Assessment of the Bioaccumulated Metal Contaminants in Broiler Chicken -a Case Study From Skardu Pakistan

doi:10.21203/rs.3.rs-4311043/v1

Chicken meats are an important source of nutrients and are consumed all over the world therefore regular screening is of utmost need for food safety to enjoy good health. The present study is designed to assess the quality of broiler chicken meat available in Skardu City. The meat samples were collected from different poultry shops situated in the commercial market of Skardu. A total of five samples of chicken meat were collected, 4 samples of broiler chicken, and 1 sample of frozen chicken meat. The samples were prepared using the wet digestion method and analyzed using standardized atomic absorption spectroscopy. The results showed that lead, nickel, and chromium are all present in chicken meat at different concentrations except cadmium. However, the concertation of all metals are above the permissible limit recommended by World Health Organization. Health risk assessment showed that meat is cotaminaed with toxic metal and belong to IARC class 1(human carcinogen) and class 2B (possible human cancer).

Chicken meat

Lead

Chromium

Nickel

Cadmium

atomic absorption spectroscopy

Chicken meat, liver, eggs, and meat products are excellent sources of nutrients comprised of protein, minerals, essential fatty acids, and energy which are essential for the human body's development and growth. Chicken meat is the main part of our food because it is necessary for the nourishment of adults, young children, and infants. Moreover, it is easily digestible, easily accessible, and economical as compared to other meat [1, 2]. Doctors are also recommended due to the low glycemic index that helps to protect against the development of diabetes, cancer, and obesity[3]. Copper (Cu), manganese (Mn), nickel (Ni), selenium (Se), chromium (Cr), and zinc (Zn), are important to all living organisms as micronutrients [4]. They are crucial for the regulation of gene expression, enzymatic processes, ribozyme catalysis, ribosome activities, and energy metabolism [5-7]. Although heavy metals are necessary at low doses, the higher concentrations of heavy metals may be harmful to cellular function [7-9]. They become a significant risk to the brain, lungs, kidney, liver, gastrointestinal, cardiovascular, neurological, and normal cell cycle, especially among at-risk populations like young children and fetuses. [5,8, 10]. Various carcinogenic, mutagenic, and teratogenic effects of heavy metals on human health have been reported [3]. Reactive oxygen species (ROS) which in turn may cause oxidative DNA damage that may add to the pathology of various diseases that are generated by redox-active transition metals, including cadmium, chromium, and nickel. Acute leukemia, diabetes mellitus, diabetic neuropathy, hepatocellular carcinoma, breast cancer, Parkinson’s disease, and multiple sclerosis have all been linked to an accumulation of damaged DNA. The World Health Organization (WHO) and Food and Agriculture Organization (FAO) established guidelines for recommended daily chicken meat intake to protect human health. These restrictions apply to both primary drugs and chemicals and any metabolites that may develop and become deposited or stored in cells, tissues, or organs after the compounds have been administered [7]. Considering the bio-magnification in the food chain, transmission in human organs, and causing toxicity to our health, heavy metal poisoning is a significant issue. Thus, it is necessary to critically examine how metal enters the human body through various pathways such as ingestion, inhalation, and skin contact[3]. Heavy metals have a longer lifetime, are less prone to disintegration and decomposition, and may deposit in various organs of the human body, which could have harmful side effects [11-13]. The demand for poultry meat and its products all over the world is increasing over time due to its nutritious value. New technologies, and significant formulation of chicken feed help in meeting the demand. Poultry meat has emerged as a significant source of animal protein with high levels of biological amino acids, vitamins, and all essential components of human nutrition for growth and body metabolism [14-16]. Despite the nutritional values given above, chickens are exposed continuously to heavy metal contaminants. The basic ways by which metals are entered into the chicken are poultry feed, drinking water, and processing methods. Heavy metals accumulate in various parts of chicken like the liver, gizzard, and heart, harm the chicken enzymatic system, feed refusal, and also cause weight loss, low hatchability, inhibit growth, organ failure, increased susceptibility to disease and stress, and finally cause death [17-18]. According to the literature, the primary route of heavy metals intake into the poultry tissues by feeds. The accumulation of heavy metals varies from one tissue to another [17-19], liver and kidneys are the two important organs for the detoxification and execration of harmful elements, but these two organs are the most damaged organs due to the excess of harmful elements in our food or feed of animals [1]. Instead, some dishonest merchants frequently add poisonous tannery waste to chicken feeds as a source of protein to achieve a quick profit [7]. A report found that due to its inexpensive availability, several chicken feed producers in Bangladesh have recently started using shaving dust from tannery companies as a source of protein. When hides and skins are treated with various chemicals and salts during different stages of the tanning process tannery waste accumulates an enormous amount of toxic metal and it poses a great concern to human health. Traditional chrome tanning uses basic chromium sulfate salt, of which 60% to 70% is consumed by hides and skins and 3.204% is present in chrome shaving dust. An investigation was conducted in southern Nigeria. The results obtained from that investigation are that for both adults (19-70 years old) and children (1-3 years old), the maximum tolerable Ni intake is 7 and 40 mg/day, respectively. Turkey meat samples taken from the Warri zone had the greatest mean level of Ni (20.78 mg.kg-1). The Nickel concentrations in these samples were below the maximum allowable intake amounts. A study was conducted to measure the concentrations of heavy metals (Cu, Zn, Co, Fe, Cr, Cd, Ni, and Pb) in the liver, kidney, pancreas, and meat of cows, buffaloes, goats, sheep, goats, chickens and other animals from Kohat Market in Pakistan. The concentration of heavy metals is found higher in the liver, and kidney as compared to other studies reported [20-21]. A report found that in Lahore, Pakistan, and Tamil Nadu, India several parts of the chicken were analyzed that contain high quantities of Cr [13]. Chromium (III) is an essential element if it is taken at a low concentration while chromium (IV) is carcinogenic [14]. The research used atomic absorption spectroscopy to identify the levels of heavy metals (Cr, Cd, Co, Pb, Cu, Ni, Fe, Zn, Mg, and Mn) in canned beef and four different chicken luncheons from Sulymaniah markets. Chromium content among corned beef brands showed a significant difference, whereas there was no significant difference in chromium content among the trademarks for all poultry luncheons. The iron (Fe) concentration for the corned beef trademarks A, B, C, and D, respectively, was 1.43, 5.41, 3, and 4.4 μg/gm. A and D had a minimal concentration of zinc whereas B and C had high zinc concentrations. Furthermore, compared to the G trademark, which had a considerably lower zinc concentration, the F trademark had a significantly higher zinc concentration [22]. Heavy metal contamination is considered a major threat to human health worldwide. In Pakistan, we are facing heavy metal pollution in our food products. Therefore, it is necessary to ensure food safety by knowing the extent of heavy metal content in poultry feed, meat and eggs [7].

