Heavy metals in offal and canned food sold in the Malaysian market

Abstract

Food contaminated with heavy metals poses a serious threat to consumers. This study aims to assess levels of lead (Pb) and cadmium (Cd) in offals of chicken, cattle, and pig as well as tin (Sn) in canned food. A total of 378 offal samples was collected from wet markets, while 218 canned food samples were purchased locally. Samples were digested using a microwave before analysis with inductively coupled plasma mass spectrometry (ICP-MS). Pb was determined, highest in cattle lung (0.11 ± 0.20 mg/kg) followed by cattle spleen (0.09 ± 0.14 mg/kg), and cattle tripe (0.09 ± 0.12 mg/kg). For Cd, the highest concentrations were in cattle liver (0.13 ± 0.12 mg/kg), pig liver (0.08 ± 0.05 mg/kg), and chicken liver (0.03 ± 0.02 mg/kg). Significant variations of Sn levels existed in different canned food categories with 3.21% samples (n = 7) exceeded the maximum level of 250 mg/kg set by Codex Alimentarius. All offal samples were below the Malaysian regulatory limits, indicating their safety for human consumption. However, Sn levels varied significantly among canned food categories, with the highest levels found in canned pineapple chunks in syrup, mixed pineapple cubes in syrup, pineapple slices and longan. Samples exceeding the maximum level set by Codex Alimentarius may pose a risk to consumers.

KEYWORDS:

• Heavy metal
• internal organs
• processed food
• lead
• cadmium
• tin

Introduction

Heavy metals are common elements in the earth’s crust. Although some heavy metals are found in nature, industrial and agricultural operations contribute to the discharge of harmful elements into the environment. While some heavy metals are required for human chemical and biological functions, others have no known biological functions and pose a major concern due to their toxicity, bioaccumulation, and biomagnification qualities (Demirezen and Uruç 2006). It is usual that animals at the top of the food chain contain higher metal concentrations. For instance, up to 100% of methyl mercury in fish muscle is bioavailable which may harm species above them in the trophic pyramid (Baeyens et al. 2003; Jakimska et al. 2011).

Living organisms are exposed to heavy metals and trace elements through different routes namely inhalation of contaminants, consumption of contaminated drinking water, exposure to contaminated soils of industrial waste, and the ingestion of contaminated food (Duruibe et al. 2007). These undesirable substances as well as essential heavy metals have potential adverse effects, may enter the food chain and hence pose a risk to humans.

Despite the consumption of meat as a source of protein, the production of poultry meat generates large amounts of by-products that can be further consumed or utilized as food ingredients. Offal can be described as the internal organs and entrails of a butchered animal excluding muscle and bone (Marti and Johnson 2012) with differences existing between red and white offal. Red offal can be consumed directly and is recognized as a delicacy in certain parts of the globe whereas white offal such as stomach and intestines is edible but requires further processing. The average protein content in offal, regardless the source, is generally between 15% and 18% and contains both essential and non-essential amino acids (Mullen and Álvarez 2016). Chicken liver is one of the most eaten nutritious offal meat and edible chicken by-products. It accounts for 1.6–2.3% of chicken’s live weight and is a rich source of vitamins A, B12, and minerals (Ockerman and Basu 2004).

The advancement of technology has a great impact in the food industry as it eases the handling and storage of food products (Robertson 2005), as well as preserving the nutritional value and sensory characteristics of the food (Food Standards Australia New Zealand [FSANZ] 2017). However, the benefit is sometimes outweighed by the potential risk of chemical migration from packaging to food. Food packaging materials such as glass, ceramics, tin, and plastics may release small amounts of chemicals when in contact with the food which might be harmful to human health (Ardic et al. 2015). Regarded as one of the oldest packaging materials, tinplate is a steel sheet covered with protective coating to protect the steel from rust and corrosion (FAO 2005).

Most canned food products usually contain less than 10 mg/kg of tin although slow dissolution of tin coating from inside of the can may result in higher tin concentration to protect the can from corrosion. Tin is a soft, white, lustrous heavy metal with an atomic weight of 118.7 and the chemical symbol Sn after its Latin name, stannum. Having a relatively low melting point at 231.9 °C and being highly resistant to corrosion makes it an ideal element for the protective coating of metals. However, inorganic tin can cause gastric irritation, nausea, vomiting, and abdominal discomfort (FAO 2005).

