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Estimated daily intake and health risk of heavy metals

by consumption of milkAmir Ismail

ab, Muhammad Riaz

a, Saeed Akhtar

a, Tariq Ismail

a, Zulfiqar Ahmad

c & Muhamm

Saad Hashmia

a Department of Food Science & Technology, BahauddinZakariya University, Multan-Pakista

b Department of Food Science, University of Massachusetts Amherst, Amherst-USA

c University College of Agriculture and Environmental Sciences, Islamia University

Bahawalpur-Pakistan

Accepted author version posted online: 27 Aug 2015.

To cite this article: Amir Ismail, Muhammad Riaz, Saeed Akhtar, Tariq Ismail, Zulfiqar Ahmad & Muhammad Saad Hashmi

(2015): Estimated daily intake and health risk of heavy metals by consumption of milk, Food Additives & Contaminants: Par

B: Surveillance, DOI: 10.1080/19393210.2015.1081989

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Publisher: Taylor & Francis

Journal: Food Additives & Contaminants: Part B

DOI: 10.1080/19393210.2015.1081989

Estimated daily intake and health risk of heavy metals by consumption of milk

Amir Ismail1,2

, Muhammad Riaz*1, Saeed Akhtar

1, Tariq Ismail

1, Zulfiqar Ahmad

3& Muhammad Saad

Hashmi1

1Department of Food Science & Technology, BahauddinZakariya University, Multan-Pakistan

2Department of Food Science, University of Massachusetts Amherst, Amherst-USA

3University College of Agriculture and Environmental Sciences, Islamia University Bahawalpur-Pakistan

Abstract

Cd, Co, Pb, Cu and Ni were analyzed in 480 milk samples by flame atomic absorption spectrophotometry. Meanconcentrations were 0.001, 0.061, 0.014, 0.738 and 0.028 mg/kg, respectively. Mean concentration of Cd was verylow, whereas Cu exceeded the maximum limits established by the Codex Alimentarius. In some areas the Pbconcentration exceeded the maximum limit as set by the Codex Alimentarius. The highest estimated daily intake ofCu calculated for male infants (1-3 year) was 33.534 µg/kg bw/day, while the lowest EDI was recorded for Cd(0.004 µg/kg bw/day) in adult females above 16 year. The results suggested that Cu and Pb from milk in the

investigated areas may pose a health risk to the consumers.

Keywords: Milk; Heavy metal; cadmium; lead; Pakistan.

Introduction

The safety of food regarding contaminants such as heavy metals, aflatoxins and pesticide residues is of majorconcern for researchers due to their deleterious impacts on human health. More attention is gained when these

contaminants are found in basic food items such as milk, which is most frequently consumed by the most vulnerableage group. Heavy metals persist naturally in the environment. However elevated concentrations in the food chain are primarily linked to manmade environmental pollution. Cadmium and lead are reported as the most toxic heavy

*Corresponding Author

Dr. Muhammad [email protected]+923067905770



2

metals while over consumption of some essential mineral elements also can result in the poisonous effects (Unak etal. 2007). Heavy metals are a threat for human health due to their potential damage to human cells and the skeletalsystem, osteoporosis, kidney failure and lung and blood cancer (Arora et al. 2008; Kumar et al. 2007). The routes ofentry for these heavy metals are ingestion or inhalation (Mendil, 2006). The toxicity of heavy metals is dependent ona number of factors, the most critical of which are ingestion rate and route, bioavailability, gender, age, excretionrate and the chemical state of the heavy metal (Enb et al. 2009).

Since ancient times milk has been regarded as an ideal diet for humans due to the presence of almost all macro andmicronutrients including proteins, fats, carbohydrates, minerals and vitamins (Dobrzanski et al. 2005). Milk andmilk products contribute 15% of the total food intake in European countries (González-Montaña et al. 2012) and are

particularly significant not only for infants who completely rely on this food during the first few months of their life(Ataro et al. 2008) but also for the elderly to prevent them from elevated risks of fractures and osteoporosis (Kiraand Maio, 2004). The presence of toxic elements like heavy metals in milk is therefore of prime concern to ensureits healthy impacts on human life and is focused on by researchers globally (Aslam et al. 2010; Maas et al. 2011;Ping et al. 2012; Pilarczyk et al. 2013; Suturović et al. 2014). Heavy metals are transferred into milk when animalsare fed with metal contaminated fodder or drink water originating from industrial effluents or sewage waste.

