RESEARCH

Arsenic Toxicity in Soil-Plant-Human Continuum and Remedial Options

SAROJ KUMAR SANYAL

Formerly at Bidhan Chandra Krishi Viswavidyalaya, Mohanpur, Nadia, West Bengal & Adjunct Professor, Indian Agricultural Research Institute, New Delhi & Bihar Agricultural University, Sabour, Bihar, India.
Residence address: Flat No. A1 (Ground Floor), ‘Saptaparni’, 58/3, Ballygunge Circular Road, Kolkata, West Bengal 700 019, India.
Email: sksanyalnaip@gmail.com.

Received 12 January 2018; accepted 25 March 2018; published 16 April 2018

Corresponding editor: MALAVIKA DADLANI

​DOI: 10.29195/DSSS.01.01.0006​

Abstract

Even though the widespread arsenic (As) contamination of groundwater in West Bengal (India) and Bangladesh has remained mostly confined to the Bengal delta basin, bound by the rivers Bhagirathi and Padma, the spread (detection) of such groundwater arsenic contamination has been reported from several states of India, as well as certain other parts of the Indian subcontinent. The safe limit for arsenic in drinking water has been prescribed by the World Health Organization (WHO) to be 10 μg As. L^-1 and yet, arsenic contamination in the groundwater to the tune of 50 to 3700 μg As. L^-1 has been reported from the states of West Bengal, Assam, Bihar, Uttar Pradesh, Madhya Pradesh, Manipur, Jharkhand, Chhattisgarh, Punjab, Tripura and Nagaland. The source of such arsenic contamination in groundwater is believed to be of geogenic origin. The primary attention so far has been directed towards solving the problem of contaminated groundwater-based drinking water, notwithstanding the fact that the groundwater in the affected belt is extensively used in the agricultural sector rather than for drinking purpose. The number and extent of well-planned systematic studies conducted so far to examine the influence of arsenic in groundwater, used as irrigation source, on soil-plant-human continuum are only limited. Indeed, much more research work remains to be done in this field, not only in the Bengal delta basin but also, and especially in the other parts of the affected belt mentioned above. This issue assumes particular significance in view of the fact that what remains essentially a point-source of contamination, as in the case of drinking water, becomes a diffuse-source of contamination of uncertain extent and spread, when arsenic finds its way into the human-food-web through the use of such contaminated groundwater for agricultural irrigation, coupled with the possibility of bio-magnification up in the food-chain. The present article has made an attempt to take stock of this issue of considerable and long-standing environmental impact, as well as the appropriate mitigation options, involving people’s participation. The need for appropriate policy interventions has also been highlighted.

Keywords. Arsenic contamination; food-chain; health hazards; remedial measures.

Introduction

The word ‘Arsenic’ is borrowed from the Persian word زرنيخ Zarnik meaning ‘yellow orpiment’. Zarnik was borrowed by the Greeks as arsenikon. Arsenic has been known and used in Persia and elsewhere since ancient times. Also known as the Poison of Kings and theKing of Poisons, arsenic was often included during the Bronze Age in bronze (mostly as an impurity), which made the alloy harder. Albertus Magnus is believed to have been the first to isolate the element in 1250 C.E. (​​Antman 2001​​). Arsenic has also been used as a pest killer. With pesticide sprays began the practice of contaminating human food and environment with arsenic, resulting in adverse effects on the health of many people and their offspring. Underground arsenic threatens drinking water resources in many parts of the world, and the consumption of the tainted water over the years must have resulted in the untold suffering of millions of people (​Nriagu 2002​).

Arsenic, a toxic trace metalloid, is of great environmental concern due to its presence in soil, water, plant, animal and human continuum. Its high toxicity and increased appearance in the biosphere have triggered public and political concern. Out of 20 countries (covering Argentina, Chile, Finland, Hungary, Mexico, Nepal, Taiwan, Bangladesh, India and others) in different parts of the world, where groundwater arsenic contamination and human suffering therefrom have been reported so far, the magnitude is considered to be the highest in Bangladesh, followed by West Bengal, India (​Sanyal et al. 2015​). The scale of the problem is grave and unprecedented, exposing millions of people in the Bengal delta basin to risk. The widespread arsenic contamination in groundwater in different parts of West Bengal, located primarily in five districts adjoining the river Bhagirathi, as well as the contiguous districts in Bangladesh, is of great concern. Beyond the Bengal delta basin, widespread arsenic contamination in groundwater above the permissible limit (50 μg As. L^-1; ​WHO 2001​; see below) has also been detected in several places in the country (​​Table 1​​), for instance, at Chandigarh (1976), Bihar (2002), Uttar Pradesh (2003), Jharkhand (2003–2004), Chhattisgarh and Punjab (2006–2007) (​Sanyal 2017​). Further, ​​Table 2​​ and ​​Table 3​​ present the arsenic concentration in rocks and some other materials as well as arsenic concentrations in water other than groundwater, respectively.