Thus far, in Malaysia, studies on contamination of heavy metals in the internal organs of frequently consumed poultry are very limited. Previous studies from local researchers include the prevalence and quantification of pathogenic bacteria in chicken offal (Kuan et al. 2013) as well as determination of heavy metals in internal organs of marine fish from wet markets and supermarkets in Klang Valley, Malaysia (Nor Hasyimah et al. 2011).

Consumption of offal and canned food may pose a serious threat to consumers if the food contains high levels of contaminants. Hence, this study aims to determine levels of cadmium (Cd) and lead (Pb) in the internal organs of chicken, cattle and pig as well as tin (Sn) levels in canned food.

Materials and methods

Sample collection

Sample collection for offal and canned food took place from February till May 2021. A total of 378 samples of chicken, cattle and pig offal (a minimum of 250 g) were obtained from wet markets in all fourteen states in Malaysia with the assistance of health personnel from each respective state. The internal organs consisted of chicken liver (n = 42), pig liver (n = 42), cattle liver (n = 42), chicken gizzard (n = 42), cattle spleen (n = 42), cattle lung (n = 42), pork tripe (n = 43), cattle tripe (n = 43), and pig intestine (n = 40). All edible portions of samples were individually labelled in a zip-locked bag, packed in an icebox to maintain the freshness of the samples and transported to the laboratory for further analysis. Samples were checked thoroughly by laboratory staff and those samples which did not meet the criteria (e.g. samples sent were different from the list) were rejected and new samples were requested. Upon arrival at the laboratory, offal samples were immediately homogenized. Samples were then kept in centrifuge tubes in a chiller at 4 °C prior to further laboratory analysis the following day.

For canned food, 218 samples of numerous brands were purchased from locally manufactured products comprised ten states and sent directly either by courier or by road transport to the laboratory. The canned food was from the following categories: dairy products (n = 28), fruit (n = 31), meat and poultry (n = 28), sauces (n = 29), seafood (n = 39), soup (n = 28), and vegetables (n = 35). Assigned staff who received the samples thoroughly checked the brand names, sample ID, sampling date, sampling location, date of manufacture, expiry date as well as origin of the canned food samples. If the canned food samples were not produced in Malaysia, the samples were rejected and a new sample from the same category was requested. All canned food samples were kept at room temperature until further analysis. All samples were homogenized, weighed, and digested using a microwave prior to analysis of heavy metals (Pb, Cd & Sn) using Inductively Coupled Plasma-Mass Spectrometry (ICP-MS) following the method of Xing (2022).

Reagents

All solutions were prepared with analytical reagent-grade chemicals and ultrapure water (UPW-18.2 MΩ cm). Multi-element Calibration Standard 3 containing Cd and Pb (Product Number: N9300233; 10 µg/mL), Internal Standard Mix containing iridium (Ir) and rhodium (Rh) (Product Number: N9307738; 10 µg/mL), and tin standard (Product Number: N9303801; 10 µg/mL), were purchased from Perkin Elmer and certified for purity and concentration. All the laboratory apparatus were decontaminated by soaking in 10% v/v nitric acid (HNO₃) (Suprapur, Merck) prior to analysis.

Digestion procedure

The digestion procedure using a microwave was employed for internal organs and canned food samples using a method recommended by the instrument manufacturer (Milestone ETHOS Easy, Italy). A mass of 0.5 g sample was weighed and placed in a clean Teflon vessel. Digestion reagents used were 5 mL of 65% HNO₃, 2 ml of 30% hydrogen peroxide (H₂O₂), and 1 ml of ultrapure water (UPW). The following microwave program was applied: 10 min at 100 °C with 1800 W, 30 min at 100 °C with 1800 W, 10 min at 180 °C with 1800 W, 20 min at 180 °C with 1800 W. After digestion, samples were transferred into a 50 ml polyethylene centrifuge tube and total volume was made up to 20 mL with UPW. The digest solution was then filtered with 0.45 µm PTFE syringe filter and analyzed for heavy metals in duplicate. The analytical reagent blanks were also prepared in the same manner without the food sample.