The main objective of the present study was to evaluate the level of heavy metals (Lead, Cadmium, Chromium, and Nickel) in poultry chicken meat collected from different poultry shops in Skardu and compare it with frozen chicken meat. Skardu has a cold climate and cold climate affects the food habits of the inhabitants. Usually, in Skardu, people use foods that provide fat to warm their bodies in winter. That’s why meat consumption is very high.

2.1 Study Area: Skardu city is the capital of the Baltistan region and is situated at an elevation of 7,320 feet above sea level. According to the statistics of the Government of Gilgit-Baltistan, the population in the province is 1.49 million while the population density is 20.5 people per square Km. The population growth rate of Gilgit-Baltistan is 2.56 [23–24]. The climatic conditions of Skardu are harsh and winters are too long. The average annual temperature is 10ᵒC while in winter the temperature is below the freezing point for 3 months [25]. The cold climate affects the food habits of the people of Skardu. Usually, in Skardu, people use foods that provide fat to warm their bodies in winter. That’s why meat consumption is very high due to its climatic conditions [26]. Different kinds of meat including mutton, beef, and chicken are available in the market. The consumption of chicken meat is high due to its availability and affordable rates [27]. Frozen chicken is also available in the market to fulfill the demand for chicken in Skardu. Some people also use Desi Chicken but it is very rare. According to an estimate in Skardu almost more than 5000 kg per day of sale excluding frozen chicken and desi chicken [28]

2.2. Sampling site:

This study was conducted in Skardu city. A total of five broiler chicken meat samples were collected from different commercial markets. Four samples of chicken meat were taken from four poultry shops, and 1 sample of frozen chicken meat was taken for comparison. It is common practice that chicken in the poultry shop was fed on formulated poultry feed to increase the meat and rapid growth. The samples were collected in polyethylene air-tight bags and stored in the refrigerator before analysis.