Guideline Value of Maximum Arsenic Concentration

The World Health Organization (WHO)-recommended provisional guideline value of total arsenic concentration in drinking water is 10 µg As. L^-1 since 1993 (​WHO 1993​, ​WHO 1996​), mainly because lower levels preferred for the protection of human health are not reliably measurable on a large scale. However, the National Standard for the maximum acceptable concentration (MAC) of arsenic in drinking water is 50 µg As. L^-1 in several countries including India and Bangladesh, based on an earlier ​WHO (1971)​ advice. However, recently, the acceptable limit for drinking purpose in this country has been revised to the WHO-prescribed safe limit, namely 10 µg As. L^-1. A proposed new standard value of 5 µg As. L^-1 is under consideration. This is due mainly to the fact that inorganic arsenic compounds are classified in Group 1 (carcinogenic to humans) on the basis of adequate evidence for carcinogenicity in humans and limited evidence for carcinogenicity in animals (​IARC 1987​). Adequate data on the carcinogenicity of organic arsenic have not been generated. The joint FAO/WHO Expert Committee on Food Additives (JECFA) set a provisional maximum tolerable daily intake (PMTDI) of inorganic arsenic by humans as 2.1 µg As. kg body weight^-1.day^-1 in 1983 and confirmed a provisional tolerable weekly intake (PTWI) as 15 µg As. kg body weight^-1 in 1988 (​FAO/WHO 1989​). Such guideline values for soil, plant and animal systems are not available.

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Arsenic Contamination in Groundwater in the Bengal Delta Basin

The groundwater arsenic concentration (50–3700 µg As. L^-1), reported from the affected areas of West Bengal, is several orders of magnitude higher than the stipulated Indian standard for the permissible limit in drinking water, as well as the WHO guideline value (10 µg As. L^-1). Further, the arsenic concentration in alluvial aquifers of Punjab varied from 4 to 688 µg. L^-1 (​Sanyal et al., 2012​). In West Bengal, the presence of arsenic in groundwater in concentrations exceeding the acceptable limit was first detected in 1978, while the first case of arsenic poisoning in humans was diagnosed at the School of Tropical Medicine in Calcutta in 1983 (​Acharya 1997​). The effect of ingestion of inorganic arsenic in drinking water and the associated health effects in adults have also been well-established by physicians (​Guha Mazumder et al. 1998​). The main focus of attention, until recently, has been exclusively on arsenic concentration in groundwater-derived drinking water. However, since groundwater is also used extensively (to the tune of 85–90%) for crop irrigation in the arsenic belt of West Bengal, the possibility of a build-up of arsenic concentration in agricultural soils and agronomic produce was anticipated. Indeed, arsenic uptake by crop plants grown in soils contaminated with a high concentration of arsenic, and irrigated with such arsenic contaminated groundwater has been reported by several workers (reviewed by ​Sanyal et al. 2015​; ​Sanyal 2017​). Such findings call for immediate attention since what remains essentially a point and a fixed source of arsenic contamination for the drinking water (e.g. a tube well discharging contaminated water), may well become a diffuse and an uncertain source of contamination when arsenic finds its way into the food-web, accompanied with possible bio-magnification up in the food chain. This assumes added significance in view of the reported finding of a higher (than permissible) level of arsenic in the urine samples (an early biomarker of arsenic poisoning in humans) of some people, having no history of consuming arsenic-contaminated drinking water (Dr. D. N. Guha Mazumder, personal communication). Interestingly, the surface water bodies, located in the affected belt, have remained largely free of arsenic. This tends to suggest that the soil, which receives arsenic-contaminated water, acts as an effective sink to contain the toxin, thereby preventing the surface run-off to carry it to the adjoining water systems (​Sanyal 2005​).

