrast, Se and Zn were below our detection limits in large parts of Bangladesh and prevent the toxic effects of As. Our results may allow scientists, policy makers and aid workers to initiate programs to assist the areas most affected by the toxic metals documented by these studies
Much of Bangladesh’s surface water is microbially unsafe to drink. Since independence in 1971, between 8,000,000 to 12,000,000 tubewells have been installed to supply microbially safe drinking water to the people of Bangladesh. Today 97% of Bangladeshis drink well water (WHO, 2001; WHO, 2000). Unfortunately, vast areas of this 137,000,000-person country contains groundwater with As concentrations above the World Health Organization (WHO) drinking water guideline of 0.01 mg/L (UNICEF, 2002). Chronic arsenic poisoning attributed to groundwater ingestion was first diagnosed in 1993. The total number of Bangladeshis diagnosed with chronic arsenic poisoning is expected to be in the tens or hundreds of thousands (BGS, 1999). These diagnoses include melanosis, leukomelanosis, keratosis, hyperkeratosis, nonpitting edema, gangrene, and skin cancer (Hindmarsh et al., 2002)
The 1997 United States Agency for International Development (USAID) field program produced the first national-scale map of As concentration in Bangladesh’s tubewell water. This map indicates that approximately 45% of Bangladesh’s area contains groundwater with As concentrations greater than the 0.05 mg/L Bangladesh national drinking water standard. The 1997 USAID field program also suggested the principal sources of As in Bangladesh’s groundwater might be the reductive dissolution of non-pyrite minerals, and the anion exchange of sorbed arsenate or sorbed arsenite (Maynard, Frisbie, and Hoque, 1997; Frisbie, Maynard, and Hoque, 1999)
In addition, the 1997 USAID field program discovered that tens of millions of Bangladeshis may be drinking unsafe levels of other toxic metals besides As (Maynard, Frisbie, and Hoque, 1997; Frisbie, Maynard, and Hoque, 1999). At least 27% of the samples contained an analytical interference to the 1,10-phenanthroline methods for measuring Fe(II) and total Fe. This interference was observed from suppressed matrix spike recovery (34%) during the measurement of Fe(II) and from improper color development during the measurement of total Fe. This interference could not be further characterized during the 1997 USAID field program; however, the literature suggested that it resulted from 1 or more toxic non-arsenic metals in these drinking water samples (APHA, AWWA, and WEF, 1995; ISMAC, 1969).
In response to this discovery, the hypothesis that Bangladeshis are exposed to other toxic metals besides As in their drinking water was assessed during our 1998/1999 field program. In this assessment, the concentrations of Ag, Al, As, Ba, Bi, Ca, Cd, Co, Cr, Cs, Cu, F-, Fe, H+, K, Mg, Mn, Mo, Ni, Pb, Rb, S, Sb, Si, Se, Sr, Tl, V, W, and Zn in tubewell water were mapped on a national scale. These analytes were selected based on their toxicity and potential to be the analytical interference observed during the 1997 USAID field program. This first peer-reviewed exposure assessment of As and other toxic metals in Bangladesh’s drinking water was recently published by our team (Frisbie, Ortega, Maynard and Sarkar, 2002).
Furthermore, the contention that Bangladeshis are exposed to other toxic metals besides As was strengthened by the finding of severe melanosis, keratosis, and other symptoms of chronic arsenic poisoning especially among children (Sarkar, 1998). This observation was the first indication that multimetal health effects might be involved. Therefore, the hypothesis that Bangladeshis are exposed to Sb, a metal that magnifies chronic arsenic poisoning (Gebel, 1999), was assessed during our 1998/1999 field program. Conversely, the hypotheses that Bangladeshis are not exposed to Se or Zn, metals that inhibit chronic arsenic poisoning (Biswas, Talukder, Sharma, 1999; Engel et al., 1994), were also assessed during our 1998/1999 field program.