Instrumental analysis and quality assurance

The heavy metals were analyzed using an ICP-MS ELAN 9000 (Perkin Elmer, USA) equipped with a Meinhard concentric quartz nebulizer, cyclonic spray chamber, nickel sampler, nickel skimmer cones and an autosampler. Iridium (Ir) and rhodium (Rh) were chosen as internal standards and all test batches were evaluated using an internal quality approach and validated to ensure they satisfied the defined internal quality controls. Each analysis involved a blank, internal standard in samples and samples analyzed in duplicate to eliminate batch-specific error. The calibration curves generated for Cd, Pb, and Sn determination were highly linear (r² > 0.999). External calibration standards used for quantitation were made up from a 10 µg/mL Reference Standard, ICP-MS Multi Element Calibration Standard 3 in 5% (v/v) HNO₃ acid as 1.25, 2.5, 5.0, 10.0, and 20.0 µg/L for Cd and Pb. For Sn, external calibration standards were prepared from a 1000 µg/mL Tin standard in 1% (v/v) HCl at 2.5, 5.0, 10.0, and 20.0 µg/L.

The precision of the method was evaluated by matrix spiking through the addition of low, medium, and high known concentrations of elements (Cd, Pb, Sn) to the food samples. The concentration of the samples before and after the addition was measured. The recovery values of these elements were within the acceptable range, 85% to 115%. Certified reference material (CRM), Bovine liver (European Reference Materials ERM-BB185), was analyzed to ensure quality control of this analysis. The average recovery of reference standards was 86.5% and 88.4% respectively for Cd and Pb. For Sn, no CRM was used and a quality assurance strategy of matrix spiking was employed as explained above. The LOD values for Cd, Pb, and Sn were 0.0001, 0.0011, and 0.0008 mg/kg and the LOQ was 0.0004, 0.038, and 0.027 mg/kg for Cd, Pb, and Sn respectively.

Statistical analysis

IBM SPSS Statistics 26 was used to analyse the data. Data are expressed as median ± interquartile range. Data were cleaned and examined for discrepancies before analysis Descriptive statistics were used to assess data normality using the one-sample Kolmogorov–Smirnov test, and/or the skewness of descriptive statistics was regulated between -1 and +1, whichever was true. Due to outliers, the descriptive statistical analysis revealed that both groups of data were not normally distributed. As a result, non-parametric statistics were employed. The medians and interquartile range were calculated. The Mann-Whitney U and Kruskall–Wallis tests were used to analyse differences across groups. A level of significance at 0.05 was set to ensure the results were statistically significant. Significance values were adjusted by the Bonferroni correction for multiple tests.

Comparison of heavy metal levels with existing regulation or standards

Levels of Cd and Pb in offal were compared with the Fourteenth Schedule (Regulation 38) – Maximum Permitted Proportion of Metal Contaminant in Specified Food (Tables 1 and 2) of the Malaysian Food Regulations 1985. The maximum level of Cd in meat and meat products other than edible gelatin = 1 mg/kg while for Pb = 2 mg/kg. The levels of Sn in canned food were compared to the Codex General Standard for Contaminants and Toxins in Food and Feed (Codex Alimentarius 1995), which = 250 mg/kg.

Table 1. Heavy metals in internal organ (Pb & Cd) and canned food (Sn) by different categories from selected local markets.

No	Food samples by categories	N	Heavy metals (mg/kg) (ww)
			Median	IQR	Min	Max	Range
Internal organ
	Pb
1	Chicken liver	42	0.01	0.05	0.05	0.23	0.18
2	Chicken gizzard	42	0.04	0.08	0.04	1.58	1.54
3	Pig liver	42	0.03	0.04	0.04	0.13	0.09
4	Pig intestine	40	0.04	0.05	0.04	0.85	0.81
5	Pork tripe	43	0.03	0.05	0.04	0.35	0.31
6	Cattle liver	42	0.08	0.20	0.04	1.52	1.48
7	Cattle spleen	42	0.09	0.14	0.05	0.81	0.76
8	Cattle lung	42	0.11	0.20	0.04	0.47	0.43
9	Cattle tripe	43	0.09	0.12	0.05	0.65	0.60
	Total	378
	Cd
1	Chicken liver	42	0.03	0.02	0.01	0.22	0.21
2	Chicken gizzard	42	0.01	0.01	0.00	0.03	0.03
3	Pig liver	42	0.08	0.05	0.00	0.34	0.34
4	Pork tripe	43	0.00	0.00	0.00	0.02	0.02
5	Pig intestine	40	0.01	0.02	0.00	0.39	0.39
6	Cattle liver	42	0.13	0.12	0.00	0.47	0.47
7	Cattle spleen	42	0.01	0.01	0.00	0.08	0.08
8	Cattle lung	42	0.02	0.03	0.00	0.22	0.22
9	Cattle tripe	43	0.00	0.00	0.00	0.03	0.03
	Total	378
Canned food
	Sn
1	Meat & poultry	28	0.08	0.11	0.01	0.34	0.33
2	Fruits	31	186	135	96	937	841
3	Vegetables	35	0.11	0.15	0.00	231	231
4	Seafood	39	0.34	0.64	0.00	2.06	2.06
5	Sauces	29	0.37	2.12	0.00	19.3	19.3
6	Soup	28	0.05	0.11	0.00	4.42	4.42
7	Dairy products	28	0.62	2.25	0.00	11.0	11.0
	Total	218