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Health Implications of Arsenic Poisoning

Arsenic is a widely occurring toxic metalloid in natural ecosystems. As small as 0.1 g of arsenic trioxide can prove lethal to humans (​Jarup 1992​). Early symptoms of arsenic poisoning include skin disorders, weakness, languor, anorexia, nausea and vomiting with diarrhoea or constipation. With the progress of poisoning, the symptoms attain more characteristic features, which include acute diarrhoea, edema (especially of the eyelids and ankles), skin pigmentation, arsenical melanosis and hyperkeratosis, enlargement of the liver, respiratory diseases and skin cancer. Some of these symptoms are shown in ​Plate 1​. In severe cases, gangrene in the limbs and malignant neoplasm are also observed (​Guha Mazumder et al. 1998​; ​Sanyal et al. 2012​). The ‘Bell Ville Disease’ (typical arsenic-induced cutaneous manifestations among the people of Bell Ville) in Argentina, ‘Black Foot Disease’ in Taiwan and ‘Kai Dam’ disease in Thailand are well-established as health disorders due to arsenic poisoning (​Sanyal et al. 2012​). As a matter of fact, the hair, nail, skin-scale and urine samples of a large number of people, residing in the affected belt of West Bengal (India) and Bangladesh, have been analyzed by several workers. Many of these samples had more arsenic loading than permissible.

Plate 1 Effect of arsenic exposure on humans

Arsenic Forms in Groundwater-Soil Environment and Toxicity

Arsenic in groundwater and soil is present as dissolved oxyanions, namely arsenites (trivalent arsenic) or arsenate (pentavalent arsenic), or both, besides the organic forms. The solubility, mobility, bioavailability and hence toxicity of arsenic in the soil-crop system primarily depends on its chemical form, mainly the oxidation state (valency) of arsenic, also on whether the arsenic is present in inorganic or organic combinations. The toxicity of arsenic compounds in groundwater/soil environment follows the order:

Arsine [AsH₃; valence state of arsenic: 3] > organo-arsine compounds > arsenites and oxides (trivalent arsenic form) > arsenates (pentavalent arsenic form) > arsonium metals (monovalent arsenic form) > native arsenic metal.

The arsenites are much more soluble, mobile, and toxic than arsenates in aquatic and soil environments. The organic forms, namely dimethyl arsinic acid (DMA) or cacodylic acid, which on reduction (e.g. in anoxic soil conditions) forms volatile di- and trimethyl arsines, are also present in the soil. Another organic form present in groundwater and soil is monomethyl arsonic acid (MMA). The organic forms are much less toxic or non-toxic. Even though under aerobic cultivation practices, the less toxic pentavalent arsenic forms are predominant; under submerged rice culture, the more soluble and toxic trivalent forms predominate.

Arsenic in Soil-Plant System and its Influence on Food-chain

It wasnoted that much more toxic trivalent arsenic accounted for the major arsenic species recovered from grains (edible) of the transplanted autumn paddy, while pentavalent arsenic predominates in rice straw (​Sinha and Bhattacharyya 2014a​ ; ​​Sanyal et al. 2015​​). Further, the processing of rice (e.g. parboiling and milling, etc.) was found to increase the arsenic loading in rice for both the traditional and the high yielding cultivars (​Sanyal et al. 2012​). Soil amendment through organic manure reduced arsenic accumulation in rice grain and straw of autumn rice as revealed by the corresponding reduction of inorganic arsenic loading (​Sinha and Bhattacharyya 2014b​). ​​Sinha and Bhattacharyya 2014b​​ also studied the arsenic toxicity profile in rice, grown in the contaminated area of rural Bengal, and the possible risk of its dietary exposure. The risk of dietary exposure to inorganic arsenic through rice, the staple food in rural Bengal, has been noted to pose as great a threat to human health as the threat from contaminated drinking water. Organic amendments and augmented phosphate as well as selective micronutrient (e.g. zinc and/or iron salts wherever appropriate) fertilization showed considerable promise in reducing total and inorganic arsenic accumulation in rice and the consequent dietary risk (​Mukhopadhyay et al. 2002​; ​Sinha and Bhattacharyya 2011​; ​Ghosh et al. 2012​; ​Sanyal et al. 2015​; ​Das et al. 2016​).