2.3. Reagents: HNO₃ (99.5%); HCl (37%), HClO₄ (60%), H₂O₂ (30%). All the chemicals are purchased from Sigma-Aldrich Company and are analytical grade.

2.4. Sample preparation: All samples were prepared using the wet digestion method as shown in Fig. 1 [19]. First of all, meat samples were cleaned and washed with deionized water. After that, the samples were cut into small pieces and make the samples homogenized. The chicken pieces were placed in Petri dishes and placed in an oven (WHL25A) at 65^oC for 48 hours until the samples were completely dry. Two grams (2 g) of chicken meat were placed in a beaker, and 10 ml of HNO₃ was added and heated at 135^oC until the liquor was clear. 10ml HNO₃, 1ml HClO₄, and 2ml H₂O₂ were also added into the beaker and heated continuously at 135^oC for 1 hour until the liquor became colorless.

Health Risk Assessment

The health risk assessment of metal residue in chicken meat was assessed based on estimated daily intake (EDI), target hazard quotient (THQ), and hazard index (HI) equations.

EDI= \(\frac{\text{C} \times \text{F}\text{I}\text{R}}{\text{B}\text{W}}\) …..…………………….. (1)

Where C is the concentration of metal in each sample (mg/Kg), FIR is the rate of ingestion of chicken meat (g/day) in Pakistan, BW is the average adult body weight (66 kg).

THQ= \(\frac{\text{E}\text{D} \times \text{C} \times \text{F}\text{I}\text{R}\times \text{E}\text{F} }{\text{R}\text{f}\text{D} \times \text{B}\text{W} \times \text{A}\text{T}}\) ………………………….. (2)

Where C is the concentration of metal in each sample (mg/Kg), ED is the exposure duration (70 years), FIR is the rate of ingestion (g/day) of chicken meat in Pakistan, EF is the exposure frequency (365days/year), RfD is the oral reference dose (ug/g/day), and BW is the average adult body weight (66 Kg). AT is the average exposure time (365 *70 years)

HI= \(\sum HQ\)……………………………..….. (3)

Where HI asses the combined metal exposure.

Chicken meat is widely used as a main food ingredient. The possibility of containing heavy metals in chicken meat in two ways. Either the feed consumed by boiler chicken in poultry form contains a high concentration of heavy metals as basic ingredients of feed or polluted water and nearby environment where chickens are rearing. The present study investigated the concentration of four heavy metals (cadmium, chromium, lead, and nickel) in poultry chicken meat, and one frozen chicken meat as a reference.

3.1 Cadmium: The concentration of cadmium in all chicken meat samples collected from different poultry shops in Skardu was recorded below the permissible limit set by WHO (see table 1). According to WHO, the permissible limit for cadmium is 0.5 mg/L. The research conducted in Kasur city, Pakistan showed 0.50+0.04 mg/L of cadmium in the chicken liver and 0.30+0.13 mg/L cadmium in the tissue of wings respectively. It is noticed that the concentration of cadmium in the liver and tissues is more than the WHO permissible limit. However, liver tissue achieved the maximum level of cadmium because the liver functions as a detoxication agent [29]. Another study conducted in Thatta City and Karachi City shows the cadmium concentration in chicken meat and blood was below the permissible limit of 0.5 mg/L [8]. Our study shows agreement with Thatta and Karachi research study.

There have been concerns raised recently about the presence of chromium in samples of chicken meat world-wide due to the possible effects on human health. Chromium, particularly in its hexavalent form (Cr VI)), can have damaging consequences on human health, including cancer, it is however an important trace element for many bodily activities [30-31]. Wang et al. examined chicken meat samples from several locales and found significant differences in chromium contents. To maintain food safety and reduce any possible health hazards linked to high chromium intake, the study underlined the necessity of monitoring and controlling chromium levels in poultry products [32]. Gao et al. ( ) reported the origins of chromium in chicken meat, accentuation the involvement of environmental contamination. The results of the study showed that various factors, including feed composition, water contamination, and soil quality, affect the amount of chromium present in chicken tissues [33]. To effectively apply mitigation techniques, it is imperative to comprehend the environmental pathways leading to the buildup of chromium in chicken meat. The public's health and the security of the food supply chain are at risk due to the growing demand for poultry products worldwide, which makes it crucial to address the problem of chromium contamination in chicken meat.

