Assessment of risk to public health posed by persistent organochlorine pesticide residues in milk and milk products in Mumbai, India

Abstract

The risk posed by the presence of organochlorine pesticides in milk and milk products was estimated for the population of Mumbai. To determine the levels of organochlorine pesticides in milk and milk products, a monitoring study was carried out in and around Mumbai City. 520 samples of milk and milk products of different brands were considered in this study. A survey was also conducted to determine the mean daily consumption of milk and milk products by different age groups and this data was used to evaluate the daily exposure to the public. Non-cancer effects were evaluated by comparing the predicted exposure distributions to the published guidance values. For chemicals identified as potential human carcinogens, cancer risk was evaluated using standard methodology. The majority of the chlorinated pesticides identified in the milk and milk product samples studied were found to be at levels which do not pose unacceptable risks to the public, with the exception of α-HCH. The cancer risk estimated for this chemical slightly exceeds the US EPA guidance value.

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Introduction

Human exposure to organochlorine pesticides is attributed mainly to the food chain, only in selected populations of chemical workers does occupational exposure prevail. The contamination of food, including milk and milk products, by organochlorine pesticides is a worldwide phenomenon.^1–3 A number of contaminants have been detected in milk and milk products. Contamination of food by organochlorine pesticides may occur through the previous use of these pesticides, which are now generally, but not totally, banned from agricultural use. A number of incidents of acute toxic effects in humans, including death have occurred as a result of contaminated food. Food contaminated by organochlorine pesticides can also pose chronic health risks, including cancer. Epidemiological studies provide suggestive evidence that prenatal and/or postnatal exposure to organochlorine pesticides can produce health effects early in life, including effects on immunological parameters, neurological condition and neurodevelopment, thyroid hormone status, physical size, and physical activity.^4,5

This study was undertaken to examine the relative risks to the Indian population of consuming milk and milk products containing organochlorine pesticide residues. The exposure of the public to organochlorine pesticide residues present in milk and milk product samples was calculated by using concentration data. Various brands of milk and milk product samples were collected in and around Mumbai City and the levels of organochlorine pesticide contaminants were determined by gas chromatography-electron capture detection. A rapid assessment survey was conducted in and around Mumbai City to find out the mean daily consumption of milk and milk products by different age groups. The assessment of potential non-cancer health risk for different age groups was carried out by computing the hazard indices for each chemical. The risk for the cancer incident due to the organochlorine pesticide residues present in milk and milk product samples was estimated by using the cancer potency factor values available in the literature.^6,7

Methods

Exposure to the public

The average daily dose (ADD) due to intake of contaminated milk and milk products was estimated from the following relationship,

ADD = C × F × I

Where C is the concentration of organochlorine pesticide in milk and milk product samples. F is the fat content in the milk samples, and I is the intake of milk and milk products in g kg⁻¹ bw (body weight) per day.

The average daily doses for the different age groups were calculated by assuming 100% absorption of organochlorine pesticides. Additionally, because guidance values such as reference doses and cancer potencies generally do not account for bioavailability, adjusting absorption is not appropriate for the current analysis.

Levels of contaminants

520 samples of milk and milk products of different brands available in the local market were selected randomly to determine the concentration levels of persistent organochlorine pesticides. The methods used for sample preparation and analysis are reported elsewhere.^8,9 The concentration of persistent organochlorine compound residues in milk and milk product samples are presented in Table 1. Samples were analyzed in duplicate and results represent the arithmetic mean. The organochlorine pesticide levels presented in Table 1 are expressed on a lipid basis except in milk samples where the levels are given in terms of ng ml⁻¹. Alpha, beta and gamma isomers of HCH were detected in all the milk samples analyzed. Concentrations of total HCH varied from 0.35 to 6.76 ng ml⁻¹. Total DDT (sum of p,p′-DDT, p,p′-DDD, p,p′-DDE) in milk samples was found to vary from 0.64 to 13.5 ng ml⁻¹, which is almost twice the variation of concentration of total HCH. Mean total DDT concentration was found to be higher than mean total HCH concentration in milk and in all the milk products. This difference could be attributed to the antimalaria sanitary actions, carried out throughout India. Butter and cheese samples showed higher concentrations of these compounds, compared to other milk products such as curd.