Few reports are available that characterize the daily arsenic exposure through water and diet among the people living in groundwater contaminated regions and correlate the former with arsenic biomarkers. Demographic characteristics and the total daily arsenic intake through water and diet were determined in 167 participants (Group-1 participants, selected from the arsenic-endemic region) and 69 participants (Group-2 participants, selected from the arsenic-non-endemic region) in a study conducted in West Bengal by physicians working alongside agricultural scientists in a consortium mode. The findings showed significantly high dietary arsenic intake in people living in Nadia district of West Bengal, where contaminated groundwater was used for irrigation purpose, but significantly low in the region of Hooghly district, where groundwater was uncontaminated. Even after lowering the arsenic level in drinking water to < 50 μg As. L^-1 (the permissible limit in India), significant arsenic exposure occurred through water and diet, reflected by the elevated level of arsenic in the arsenic biomarker, namely urine, in people living in the arsenic-endemic region studied. Those with skin lesions were found to have a higher level of arsenic in urine and hair, compared to those without skin lesion (​Guha Mazumder et al. 2013​, ​Guha Mazumder et al. 2014​). In yet another study, the dose of daily arsenic intake from both water and diet was found to be significantly and positively associated with urinary arsenic levels in an arsenic-endemic region of West Bengal, even when people were using arsenic-safe water (< 50 μg As. L⁻¹) for drinking and cooking purposes. When arsenic levels in drinking water were further reduced to < 10 μg As. L⁻¹ (WHO safe limit), the dose from the diet was still found to be significantly associated with urinary arsenic excretion. But no significant association was found with arsenic dose from drinking water in this group (​Halder et al. 2012​ ; ​​Guha Mazumder et al. 2013​​; ​​Sanyal 2017​​). Further, when exposed to arsenic only through diet, the urinary arsenic concentration was found to correlate positively with dietary arsenic intake in the participants, showing skin lesions, while this correlation was insignificant in participants without skin lesion. Thus these facts, taken together, amply demonstrate that supply of arsenic-safe drinking water (< 10 μg As. L^-1) to the population in rural Bengal alone is not enough to reduce the risk of arsenic poisoning, consumption of rice provides yet another potential pathway to inorganic arsenic (i-As) exposure, which must also be considered as a remedial option. Thus, any mitigating intervention to address chronic arsenic toxicity requires an integrated approach. The essential components should include attempts to bring down arsenic entry into the food-chain, and to reduce arsenic loading in drinking water to below safe limits. (​Halder et al. 2012​; ​Guha Mazumder et al. 2014​; ​Sanyal et al. 2015​, ​Golui et al. 2017​; ​Sanyal 2017​).

Remedial Options at a Glance

A number of remedial measures have been noted to be quite effective in reducing the arsenic loading in the economic produce of several crops including rice. Some of these have been mentioned earlier. The more effective ones are summarized below:

• Optimum conjunctive use of ground and surface water (e.g. harvested rainwater), to reduce contaminated groundwater for irrigation during the lean period, and recharge of groundwater resource with harvested rainwater, free of arsenic.
• Develop/identify low arsenic-accumulating, less water-intensive high yielding crop varieties and cropping sequences suitable for arsenic-contaminated areas, especially for the lean period of January to May (e.g. cropping sequences, Elephant foot yam-mustard-sesame, Green gram-rice-mustard, etc., instead of, for instance, Olitorius jute-rice-rice and Green manure-rice-rice).
• Irrigate with pond-stored groundwater in which partial decontamination is facilitated by sedimentation-cum-dilution with rainwater.
• Enhancing the water use efficiency (through optimum water management) for groundwater irrigation, especially for summer (boro) paddy (e.g. by having recourse to judicious intermittent ponding of summer paddy during the vegetative growth period, followed by continuous ponding during the subsequent reproductive phase, which does not affect the yield significantly while cutting down the contaminated groundwater use considerably).
• Increased use of FYM and other organic manures + green manure crops, as well as the application of appropriate inorganic amendments (zinc/iron salts as and wherever applicable).
• Identification/development of varieties/crops which accumulate less arsenic in the consumable parts, and where the ratio of inorganic to organic forms of arsenic is low.
• Developing cost-effective phyto- and bio-remediation options.
• Creation of general awareness through mass campaigning, holding of farmers’ day, field demonstrations, taking due cognizance of the socioeconomic factors.
• People’s participatory approach in the creation of mass-awareness about the menace as well as adopting and popularizing the remedial measures to address the problem at the local level (​Mukhopadhyay and Sanyal 2004​; ​Sanyal 2005​; ​Sinha and Bhattacharyya 2011​, ​Sinha and Bhattacharyya 2014a​, ​Sinha and Bhattacharyya 2014b​; ​Ghosh et al. 2012​; ​Chatterjee et al. 2013​; ​Majumdar et al. 2013a​, ​Majumdar et al. 2013b​; ​Das et al. 2014​, ​Das et al. 2016​; ​Basu et al. 2015​; ​Sanyal et al. 2012​, ​Sanyal et al. 2015​; ​Sanyal 2016​, ​Sanyal 2017​).