ww: wet weight; IQR: Interquartile range.

Table 2. Pairwise comparison for significant differences (p-value < .05) between median concentration of heavy metal for different categories of food samples.

No	Sample categories/elements	p-values
		Chicken liver	Pig liver	Cattle liver	Chicken gizzard	Cattle spleen	Cattle lung	Pork tripe	Cattle tripe	Pig intestine
Internal organs/Cd
1	Chicken liver	–
2	Pig liver		–
3	Cattle liver	0.026	–	–
4	Chicken gizzard	–	0.001	0.000	–
5	Cattle spleen	0.000	0.000	0.000	–	–
6	Cattle lung	–	0.003	0.000	–	–	–
7	Pork tripe	0.000	0.000	0.000	0.002	–	0.000	–
8	Cattle tripe	0.000	0.000	0.000	0.000	–	0.000	–	–
9	Pig intestine	0.014	0.000	0.000	–	–	–	–	0.005	–
Internal organs/Pb
1	Chicken liver	–
2	Pig liver	–	–
3	Cattle liver	0.000	0.006	–
4	Chicken gizzard	–	–	–	–
5	Cattle spleen	0.000	0.009	–	–	–
6	Cattle lung	0.000	0.000	–	–	–	–
7	Pork tripe	–	–	0.026	–	0.035	0.001	–
8	Cattle tripe	0.000	0.008	–	–	–	–	0.026	–
9	Pig intestine	–	–	–	–	–	0.008	–	–	–
Canned food/Sn		Meat & poultry	Fruits	Vegetables	Seafood	Sauces	Soup	Dairy products
1	Meat & poultry	–
2	Fruits	0.000	–
3	Vegetables	–	0.000	–
4	Seafood	–	0.000	–	–
5	Sauces	–	0.000	–	–	–
6	Soup	–	0.000	–	0.032	–	–
7	Dairy products	–	0.000	–	–	–	–	–

Results

Sample distribution

A total of 596 food samples which consisted of 378 internal organ and 218 canned food samples were collected throughout the country. An equal number of samples were collected for internal organs by all States but for canned food samples, no samples were received from Kedah, Kelantan, Negeri Sembilan and Perlis. The canned foods collected during this study were from 50 different brands, Brand C (n = 39; 17.9%), Brand F (n = 20; 9.2%), Brand N (n = 16; 7.3%), Brand O (n = 15; 6.9%), Brand A (n = 15; 6.9%), Brand P (n = 10; 4.6%), Brand G (n = 9; 4.1%) and Brand J (n = 7; 3.2%). For other brands, a smaller number of samples were received, with most of them only 1 or 2 samples.