Pakistan is one of the leading milk producers in the world with a total milk production of 37.86 million tons in 2012.Milk is mainly obtained from buffalos (62.5%), cows (35.4%) and goats (2.1%), while most of the milk is producedin rural areas. Per capita availability of milk in Pakistan in 2011 was 286 g/day (FAO, 2015a, b). In Pakistan only

4% of the milk is processed while the remaining 96% is used as fresh milk, mostly supplied by milkmen called“doodhies” (Zia et al. 2011), who are responsible for the quality of the milk. Besides other contaminants (Bashir etal. 2013), milk can also be a major source of heavy metals. However, proper implementation of good quality

practices at dairy farm levels and at each and every step of industrial processing can ensure food safety of milk andmilk products in Pakistan.

Lactating animals accumulate heavy metals in milk if they are exposed to high concentrations of these metalsthrough feed or water. The consumption of metal contaminated milk by humans can cause serious health issues.Increased food safety concerns call upon a study comprising of a complete quantitative evaluation for heavy metallevels of milk in Pakistan. Therefore, milk samples from various areas of Multan city were analyzed for nickel,copper, cadmium, lead and cobalt content by using flame atomic absorption spectrophotometry. Estimated dailyintake (EDI) of heavy metals was calculated on the basis of heavy metal content of milk samples, milk consumptionrate and body weight of an individual of various age groups.

Material and Methods

Sampling Plan

A total of 480 milk samples (cow: 180, buffalo: 160, goat: 140) were collected directly from the farms duringFeburary-August 2014 in Multan city, Punjab Province, Pakistan. Multan city was divided into 4 zones (Fig. 1.),setting Chungi No 9 as central point, while Zone 1 – South west (n = 160), Zone 2 – North west (n = 90), Zone 3 –South East (n = 110) and Zone 4 – North east (n = 120). Zone 1 comprises of the major industrial areas of Multancity, while all other zones mainly encompas residential and market areas. Milk samples were collected in 250 mlclean plastic bottles and immediately transported to the labs of the Department of Food Science & Technology,Bahauddin Zakariya University, Multan in ice boxes and stored at -20˚C until further analysis. Prior to analysis thesamples were thawed at ambient temperature.

Chemicals & Apparatus

The chemicals employed were all of analytical grade and purchased from Merck chemicals (Darmstadt, Germany),unless otherwise stated. Metals were analyzed by using a flame atomic absorption spectrophotometer (Thermo



3

Scientific 3000 Series, Waltham, MA, USA). Standard solutions for different elements were purchased from CPAchemicals (CPA chemicals ltd., Stara Zagora, Bulgaria). For sample digestion and drying, a hot plate (Lab Tech EH35A plus, Beijing, China) and hot air oven (Memmert UNB 200, Munich, Germany) were used, respectively.Double de-ionized water was used for dilution of samples and standard solutions.

Analytical Procedure

Milk samples were digested by the wet digestion method of Richards (1968). Briefly, 1 ml milk sample and 10 mlHNO3 were mixed in a 100 ml flask. The mixture was heated for 20 min at 80 ˚C, cooled at ambient temperature,followed by addition of 5 ml of HClO4. The mixture was again heated, at 180 ˚C, until the solution became clearand the volume decreased to 2-3 ml. Finally, the solutions were diluted to 50 ml with double distilled water. Metalswere analyzed in an atomic absorption spectrophotometer by employing an air and acetylene flame. The operating

parameters are described in Table 1.

Quality Control

Blanks were analyzed and the recorded concentrations for various elements were below the limits of detection,calculated as three times the standard deviation of twenty procedural blanks (3.3 SD/b). LODs for Pb, Ni, Cd, Cuand Co were 0.5, 0.7, 0.1, 3.2 and 0.2 µg/kg, respectively. The certified reference material used was NIST 1549(National Institute of Standards and Technology, Gaithersburg, MD, USA), obtained from the IRMM (Institute for

Reference Materials and Measurements, Geel, Belgium) whose certified values were found very much close to theobserved values (table 2). All analyses were performed in triplicate and repeated when repeatability exceeded thelimit of 1%.