This is a summary of our 1998/1999 field program. A more detailed account of this field program is found in Frisbie, Ortega, Maynard, and Sarkar (2002). In addition to summarizing these previously reported findings, the important medical observation that melanosis can be reversed if As patients are given safe drinking water is reported here for the first time.
Groundwater samples were collected from 112 tubewells throughout Bangladesh during December 20, 1998 to January 18, 1999. One sample was collected from each tubewell. All of these samples were analyzed for Ag, Al, As, Ba, Bi, Ca, Cd, Co, Cr, Cs, Cu, F-, Fe, H+, K, Mg, Mn, Mo, Ni, Pb, Rb, S, Sb, Si, Se, Sr, Tl, V, W, and Zn.
The sampled tubewells were distributed as evenly throughout Bangladesh as possible, given limited access due to the country’s extensive river delta and developing network of roads. Random samples were typically collected by traveling on roads and across rivers for 20 km to 30 km, stopping at a random location, and collecting groundwater from the first tubewell we found. The latitude and longitude of these tubewells were determined using a Garmin Global Positioning System 12 Channel Personal Navigator ™.
Established collection, preservation, and storage methodologies were used to ensure that each sample was representative of groundwater quality (APHA, AWWA, and WEF, 1995; Stumm, and Morgan, 1981). Accordingly, all sampled tubewells were purged by pumping vigorously for 10 minutes immediately before sample collection. All samples were collected directly into polyethylene bottles. These samples were not filtered. Samples were analyzed immediately after collection for pH by glass electrode or pH paper, preserved by acidification to pH <2 with 18.6% (w/w) HNO3, and stored in ice-packed coolers. The temperature of all stored samples was maintained at 0° to 4° C until immediately before analysis at our laboratories in France
All samples were analyzed for Mg, Al, Ca, V, Cr, Mn, Co, Ni, Cu, Zn, As, Se, Rb, Sr, Mo, Ag, Cd, Sb, Cs, Ba, W, Tl, Pb, and Bi at the Laboratoire Pierre Süe, Centre National de la Recherche Scientifique in Gif-sur-Yvette, France. These samples were analyzed by Inductively Coupled Plasma Mass Spectrometry (ICP/MS) with a Fisons PlasmaQuad PQ2+ spectrometer. Multi-element standard solutions were prepared from SPEX CertiPrep, Inc. (SPEX) certified solutions. Mono-elemental SPEX certified solutions of Be, In, and Re were used as internal standards. All samples were analyzed by ICP/MS twice. First undiluted samples were analyzed for trace elements. Then samples were diluted 10 times using ultrapure water and acidified to pH 2 with Prolabo Normatom I grade nitric acid for the determination of major elements (Ortega, 2002).
All samples were analyzed for Si, S, K, and Fe at the Université de Bordeaux 1, Laboratoire de Chimie Nucléaire Analytique et Bioenvironnementale (LCNAB) in Gradignan, France. These samples were analyzed by Particle Induced X-ray Emission (PIXE) Rutherford Backscattering Spectrometry (RBS) with the 4 MV Van de Graaff accelerator and nuclear microprobe beamline (Ortega, 2002). Multi-element standard solutions were prepared from Sigma certified solutions. Yttrium at a final concentration of 50 mg/L was used as an internal standard. All samples were analyzed for F- at the LCNAB by Fluoride Selective Electrode by established methods (APHA, AWWA, and WEF, 1995).
RESULTS AND DISCUSSION
In our study, groundwater concentrations of Ag, Al, As, Ba, Bi, Ca, Cd, Co, Cr, Cs, Cu, F-, Fe, H+, K, Mg, Mn, Mo, Ni, Pb, Rb, S, Sb, Si, Se, Sr, Tl, V, W, and Zn were mapped on a national scale. These maps are the first national-scale surveys of Ag, Al, Ba, Bi, Ca, Cd, Co, Cr, Cs, Cu, F-, Fe, K, Mg, Mn, Mo, Ni, Pb, Rb, S, Sb, Si, Se, Sr, Tl, V, W, and Zn in Bangladesh’s drinking water. These maps identify several potentially significant public health challenges that require urgent attention and additional study.