Table 1 Range and mean concentrations of organochlorine pesticide residues in milk and milk products ^a

Compounds	Milk/ng ml^−1 (N = 22)	Curd/ng g^−1 (N = 18)	Butter/ng g^−1 (N = 6)	Cheese/ng g^−1 (N = 6)
a N is the number of brands of milk and milk products analysed. 10 samples of each brand were analysed. The values in brackets show the average of the total samples analysed
α-HCH	0.18–1.28 (0.49)	0.03–0.6 (0.65)	3.1–3.4 (3.2)	0.16–8.6 (5.69)
β-HCH	0.08–3.64 (0.62)	0.06–1.15 (0.45)	<0.5–10.8 (6.17)	0.02–13.2 (5.72)
γ-HCH	0.1–1.84 (0.47)	0.04–0.54 (0.27)	2.5–5.1 (3.77)	0.12–6.12 (3. 37)
δ-HCH	<0.03–0.19 (0.1)	<0.03–0.25 (0.06)	<0.03–2.7 (0.9)	<0.03–3.23 (1.35)
Pp′-DDD	<0.07–9.9 (2.33)	<0.07–6.9 (1.13)	12.3–63.2 (36.63)	<0.07–22.9 (8.27)
pp′-DDE	0.22–5.5 (1.33)	0.06–0.7 (0.48)	0.3–31.9 (13.43)	0.15–5.2 (3.12)
pp′-DDT	<0.25–2.9 (1.05)	<0.25–5.5 (1.2)	8–25.1 (20.97)	<0.25–26.7 (9.53)

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Exposure parameters

The fraction of fat contained in milk was calculated for each of the milk samples. The mean fat content was found to be 0.05 g fat per g milk, with a standard deviation of 0.02. The fraction of fat in milk was assumed to remain constant over time. The mean daily consumption of milk and milk products was determined by a rapid assessment survey conducted in 1060 households in and around Mumbai. The surveyed sample was classified according to the age groups of 1–10, 11–20, 21–40 and over 40 years. The results of the survey are represented in Table 2.

Table 2 Mean daily intake of milk and milk products by Mumbai population

Age group/year	Mean daily intake
	Milk/ml kg^−1 bw per d	Butter/g kg^−1 bw per d	Cheese/g kg^−1 bw per d	Curd/g kg^−1 bw per d
1–10	15	0.50	0.50	2.25
11–20	6.3	0.22	0.11	1.02
21–40	4.5	0.13	0.09	1.36
>40	2.3	0.09	0.08	1.37

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Non-cancer risk assessment

Chemical-specific reference doses (RfDs) are assigned to represent a measure of toxicity for non-carcinogenic health effects. These values estimate a daily dose below which no health effect is likely to be observed if an individual is exposed to a particular agent. A reference dose is derived by identifying a No Observed Adverse Effect Level (NOAEL), or a Lowest Observed Adverse Effect Level (LOAEL) and adjusting these concentrations with numerical safety factors. In the present study, RfDs published by US EPA^6,7 and acceptable daily intake (ADI) levels published by WHO¹⁰ were used to measure the toxicity of organochlorine pesticides for non-carcinogenic health effects. For some chemicals which do not have published guidance values, a reference dose for a similar chemical was used as a surrogate guidance value (Table 3). The Hazard Quotients (HQs) were determined by dividing the average daily dose (ADD) by the guidance value. Individual HQs for each constituent of concern were summed to produce a Hazard Index (HI). Exposure for which the HI is less than one are considered to pose no hazard.¹¹

Table 3 Guidance values for persistent organochlorines in milk and milk products

Chemicals	RfD^a/µg kg^−1 per d	ADI^b/µg kg^−1 per d	Surrogate guidance value/µg kg^−1 per d
a RfD obtained from US EPA^6 b ADI obtained from IRPTC^8 c RfD for γ-HCH applied to other HCH isomer d RfD for p,p′-DDT applied to DDT and related compounds
α-HCH	—	—	0.3^c
β-HCH	—	—	0.3^c
γ-HCH	0.3	10	—
δ-HCH	—	—	0.3^c
DDD	—	—	0.5^d
DDE	—	—	0.5^d
DDT	0.5	20	—

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Cancer risk assessment

Most of the organochlorine pesticides found in milk and milk products have been identified as potential human carcinogens by the US EPA and IARC (International Agency for Research on Cancer), cancer potencies are summarised in Table 4. The carcinogenic risk was estimated by multiplying the lifetime average dose of a chemical by its cancer potency factor. The cancer potencies for current analysis were obtained from the US EPA. The EPA has traditionally suggested a range of cancer risk 10⁻⁶ to 10⁻⁴ as acceptable, with 1 × 10⁻⁵ as the typically recommended value.^12,13 The carcinogenic risk was calculated by using the following relation with an assumed 70 year lifespan.

Risk = ADD × ED × (1/70) × CPF × 10

⁻⁶

where ADD is the average daily dose in ng kg⁻¹ bw per d, ED is the exposure duration which is equal to the age of the exposed person. CPF is the cancer potency factor in (mg kg⁻¹ bw per d)⁻¹.