Estimated Daily Intake

The EDI was calculated by the method of Cano-Sancho et al. (2010). A food frequency questionnaire was designedto calculate the daily intake of milk by the different age groups of Multan city. Five different age groups of bothmale and female were surveyed. EDI values were calculated by the formula:

EDI = Milk intake (kg/day) × Heavy metal content in milk (µg/kg)Average individual weight (kg)

Statistical Analysis

Statistix 8.1 software (Statistix Inc., Florida, USA) was used for statistical analysis of the data obtained for each parameter. For comparison purposes the data were subjected to one way analysis of variance (ANOVA) followed bya LSD (Least Significant Difference) test. The differences were considered statistically significant at the probabilitylevel of P < 0.05. Mean values and the measurement uncertainty (standard deviations) were computed withMicrosoft Excel 2007.

Results and Discussion

The heavy metal content of milk samples collected from different areas of Multan city is presented in Table3.Statistical analysis showed significant differences in heavy metal concentrations from various zones as well asamong different species. Zone 1 (industrial zone) was the most contaminated zone, while buffalo milk had thehighest concentrations, followed by cow and goat samples. In the current study, milk samples were collected directlyfrom the farms. Therefore the chances of indirect contamination through utensils, air and milk processing machinesare minimal and most likely contamination sources are fodder and drinking water for the animals.

Cd concentrations were below the limit of detection (<0.0001 mg/kg) in milk samples from zone 2 and zone 3 of allanimal species, while it was highest in goat milk samples from zone 4 (0.004 mg/kg). The maximum tolerance limitfor Cd in milk proposed by the International Dairy Federation (IDF, 1979) is 0.0026 µg/g. Comparing our results



4

with the standard limit, only cow and goat milk samples from zone 1 and zone 4, respectively were found slightlyhigher than the maximum limit. The mean concentration of cadmium in the present study (0.001 µg/g) is also lowerthen earlier reported in Poland (0.0036 mg/kg) by Pilarczyk et al. (2013), in Egypt (0.006-0.018 mg/kg) by Sayed etal. (2011), in Spain (0.002 mg/kg) by González-Montaña et al. (2012) and in Iran (0.002 mg/kg) by Rahimi (2013)and Najarnezhad et al. 2015 (0.007 mg/kg in bovine milk ). However, all samples from zone 4 were contaminatedwith cadmium indicating the presence of possible contamination sources of fertilizer applications, coal productionand burning fossil fuels (Žukowska and Biziuk, 2008).

The mean concentration of Pb found in the present study was 0.014 mg/kg, which is below the standard limit of 0.02mg/kg as set by the Codex Alimentarius Commission (2011). However, mean Pb values of bovine milk samples ofzone 1 and zone 2 and buffalo milk samples from zone 4 were slightly higher than this limit. Increased lead contentin milk is a serious threat for the health of consumers as lead may interrupt the nervous and circulatory systems aswell as several other organs of the body (Malhat et al. 2012). In line with our study Kazi et al. (2009) also reportedlead values higher than the standard limit in milk samples collected from Hyderabad city of Pakistan. In a studyconducted in Nigeria (Jigam et al. 2011) the level of Pb was in the range of 0.16 - 0.62 mg/kg, which is much higherthen in our study. Mean Pb values of the present study are almost in line with earlier bovine milk lead concentrationsof 0.013 mg/kg as reported in Iran by Najarnezhad and Akbarabadi (2013). Elevated Pb levels might be due to theusage of canal water for irrigation of fodder as well as drinking of canal water by animals, which is common

practice in Pakistan. The canal water has already been reported before to have elevated lead levels in Multan city(Ismail et al. 2014). Use of waste water and pesticides application on animal fodder is also a potent source of Pb

contamination in animal milk (Hafez and Kishk, 2008; Jan et al. 2009).

Nickel is an essential mineral element but is also categorized as a toxin if its level exceeds certain limits. It acts as anactivator or cofactor for a number of enzymes as well as hormones (Belitz et al. 2004), while excessive intake maylead to cell damage, alteration of enzyme and hormone activities and may also effect bioavailability of other mineralelements. The average Ni concentration found in this study was 0.027 mg/kg. Maximum nickel concentration (0.069mg/kg) was found in buffalo milk of zone 4, whereas it could not be detected in goat milk (<0.0007 mg/kg) from thesame zone. Average nickel concentration reported by Enb et al. (2009) in cow and buffalo milk was 0.004 mg/kgand 0.006 mg/kg, respectively, which were lower then our study. Otherwise, results of the current study are muchlower than those reported earlier by Anetta et al. (2012) in bovine milk (1.01 mg/kg), indicating less chances ofnickel toxicity through milk consumption for people of Multan (Pakistan), when compared to Nitra (Slovakia).Average nickel concentration in present study is also less then found in Zagreb (0.06 mg/kg) as reported by Vahcicet al. (2010). The possible reason for the low nickel level in milk in the present study could be the collection of milk

samples directly from the animal farms rather than at markets or lower levels of nickel contamination in feed andwater of the animals as well as in the local environment.