The relatively poor correlation between arsenic and total sulfur (r = -0.08) supports the 1997 hypothesis that pyrites are not the principal source of As in Bangladesh’s groundwater (Maynard, Frisbie, and Hoque, 1997; Frisbie, Maynard, and Hoque, 1999). In addition, the relatively small and negative correlation between As and depth (r = -0.13) supports the 1997 hypothesis that drilling deeper tubewells can access drinking water with significantly lower As concentrations approximately 20% of the time (Maynard, Frisbie, and Hoque, 1997; Frisbie, Maynard, and Hoque, 1999).
Of these analytes, the concentrations of As, Mn, Pb, Ni, and Cr exceeded WHO (1993; 1998a) or United States Environmental Protection Agency (USEPA, 1996; 2001) health-based drinking water criteria (see Table 1). Maps showing the extent of As, Mn, Pb, Ni, and Cr in groundwater were drawn using kriging , a standard geostatistical technique.
It is very important to realize that the 0.01 mg/L WHO drinking water guideline for As is based on a 6x10-4 excess skin cancer risk for human males in Taiwan, which is 60 times higher than the 1x10-5 factor that is typically used to protect public health (WHO, 1996). WHO states that the health-based drinking water guideline for As should be 0.00017 mg/L. However, the detection limit for most laboratories is 0.01 mg/L, which is why the less protective guideline was adopted (WHO, 1993; WHO, 1998a). There is sufficient evidence from human epidemiological studies linking increased mortality from liver, colon, kidney, bladder, and lung cancers to drinking arsenic-contaminated water; however, this relatively new discovery is not used to calculate the drinking water standard for As due to a lack of dose response data (USEPA, 2002; Tchounwou, Wilson, and Ishaque, 1999).
In our study, the As concentration ranged from <0.0007 to 0.64 mg/L. Arsenic was measured at or above its 0.0007 mg/L detection limit in 84% of the samples. Arsenic exceeded the 0.01 mg/L WHO drinking water guideline in 48% of the samples.
12% to 50% of Bangladesh’s tubewells exceed the WHO health-based drinking water guideline for uranium.
The most important finding of our national-scale study is that approximately 50% of Bangladesh’s area may contain groundwater with Mn concentrations greater than the WHO health-based drinking water guideline. Our study also indicates that Pb (3% of Bangladesh’s area), Ni (<1% of Bangladesh’s area), and Cr (<1% of Bangladesh’s area) concentrations exceed WHO health-based guidelines. These results are supported by the BGS/DPHE’s national-scale study of between 20 to 3,530 samples (BGS, and DPHE, 2001). This BGS/DPHE study suggests that 35%, <1%, 0%, and 0% of Bangladesh’s tubewells exceed the WHO health-based drinking water guidelines for Mn, Pb, Ni, and Cr, respectively. In addition, the BGS/DPHE study suggests that 5.3%, 0.3%, and an unspecified percent of Bangladesh’s tubewells exceed the WHO health-based drinking water guidelines for B, Ba, and Mo, respectively.
Moreover, the BGS/DPHE study suggests that 12% to 50% of Bangladesh’s tubewells exceed the WHO health-based drinking water guideline for uranium.