Table 1: Concentration of Cadmium in chicken samples

Sampling Site	Concentrations (mg/L)	WHO Permissible limit (mg/L)
Kharmang Poultry Shop	-10.7114	0.5
Kisaan Poultry Shop	-10.6402	0.5
GM Jawaid poultry	-10.6667	0.5
Shah Je poultry chicken	-10.5691	0.5
K&N’s meat	-10.7195	0.5

3.2 Lead: Lead has been detected in all chicken meat samples collected from different poultry shops in Skardu above the WHO permissible limit i.e., 0.2 mg/L (see table 2). The highest concentration of lead was observed in the kharmang poultry chicken meat sample which is 6.16 mg/L, while the lowest concentration of 3.62 mg/L was observed in the GM Jawaid poultry sample (see table 3.2. Similarly, different research articles also mentioned the high concentration of lead in different tissues of chicken such as wing, rib cage. Ingestion of contaminated feed and water is the most frequent way of lead exposure. The main target organs of lead are the kidneys, blood, and neurological system. Lead also affect the reproductive system of the body which includes miscarriage, male infertility, and infant morbidity and mortality. Lead contamination in food can have harmful consequences on health, it is a universal issue when it comes to meat products like chicken. Several global researchers have examined the level of lead present in chicken meat to determine the level of contamination. High amounts of lead were revealed in chicken meat in a study done in Bangladesh by Rahman et al.[34] which raised concerns about the possible health consequences connected to consumption of meat on regular bases. Li et al.'s reported the lead contamination in chicken, accent the necessity of regulation and oversight [ 35]. Discrepancies in the level of lead contamination were in chicken meat across the world according to a thorough study conducted by Smith et al. [36]. Certain areas, especially those with substantial levels of environmental contamination, showed higher levels of lead concentrations, while other regions reported comparatively low amounts. Research shows the higher lead contamination worldwide in chicken meat and demonstrate the importance of surveillance to guarantee food safety. Ahmed et al. observed the lead levels in samples of chicken meat from different parts of the country. The results showed different degrees of lead contamination, with larger concentrations found in areas, which may be related to environmental conditions and procedures used in poultry production [37]. Furthermore, Khan et al.'s research from 2021 looked at the connection between lead concentrations in chicken meat and possible health hazards for Pakistani chicken product consumers [38]. Comparing research from Pakistan with studies conducted worldwide shows regional differences and particular factors that affect lead levels in chicken meat [38-40].

Table 2 shows the concentration and absorbance of Pb in chicken meat samples

Sample name	Concentration (mg/L)	WHO Permissible limit (mg/L)
Kharmang poultry chicken meat	6.165	0.2
Kisaan poultry chicken meat	4.50	0.2
K&N’s meat	5.64	0.2
GM Jawaid poultry chicken meat	3.62	0.2
Shah Je poultry	4.03	0.2

3. 3 Nickel: The concentration of nickel was very high in all chicken meat samples and also above the WHO permissible limit which is 0.5 mg/L (see table 3). The highest concentration of nickel was recorded in the kisaan poultry chicken meat sample which is 157 mg/L, while the lowest concentration was observed in the GM Jawaid poultry chicken meat sample which is 150 mg/L. It is observed that the highest concentration of nickel was found in the chicken liver (8.29 mg/L) than in chicken blood (0.35 mg/L). That means it accumulates in the liver more than meat [8]. Several researchers worldwide conducted studies to determine the content of nickel in chicken meat. Smith et al. conducted a systematic study to inspect the concentrations of several heavy metals, including nickel, in poultry products in various nations. Significant differences in nickel concentrations were found in the study, with certain areas having higher levels than others [36]. Similarly, Jones and Brown investigated the presence of heavy metals in European poultry products, highlighting the significance of keeping an eye on nickel levels because of its cumulative toxicity. The aforementioned international studies offer significant perspectives on the worldwide context, emphasizing the necessity of standardization and regulation in the poultry sector to guarantee food safety [39]. There hasn't been much research done in Pakistan on the amount of nickel in chicken meat, therefore more investigation is necessary to determine any possible health risks. Khan et al.'s study focused on nickel levels and other heavy metal contamination in Pakistani poultry products [40]. The results highlighted the influence of regional characteristics on pollution levels by showing variations in concentrations between different regions. Establishing baseline data on nickel content in Pakistani chicken meat is essential for improving food safety laws. Current studies of the analysis of nickle in chicken meat samples of Skardu region agreed well with the studies of Khan et al.[40].