Copper is an essential element for normal human growth, but becomes a toxin at high levels. Mean concentration ofcopper in bovine milk estimated in the present study was 0.738 mg/kg, with a range of 0.244-1.163 mg/kg. All milksamples analyzed in the present study exceeded the maximum limit of IDF (1979). The short term exposure ofhigher doses of copper is harmless to the human body, however elevated and prolonged exposure may disturb theimmune system (Turnlund et al. 2004). Higher doses of copper up to 4-6 mg/kg are reported to cause gastrointestinaldisorders, however all the milk samples were found below this range (Barn et al. 2014). Mean copper concentrationin the milk samples from Multan city is lower than that reported earlier from Egypt (1.45 mg/kg) by Malhat et al.(2012) and in Slovakia (3.90 mg/kg) by Anetta et al. (2012), but higher than reported in Italy (0.34 mg/kg) by Licataet al. (2012). Elevated Cu levels in milk samples indicate possible threats of gastrointestinal disorders especially ininfants due to their higher milk intake rates.

Cobalt is a part of vitamin B12 and is essential for nucleic acid formation. Excessive intake may result in reducedappetite, weight loss, dermatitis and cancer (Andrew, 1965; Basketter et al. 2003). Available data regarding the

prevalence of Co in milk are scarce. Mean cobalt concentration measured in the present study was 0.061 mg/kg,ranging between 0.015 and 0.137 mg/kg. The maximum level was measured in buffalo milk from zone 2, while theminimum was found in goat milk from zone 4. Mean values from the present study were almost in line with thosereported earlier by Enb et al. (2009), while mean levels are much lower than those reported earlier from theunpolluted areas of India (0.19 mg/kg) by Patra et al. (2008).

Estimated Daily Intake



5

EDI data for various heavy metals were in the order Cu > Co > Ni > Pb > Cd. The obtained data (Table 4) show thatchildren at the age of 1-3 year had the highest daily intake, while above the age of 16 had the lowest risk. Possiblefactors contributing to daily intake of heavy metals are the quantity of milk consumption and the mean body weight(bw). Highest daily intake was calculated for copper (33.534 µg/kg bw/day), while the lowest value was recordedfor cadmium (0.004 µg/kg bw/day). In a study conducted in Egypt by Hafez and Kishk (2008), EDI values for Pband Cd for infants (<1 year) by milk consumption were in the ranges of 0.4-0.82 and 0.004-0.011 µg/kg bw/day,respectively. EDI values for Pb in Egypt were almost in parallel with our data, while those for Cd were slightlylower. EDI values of Cd and Pb for adults reported by Salah et al. (2013) were 158.5 and 64.4 µg/kg bw/day,respectively, much higher then in our study. EDI values of Pb & Cd and Cu for infants in India reported by Tripathiet al. (1999) were 1.1 and 0.01 µg/kg bw/day, respectively. Compared to our study, EDI values for Pb are higher andfor Cd are lower. Recommended dietary allowance (RDA) values for Cd, Pb and Cu are 52-72, 429 and 2000-3000µg/day, respectively (Farid et al. 2004). Thus, EDI values of Cd, Pb and Cu in the present study are much lowerwhen compared to RDA values. However, several other dietary and non-dietary factors may also affect heavy metaldaily intake by Pakistan consumers, demanding a separate study from other possible routes.

Conclusion

In this survey most heavy metal levels in milk were within safe limits, except for copper which consistentlyexceeded the safety limit. Additionly, lead and cadmium were also excessive in some areas. EDI data of heavymetals due to milk consumption in the investigated area of Pakistan indicated that mean levels of the studied heavymetals are within in acceptable RDA ranges. Prevention of excessive lead, cadmium and copper in milk demandsstrict regulatory action for control and monitoring of animal feed and water by the health authorities.

Acknowledgement

This study is a part of the PhD research of Mr. Amir Ismail, carried out under the supervision of Dr. MuhammadRiaz, Department of Food Science & Technology, BahauddinZakariya University, Multan, Pakistan. The HigherEducation Commission Islamabad-Pakistan is highly acknowledged for financial aid under project number 20-1932,titled “Safety Status of Street Vended Raw Milk in Southern Punjab”.