Policy Interventions

The issue of arsenic contamination in groundwater in parts of the country and its adverse effect on human health has been agitating scientists, physicians, community workers, lawmakers and the general public at large, especially those who are suffering from its toxic effect. The primary attention, however, is directed towards solving the problem of such contaminated resource-based drinking water supplies to mostly the rural population. This is mentioned at the beginning of this article but is reiterated here to emphasize that the issue of addressing the drinking water sector itself is a huge challenge. The options have been mostly confined to the use of the relatively safe surface water, adequately clarified of its pathogen load, or tap the relatively deep aquifer layer (at a depth more than 150–200 m below the ground level) which is essentially free of the toxin in the affected belt. Periodic monitoring of the quality of such drinking water sources is also ensured quite satisfactorily.

However, what remains to be addressed is the food-chain issue which gets contaminated due to the entry of arsenic in it through the contaminated groundwater sources being pressed to irrigate the agricultural crops. This is not to undermine the existence of quite a vast amount of experimental data already generated by not only the agricultural scientists, but also the geologists, hydrogeologists, environmental experts and, most of all, the medical professionals (the latter till date in a moderate scale though) working in a consortium mode. It is quite reasonably well-established now that the food-chain contamination provides yet another potential pathway of arsenic exposure of the population in rural areas. Hence it is imperative that any comprehensive mitigating intervention of chronic arsenic toxicity in people requires integrated approaches toward reducing arsenic entry into the food chain, on one hand, while reducing arsenic in the drinking water below the safe limits, on the other. Unless this is attempted and accomplished, the food bio-safety concern, in its totality, is unlikely to go hand-in-hand with the food and nutritional security concerns of the country, not only for the domestic population but also for the export market. It appears that despite such realization at the level of scientists, it is yet to translate itself in terms of a concrete action plan, perhaps as a pilot programme initially, and finally as a large-scale initiative, to be implemented covering the entire affected belt. To ensure the latter, the concerned planners and the policymakers need to be adequately sensitized.

The success of such an integrated approach would essentially depend on its multi-level stakeholder nature, involving researchers, technologists as well as the planners with a focus on the real beneficiaries. The beneficiaries ought to be empowered through awareness and training to understand and participate actively in such mitigation programmes. A major shift from a purely technical to a holistic approach is needed to ensure a technically feasible, socially acceptable, economically viable and environmentally sound action plan.

Conclusions

Generating awareness and motivating people to test the quality of their drinking water for arsenic remains a key factor to contain the exposure to arsenic. In view of the unprecedented health hazard and misery among the affected people with severe skin lesion, the supply of arsenic-free drinking water, coupled with the arrangement of free treatment of these patients in the state referral hospital, could help considerably in alleviating the disease prevalence. This is all the more important keeping in view that the majority of the affected people are very poor and live in remote villages.

As stated earlier, arsenic-contaminated groundwater has been the main source of irrigation, drinking and allied activities in the affected areas of rural Bengal and elsewhere. Excessive use of arsenic contaminated groundwater resulted in an elevated level of arsenic in soil and food-chain. Thus, it is indeed high time that appropriate mass awareness is generated among the farming communities towards the judicious use of groundwater, coupled with appropriate remedial options discussed above to minimize the hazards of the toxin affecting the human food-web. Also, an integrated approach should bring together not only the agricultural scientists but also the physicians, social scientists as well as the planners at the local level.

The immediate needs, among others, include improvements of the field and the laboratory protocols for large-scale measurement of arsenic, as well as different forms/species of arsenic in groundwater-soil-plant-animal-human continuum. The latter is essential to characterize the net toxicity due to the entry of arsenic in the food-chain. Furthermore, strengthening of inter-institutional and inter-disciplinary action programme, long-term technical alternatives to reduce the dependence on arsenic contaminated resources is also the need of the day.