In our study, Mn exceeded the 0.5 mg/L WHO drinking water guideline in 37% of the samples. The maximum concentration of Mn was 2.0 mg/L. Despite the relatively poor -0.13 correlation coefficient between As and Mn, 35% of the samples that exceeded the WHO drinking water guideline for As also exceeded the WHO drinking water guideline for Mn. The areas where the WHO drinking water guidelines were exceeded for both As and Mn can be estimated by superimposing Figures . Similarly, 2% of the samples that exceeded the WHO drinking water guideline for As also exceeded the WHO drinking water guideline for Pb (r = 0.01). Likewise, 2% of the samples that exceeded the WHO drinking water guideline for As also exceeded the WHO drinking water guideline for Ni (r = -0.02). Correspondingly, 2% of the samples that exceeded the WHO drinking water guideline for As also exceeded the WHO drinking water guideline for Cr (r = 0.09). If a sample exceeded the WHO drinking water guideline for Ni, then the sample also exceeded the WHO drinking water guideline for Cr (r = 0.92).
Mn in drinking water is associated with neurological damage
The above findings raise serious concerns relating to environmental health issues caused by multimetal effects. The As, Mn, Pb, Ni, and Cr in Bangladesh’s drinking water are associated with known health risks. Arsenic is classified as a “human carcinogen” based on sufficient epidemiological evidence (USEPA, 2002). Manganese is a known mutagen (Beckman, Milvran, and Loeb, 1985). The accumulation of Mn may cause hepatic encephalopathy (Layrargues et al., 1998). Moreover, the chronic ingestion of Mn in drinking water is associated with neurological damage (Kondakis et al., 1989). The 0.5 mg/L WHO drinking water guideline for Mn was calculated using human exposures in Japan and Greece, and studies of various laboratory animals where neurotoxic and other effects were observed (WHO, 1996).
Lead is a “possible human carcinogen” due to inconclusive evidence of human and sufficient evidence of animal carcinogenicity (WHO, 1996). In addition, lead also causes many non-carcinogenic disorders in humans (Goyer, 1988). The 0.01 mg/L WHO drinking water guideline for Pb was calculated using the lowest measurable retention of Pb in the blood and tissues of human infants (WHO, 1996). Nickel is a “probable human carcinogen” (ICNCM, 1990). The 0.02 mg/L WHO drinking water guideline for Ni was calculated using No Observed Adverse Effects Level (NOAEL) and Lowest Observed Adverse Effects Level (LOAEL) in studies of laboratory rats (WHO, 1998b). The International Agency for Research on Cancer categorizes Cr(VI) as “carcinogenic to humans” and Cr(III) as “not classifiable” (IARC, 1987); however, the USEPA lists total Cr in drinking water as having “inadequate or no human and animal evidence of carcinogenicity” (USEPA, 1996). The WHO states that 0.05 mg/L drinking water guideline for total Cr is unlikely to cause significant health risks (WHO, 1998b).
Unsafe levels of As, Mn, Pb, Ni, and Cr
Groundwater with unsafe levels of As, Mn, Pb, Ni, and Cr extend beyond Bangladesh’s borders into the 4 adjacent and densely populated Indian states of West Bengal, Assam, Meghalaya, and Tripura. West Bengal has over 200,000 suffering from chronic arsenic poisoning (Mandal et al., 1999); however, we are unaware of any systematic survey of other toxins in West Bengal’s groundwater. We are also unaware of any systematic survey of tubewell water quality in Assam, Meghalaya, or Tripura. Prudence suggests that the 11-year delay between the discovery of chronic arsenic poisoning from groundwater in West Bengal and neighboring Bangladesh should not be repeated (Bhattacharya, Jacks, Frisbie, Smith, Naidu, and Sarkar, 2002). Therefore, the groundwater used for drinking in the adjacent and densely populated Indian states of West Bengal, Assam, Meghalaya, and Tripura should be immediately tested to determine if it is safe.