Table 4 Cancer potencies for potentially carcinogenic persistent organochlorines identified in milk and milk products

Potential human carcinogens	US EPA classification^a	IARC^b classification	Cancer potency^c (mg kg^−1 per d)^−1
a Relevant US EPA classifications: A, known human carcinogen; B2, probable human carcinogen; C, possible human carcinogen. b Relevant IARC classifications: 1, carcinogenic to humans; 2A, probably carcinogenic to humans; 2B, possibly carcinogenic to humans; 3, unclassifiable as to carcinogenicity in humans. c The cancer potency of a chemical is the risk of cancer per unit dose of that chemical. Potencies were obtained from the US EPA.^6,7
α-HCH	B2	2B	6.3
β-HCH	C	2B	1.8
γ-HCH	—	2B	1.3
DDE	B2	—	0.34
DDT	B2	2B	0.34

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Results and discussion

Non-cancer risk assessment

Hazard indices were use to evaluate the potential non-cancer health impact of organochlorine pesticide residues present in milk and milk products. The HI values are summarized in Table 5. All the HIs fall below the target value of 1 for all the age groups. HIs for the age group 1–10 years range from 0.027 for δ-HCH to 0.428 for DDD. HIs for the age group of 40 years and above range between 0.005 for δ-HCH and 0.069 for DDD. For all the age groups, the highest HIs were found for DDD and the lowest for δ-HCH.

Table 5 Hazard indices for persistent organochlorines in milk and milk products

Age group/years	Compounds
	α-HCH	β-HCH	γ-HCH	δ-HCH	DDD	DDE	DDT
1–10	0.137	0.178	0.131	0.027	0.428	0.228	0.204
11–20	0.056	0.073	0.052	0.011	0.173	0.094	0.082
21–40	0.042	0.053	0.039	0.008	0.124	0.067	0.059
>40	0.024	0.029	0.021	0.005	0.069	0.036	0.034

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Cancer risk assessment

The cancer risk to the public, of different age groups, from organochlorine pesticide residues in milk and milk products are summarized in Table 6. Most of the risks are close to or below the accepted value of 1 × 10⁻⁵. The exception is α-HCH, for which the mean risk is 2.05 × 10⁻⁵ to 3.50 × 10⁻⁵. The cancer risk due to DDT was 2.73 × 10⁻⁶ to 4.61 × 10⁻⁶ while that for DDE was 3.05 × 10⁻⁶ to 4.87 × 10⁻⁶. The risk was found to increase with age; this may be because of the accumulation of these persistent compounds.

Table 6 Estimated cancer risk associated with exposure to organochlorine pesticides in milk and milk products

Age group/years	Compounds
	α-HCH	β-HCH	γ-HCH	DDE	DDT
1–10	2.05 × 10^−5	7.95 × 10^−6	4.04 × 10^−6	3.05 × 10^−6	2.73 × 10^−6
11–20	2.39 × 10^−5	8.78 × 10^−6	4.49 × 10^−6	3.57 × 10^−6	3.10 × 10^−6
21–40	3.46 × 10^−5	1.25 × 10^−5	6.66 × 10^−6	4.03 × 10^−6	4.28 × 10^−6
>40	3.50 × 10^−5	1.24 × 10^−5	6.55 × 10^−6	4.87 × 10^−6	4.61 × 10^−6

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Uncertainties

Considerable uncertainty exists in this type of analysis, which may arise from a number of potential sources, which are summarized here.

In conducting this analysis, conservative assumptions were adopted in order to estimate exposure. Assumptions were made about the mean, variance, and shape of the input distributions that may or may not be representative of the population in and around Mumbai City of India. The potential health impact due to intake of milk and milk products which contain a chemical in excess of the guidance value is unclear. The doses considered “safe” vary amongst regulatory agencies. Exposure above these levels could pose a health risk, but the true thresholds for toxic effects could be much higher. Other sources of uncertainty in estimating guidance values include the extrapolation from animals to humans for the identification of a No Observed Adverse Effect Level and the application of a safety factor.¹⁴ The toxicological effects were assessed on a single compound basis and potential effects of the mixture of chemicals were not considered. In addition, certain chemicals detected in milk and milk products do not have published guidance values and have not been evaluated for carcinogenicity, making the assessment of these chemicals highly uncertain.

The cancer risk reported in this study could be over- or underestimated, depending on the accuracy of the assumptions applied in the analysis. In estimating human cancer potency from animal bioassay data, a number of uncertain assumptions are made.¹⁵ Cancer potencies are typically derived by extrapolating the results of animal bioassays conducted at relatively high doses to low doses experienced by human via environmental exposure. The potentially increased sensitivity of lower age groups to chemical exposure is typically not accounted for in the cancer potencies. Exposure in early life is thought to be more hazardous because the children are more sensitive and the cancer has a long latent period.

Conclusion

Based on the results presented here, most organochlorine compounds in milk and milk products are not present at high enough levels to cause concern, with the exception of α-HCH. The cancer risk estimated for this chemical exceeds the US EPA guidance value. However, all other chemicals are found to possess both the non-cancer and cancer risk within the prescribed acceptable limits.

Acknowledgements

Authors thank Dr S. Sadasivan, Head, Environmental Assessment Division, Bhabha Atomic Research Center, for continuous encouragement and guidance and useful discussions. The authors would also like to thank Mrs Suman Sharma and Miss V.N. Naik for their support for sample collection and analysis.

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