Table 3 shows the concentration and absorbance of Ni in chicken meat samples

Sample name	Concentration in (mg/L)	WHO Permissible limit (mg/L)
Kharmang poultry chicken meat	157.1454	0.5
Kisaan poultry chicken meat	157.3027	0.5
K&N’s meat	155.4154	0.5
GM Jawaid poultry chicken meat	150.5727	0.5
Shah Je poultry chicken meat	151.1276	0.5

3.4. Chromium: The chromium contamination has been observed in all chicken meat samples collected from different poultry shops in Skardu. The highest concentration of chromium was observed in the GM Jawaid poultry chicken meat sample which is 8.26 mg/L, while the lowest concentration of 3.03 mg/L was observed in the frozen meat sample (see table 4). In all chicken meat samples, the concentration of chromium is very high as compared to the WHO permissible limit which is 0.5 mg/L. The vital trace element chromium is involved in the metabolism of glucose, but too much of it might have negative consequences. Research conducted worldwide has sought to evaluate the chromium content of chicken meat while accounting for differences in environment, farming methods, and geographic areas. For example, a thorough studies by Wang et al. evaluated the concentration of chromium in chicken meat and found higher concentrations in different region of China [41], In a similar study, Jones et al.'s studied the chromium content in poultry products in the united states and concluded the possible health hazards connected to chicken meat consumption [ 42]. Ali et al. conducted a significant investigation on the presence of heavy metals in chicken meat, in different locations of Pakistan and found higher concentrations of chromium in chicken samples [43]. The lack of a thorough national comparison, however, underscores the need for further investigation on the heavy metal contents in chicken meat from various parts of Pakistan. It is critical to realize the heavy metal content of chicken that is consumed in the area in order to guarantee food safety and guide regulatory actions.

Table 4 shows the concentration and absorbance of Cr in chicken meat samples.

Sample name	Concentration (mg/L)	WHO (mg/L)
Kharmang poultry chicken meat	3.78	0.5
Kisaan poultry chicken meat	8.13	0.5
K&N’s meat	3.03	0.5
GM Jawaid poultry chicken meat	8.26	0.5
Shah Je poultry chicken meat	5.18	0.5

4.1. EDI: Estimated daily intake of heavy metal bio-accumulated in chicken meats collected from four different locations in the Skardu district were analyzed. The results are tabulated in table 5. The metal analysis showed that nickel showed the highest concentration of EDI in comparison to lead and chromium.

Table 5: EDI (mg/ kg) of analyzed metals in Chicken meat of five locations

Locations	Metal	MC (mg/Kg)	DC(g/day)	BW (Kg)	EDI (mg/kg/day)	*IARC Classification for Heavy Metals
Kh P	Ni	157.145	6.45	66	0.0177	2B
	Pb	6.165	6.45	66	0.0006	2B
	Cr	3.784	6.45	66	0.0004	1
KP	Ni	157.302	6.45	66	0.0177	2B
	Pb	4.501	6.45	66	0.0005	2B
	Cr	8.130	6.45	66	0.0009	1
JP	Ni	150.572	6.45	66	0.0169	2B
	Pb	3.624	6.45	66	0.0004	2B
	Cr	8.267	6.45	66	0.0009	1
SP	Ni	151.127	6.45	66	0.0170	2B
	Pb	4.038	6.45	66	0.0004	2B
	Cr	5.183	6.45	66	0.0005	1
FC	Ni	155.415	6.45	66	0.0175	2B
	Pb	5.647	6.45	66	0.0006	2B
	Cr	3.039	6.45	66	0.0003	1

*IARC classification for heavy metals: 1: human carcinogen; 2B: possible human cancer (IARC. (2012).