The severity of chronic arsenic poisoning in Bangladesh suggests that the other metals in groundwater might be magnifying As toxicity. Multimetal synergy could explain why 7- and 8-year olds exhibit melanosis long before it typically develops given their level of As exposure. In 1997 and 1998 we discovered 7- and 8-year old children with melanosis in communities near Jessore (N23° 19.18’ E 89° 10.89’) and Pabna (N 23° 38.35’ E 90° 35.02’). These communities had approximately 0.16 and 0.34 mg/L of As in their drinking water, respectively. An early effect of As toxicity in children might result from multimetal effects, nutritional deficiencies, other environmental factors, or genetic differences. However, a recent population-based study including children in the neighboring West Bengal suggested that the nutritional status of this population is not the reason for the high prevalence of skin lesions (Guha Mazumder et al., 1998). This report further noted that some cases appear to be occurring at surprisingly low levels of exposure and raised the possibility that some dietary factors affect the susceptibility of the whole population irrespective of being malnourished or not. Clearly, more studies are needed to evaluate As exposure in the context of multimetal health effects.
Sb may cause a magnification of As toxicity
Our study suggests the severity of chronic arsenic poisoning in Bangladesh might be magnified by exposure to Sb. Antimony in drinking water has been reported to modulate the toxicity of As (Gebel, 1999). Antimony was measured at or above its 0.0015 µg/L detection limit in 98% of the samples from this study. Arsenic was measured at or above its 0.7 µg/L detection limit in 84% of the samples from this study. Despite the relatively poor -0.05 correlation coefficient between As and Sb, 97% of the samples with detectable concentrations of As had detectable concentrations of Sb. The concentration of Sb ranged from 0.0015 to 1.8 µg/L and did not exceed its 5 µg/L WHO health-based drinking water guideline. However, this guideline is based on the toxicity of exclusively ingesting Sb, not the influence of Sb on chronic arsenic poisoning. The 5 µg/L WHO drinking water guideline for Sb was calculated using the LOAEL for decreased longevity, altered blood glucose levels, and altered blood cholesterol levels in laboratory rats (WHO, 1996). It is possible that these otherwise safe levels of Sb may cause a magnification of As toxicity. Humic substances might also magnify As toxicity (Engel et al., 1994) and were measured at relatively high concentrations in tubewells from Faridpur, one of Bangladesh’s most severely affected districts (Safiullah, 1999).
The WHO and USEPA have not established health-based drinking water guidelines for Fe; however, approximately 69% of Bangladesh’s area may exceed the WHO and USEPA’s 0.3 mg/L secondary criteria. In addition, As and Fe have a positive 0.25 correlation coefficient. Moreover, the As contaminated water has relatively high Fe concentrations; for example, drinking water samples exceeding 0.05 mg/L As have an average of 8.0 mg/L Fe. The potential health effects of these high Fe concentrations on chronic arsenic poisoning are unknown. However, there are reports suggesting high body Fe stores and dietary intakes of Fe are associated with hepatocellular carcinoma in humans (Marrogi et al., 2001) and mammary carcinogenesis in female Sprague-Dawley rats (Diwan, Kasprzak, and Anderson, 1997). In addition, As causes the release of Fe from ferritin, the generation of activated oxygen species, and DNA damage (Sarfaraz, Kitchin, and Cullen, 2000).
Se is an essential element that prevents the cytotoxic effects of As
In contrast, Se is an essential element that prevents the cytotoxic effects of As (Biswas, Talukder, Sharma, 1999). Selenium was not found above its 3 µg/L detection limit in 93% of the drinking water samples from this study. Importantly, 92% of the samples with detectable concentrations of As did not have detectable concentrations of Se. This general absence of Se and presence of As in drinking water is supported by the relatively poor 0.06 correlation coefficient for these elements. The maximum concentration of Se was 5.4 µg/L. Additionally, Zn is an essential element that promotes the repair of tissues damaged by As (Engel et al., 1994). Zinc was not found above its 0.7 µg/L detection limit in 21% of the drinking water samples from this study. Importantly, 18% of the samples with detectable concentrations of As did not have detectable concentrations of Zn (r = 0.17). If the sample did not have a detectable concentration of Zn, then the sample did not have a detectable concentration of Se (r = -0.02). Furthermore, Bangladesh’s agricultural soils might be Se deficient and are often Zn deficient (Brammer, 1996); therefore, it is possible that the apparent absence of these essential nutritive elements in drinking water and possibly food may cause a magnification of As toxicity.