Conflict of Interest

The authors declare no conflicts of interest.

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Table 1: Instrumental parameters for the investigated metals

Metal Wavelength (nm) Fuel flow rate (L/min) Bandpass (nm)

Nickel 232 0.8-1.0 0.2Copper 324.8 0.8-1.1 0.5

Cadmium 228.8 1.0-1.3 0.5

Lead 217 0.9-1.2 0.5

Cobalt 240.7 0.8-1.0 0.2

Table 2. Comparison of measured & certified reference material values (mg/kg)

Metal (CRM) Certified Value Observed Value Recovery (%)

Cd (NIST 1549) 0.0005±0.0002 0.00045±0.0001 90.0Pb (NIST 1549) 0.019±0.003 0.018±0.002 94.7Co (NIST 1549) 0.0041±0.002 0.0039±0.001 95.1Cu (NIST 1549) 0.07±0.008 0.064±0.007 91.4

Ni (CPA Chm.) 0.003±0.001 0.0026±0.002 86.7



9

Table 3: Heavy metal content (mg/kg) in milk samples collected from different areas of Multan city

Area Animal Cd Co Pb Cu Ni

Zone 1 Bufalo 0.0023±0.0002c 0. 127±0.030a 0. 013±0.004c 1. 054±0.05ab 0. 068±0.007a

Cow 0.0033±0.0001 b 0. 075±0.004 bc 0. 034±0.004a 1. 163±0.04a 0. 032±0.002c

Goat <0.0001

e

0. 036±0.003

def

0.009±0.001

cd

0. 693±0.05

fg

0.012±0.003

e

Zone 2 Bufalo <0.0001e 0. 137±0.025a 0.012±0.004c 0. 965±0.05 bc 0. 025±0.003d

Cow <0.0001e 0. 042±0.003cdef 0. 022±0.003 b 0. 605±0.04g 0. 045±0.004 b

Goat <0.0001e 0.016±0.004f 0.009±0.001cd 0. 244±0.03i 0.014±0.002e Zone 3 Bufalo <0.0001e 0. 083±0.003 b 0.006±0.002d 0. 937±0.02cd 0.014±0.002e

Cow <0.0001e 0. 054±0.005 bcde <0.0005e 0. 752±0.04ef 0.004±0.0005f

Goat <0.0001e 0. 025±0.004ed 0.013±0.002c 0. 453±0.04h 0.014±0.001e

Zone 4 Bufalo 0.0014±0.0005d 0. 057±0.004 bcde 0. 034±0.004a 0. 821±0.03e 0. 069±0.003a

Cow 0.0013±0.0003d 0. 063±0.003 bcd 0.012±0.002c 0. 834±0.03de 0. 032±0.003c

Goat 0.0043±0.0002a 0.015±0.003f <0.0005e 0. 340±0.02i <0.0007f

Total Mean0.001 0. 061 0.014 0. 738 0. 028 Values expressed as mean ± standard deviation (=3). Data within a column with different letters are significantly

different (p < 0.05).



10

Table 4: Estimated Daily Intake (µg/kg bw/day) of Metals through Milk by Different Age Groups

Age Group No of

ConsumersMean

Weight (kg)Milk Intake

(kg/day)µg/kg bw/day

Cd Co Pb Cu Ni

Male, 1-3 30 12.53 0.569 0.049 2.773 0.631 33.534 1.259

Female, 1-3 27 10.21 0.395 0.042 2.362 0.538 28.569 1.073

Male, 4-5 36 19.89 0.667 0.036 2.047 0.466 24.764 0.930

Female, 4-5 38 15.38 0.377 0.027 1.497 0.341 18.101 0.680

Male, 6-9 23 29.79 0.344 0.012 0.705 0.161 8.527 0.320

Female, 6-9 26 24.66 0.345 0.015 0.854 0.195 10.331 0.388

Male, 10-15 37 52.93 0.260 0.005 0.300 0.069 3.627 0.136

Female, 10-15 42 43.57 0.240 0.006 0.336 0.077 4.068 0.153

Male, > 16 132 67.32 0.308 0.005 0.279 0.064 3.379 0.127

Female, > 16 104 53.45 0.195 0.004 0.223 0.051 2.694 0.101

Figure1.Map showing the Location of Multan city in Punjab Province of Pakistan and the division ofMultan city in different zones

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