4.2. Target Hazard Quotient (THQ) and Hazard Index (HI):

The target hazard quotient (THQ) is used to assess the health impact of nickel, chromium, and lead through the consumption of chicken meat. It is observed that the THQ value is higher than the Reference daily intake (RfD) value. Whereas, EF, exposure frequency (365 days/ year); reference daily chicken consumption in Pakistan (109.6 and 82.2 g/person/day) for adults and children respectively); ED, exposure duration (70 years); BW, the average body weight of the population i.e., 66 Kg, and At, is the average time of exposure (365 days/year x ED). The values of RfD in the present investigation were 1.77 E-02, 6.96 E-04, and 4.27E-04 for Ni, Pb, and Cr, respectively (De Miguel et al., 2007). The HI of KP and JP are recorded highest in concentration.

Table 2: THQ and HI of the analyzed metals in chicken meat of five locations

Metals	ED	MC(ug/g)	FIR (g/day)	EF (365days/year)	RfD (mg/kg/day)	BW (Kg)	At (365 x exposure year )	TQ	THQ
KhP
Ni	70	157145.4	6.45	365	0.017738	66	25550	865771.8	8657.718
Pb	70	6165.049	6.45	365	0.000696	66	25550	865771.8	8657.718
Cr	70	3784.314	6.45	365	0.000427	66	25550	865771.8	8657.718
								HI	25973.15
KP
Ni	70	157302.7	6.45	365	0.017738	66	25550	866638.3	8666.383
Pb	70	4501.618	6.45	365	0.000696	66	25550	632172.5	6321.725
Cr	70	8130.719	6.45	365	0.000427	66	25550	1860138	18601.38
								HI	33589.49
JP
Ni	70	150572.7	6.45	365	0.017738	66	25550	829560.4	8295.604
Pb	70	3624.595	6.45	365	0.000696	66	25550	509010.2	5090.102
Cr	70	8267.974	6.45	365	0.000427	66	25550	1891539	18915.39
								HI	32301.1
SP
Ni	70	151127.6	6.45	365	0.017738	66	25550	832617.5	8326.175
Pb	70	4038.835	6.45	365	0.000696	66	25550	567182.8	5671.828
Cr	70	5183.007	6.45	365	0.000427	66	25550	1185763	11857.63
								HI	25855.64
FC
Ni	70	155415.4	6.45	365	0.017738	66	25550	856240.8	8562.408
Pb	70	5647.249	6.45	365	0.000696	66	25550	793056.1	7930.561
Cr	70	3039.216	6.45	365	0.000427	66	25550	695309	6953.09
								HI	23446.06

Based on the present study, it is concluded that the chicken meat from different locations was found to be contaminated with heavy metals (lead, nickel, and chromium). The concentration of cadmium was recorded below the maximum permissible limit, while the contamination level of nickel, lead, and chromium exceeded the maximum permissible limit set by WHO. Nickel it is inferred that from current research, these contaminants come either from poultry feed or open environment where chicken rears. Heavy metals is added in feed to increase meat production. However, monitoring is important to avoid the hazardous effects on human health. Knowing the highly toxic nature of these heavy metals, it is advised that the government and quality control authorities take quick action to ensure the cleanliness of the areas used to process poultry feed as well as to reduce environmental sources of heavy metal contamination.

ACKNOWLEDGMENT:

The research support is provided by the Chemistry lab of the Pakistan Council of Scientific and Industrial Research (PCSIR) Skardu.

FUNDING DECLARATION:

The authors declare that no funds, grants, or other support were received during the preparation of this manuscript.

COMPETING INTERESTS

The authors have no relevant financial or non-financial interests to disclose.

CONTRIBUTING AUTHORS:

Fazila Butt: Data Collection and Experimentation; Ishrat Jamil: Conceptualization; Supervision; Sample analysis Kousar Parveen: Draft preparation;Visualization:Data Analysis and validation; Muhammad Hussain: Paper Review; Hasnain Ali: Formal analysis

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No competing interests reported.

Assessment of the Bioaccumulated Metal Contaminants in Broiler Chicken -a Case Study From Skardu Pakistan

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Version 1

Abstract

Figures

1. Introduction

2. EXPERIMENTAL

3. RESULTS AND DISCUSSION

4. Health Risk Assessment

5. CONCLUSION

Declarations

References

Additional Declarations

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Version 1