The catastrophic health crisis caused by drinking metal-contaminated groundwater in Bangladesh affects tens of millions of people and requires urgent attention. Our study suggests that 49% of Bangladesh’s area has As concentrations above WHO guidelines. Similarly, 50%, 3%, <1%, and <1% of Bangladesh’s area exceeds WHO guidelines for Mn, Pb, Ni, and Cr, respectively. Our estimate that 60,000,000 Bangladeshis are drinking water with As concentrations above the WHO health-based guideline agrees with the BGS/DPHE’s 57,000,000-person estimate. In addition, our estimate that 50% of Bangladesh’s area exceeds the WHO health-based guideline for Mn is comparable to the BGS/DPHE’s estimate. Similarly, B, Ba, Cr, Mo, Ni, Pb, and U were discovered at concentrations above WHO health-based guidelines in relatively small areas of Bangladesh by our team, the BGS/DPHE team, or both teams (BGS, and DPHE, 2001).
Considering the population of this country and that 97% of its people drink from wells (UNICEF, 2002; WHO, 2000), these data suggest that tens of millions of Bangladeshis are drinking water with unsafe levels of As, Mn, B, Ba, Cr, Mo, Ni, Pb, or U. In our study, arsenic in Bangladesh’s tubewell water was found to be the most significant health risk. Drinking water with safe levels of As could be supplied to tens of millions by the integrated use of groundwater monitoring, drilling deeper tubewells, and appropriate treatment systems (Maynard, Frisbie, and Hoque, 1997; Frisbie, Maynard, and Hoque, 1999; Mandal et al., 1999).
During our field work, we made an important observation that melanosis, an early symptom of chronic arsenic poisoning, is typically reversed when affected Bangladeshis switch to drinking water from tubewells with significantly lower As concentrations. This observation is based on our findings in two separate field visits of the same community. Arsenic patients with visible signs of melanosis were examined in a community near Kushtia (N23° 80.81’ E89° 09.61) during October 1997. This community had approximately 0.17 mg/L of As in its drinking water. We returned in February 1998 and observed that melanosis had disappeared in some of the patients that switched to drinking water with As concentrations <0.05 mg/L. A recent report has also noted the disappearance of melanosis after drinking safe water (Chowdhury et al., 2000). Based on these limited exposure assessments, it appears that As poisoning at an early stage can be reversed by supplying safe drinking water.
However, mitigation efforts should not be limited to As; the health risks from other toxins in this region’s drinking water must also be addressed. Figures 1-5 will allow scientists, policy makers, and aid workers to initiate a rapid action program to focus in more detail on the areas with the highest concentrations of As, Mn, Pb, Ni, and Cr as we have documented in these maps. Strategies to supply this region with drinking water that has safe levels of As, Mn, Pb, Ni, Cr, other toxic elements, and agents that magnify chronic arsenic poisoning must be studied, developed, and quickly implemented.
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Seth H. Frisbie,Better Life Laboratories, Inc., East Calais, VT 05650, USA
Richard Ortega,Laboratoire de Chimie Nucléaire Analytique et Bioenvironnementale, CNRS UMR 5084, Université de Bordeaux 1, 33175 Gradignan, France
Donald M. Maynard,The Johnson Company, Inc., Montpelier, VT 05602, USA *Bibudhendra Sarkar,Department of Structural Biology and Biochemistry, The Hospital for Sick Children and Department of Biochemistry, University of Toronto, Toronto, Ontario M5G 1X8, Canada; *Corresponding author1. Arsenic and Uranium in Fertilizer
2. RADIACTIVE MINERAL IN DRINKING WATER OF BANGLADESH
3.Arsenic in Groundwater Research and Rhetoric