Heavy metals in food samples

A total of 56 samples (14.8%) did not contain detectable Pb whilst another 43 samples (11.4%) did not contain detectable Cd. For the rest of the samples, both elements were determined and their concentrations were calculated accordingly (Table 1). From independent samples, the Kruskal–Wallis test showed that there are significant variations at p < .001 for both Pb and Cd levels existed in different categories of internal organs at ${\mathrm{\chi }}_{\mathrm{KW}}^2$ =70.44 and at ${\mathrm{\chi }}_{\mathrm{KW}}^2\mathrm{ }=$215.23, respectively. Pb was found in different concentrations, ranging from 0.04 mg/kg in pork tripe to a maximum of 1.58 mg/kg in chicken gizzard. Median concentrations of Pb in internal organs were highest in cattle lung (0.11 ± 0.20 mg/kg) followed by cattle spleen (0.09 ± 0.14 mg/kg), cattle tripe (0.09 ± 0.12 mg/kg) and cattle liver (0.08 ± 0.20 mg/kg). The concentration of Cd was highest in cattle liver samples (0.13 ± 0.12 mg/kg) and its median concentrations in internal organs in descending order were as follows: pig liver (0.08 ± 0.05 mg/kg), chicken liver (0.03 ± 0.02 mg/kg) and cattle lung (0.02 ± 0.03 mg/kg).

Sn was not detected in 4.1% (n = 9) of canned food samples. Significant variations of Sn levels existed in different canned food categories (${\mathrm{\chi }}_{\mathrm{KW}}^2$=94.7; p < .001). When compared to different categories of canned food, an extreme level of Sn was shown in canned fruits ranging between 95.9 mg/kg to 937 mg/kg with median levels of 186 ± 135 mg/kg. The highest concentration of Sn found for each of the categories canned vegetable, sauces and dairy products was 231 mg/kg, 19.3 mg/kg and 11.0 mg/kg, respectively.

Pairwise comparison using Bonferroni correction on the median concentration of heavy metal levels in different food samples showed significant differences (p-value < .05) between different food categories and are shown in Table 2. Cd in chicken liver was significantly lower (p < .05) compared to its level in four categories of internal organ; a cattle spleen, pork tripe, cattle tripe and pig intestine. No significant differences (p > .05) were shown for other internal organ samples. In contrast, Cd levels in pig liver and cattle liver were significantly higher (p < .05) than those in all other internal organ samples. Cd levels were significantly higher in chicken gizzard and cattle lung when compared to those found in pork tripe and cattle tripe. Pb levels were significantly higher (p < .05) in chicken liver when compared to those in cattle liver and cattle spleen, but were significantly lower (p < .05) in both cattle lung and tripe samples. Pb levels in pig liver and its tripe were significantly the lowest (p < .05) when compared to those in four other internal organs: the cattle liver, lung and tripe, also the cattle spleen.

Highly significant differences (p < .001) were found for Sn in canned fruits compared to all other canned food categories. Sn level in canned seafood was significantly higher (p = 0.032) compared to its level in canned soup. Other canned food samples showed no differences (p > 0.05) for Sn level between food categories.

Samples exceeding the Malaysian food Regulations 1985 and Codex Alimentarius

The 14^th Schedule of Regulation 38, Malaysian Food Regulation 1985 sets a maximum level of Cd and Pb in selected food from different categories. None of the Cd and Pd levels in the internal organs exceeded the maximum level prescribed in the 14^th Schedule of Regulation 38, Malaysian Food Regulations 1985. However, for canned food, seven samples (3.2%) exceeded the maximum level of 250 mg/kg which was set in the Codex General Standard for Contaminants and Toxins in Food and Feed (Codex Alimentarius 1995) (Table 3). Levels of Sn in canned food that exceeded the standard were between 251 mg/kg and 937 mg/kg. The highest Sn concentration was found in four samples of pineapple slices/cubes/chunks in syrup and longan fruit in syrup, which were collected from East Malaysia (Sabah and Sarawak) under different brand names. All samples exceeding the limit for pineapple in syrup except one sample which was longan fruit in syrup. Canned pineapple chunks in syrup were from Brand C, the pineapple slice was under Brand A while the mixed pineapple cubes and longans in syrup were from Brand B and Brand D, respectively.

Table 3. Levels of Sn (mg/kg) in canned food exceeding Codex General Standard for Contaminants and Toxins in Food and Feed (CXS 193-1995).

No	Sample name	Brand	Categories	Sampling locations	Levels (mg/kg)	Maximum level (mg/kg)
1	Pineapple slices	Brand A	Fruits	JKN Sabah	937	250
2	Mixed pineapple cubes in syrup	Brand B	Fruits	JKN Sarawak	550
3	Pineapple chunks	Brand C	Fruits	JKN Sarawak	403
4	Longan	Brand D	Fruits	PKB Mukah	302
5	Pineapple chunks in syrup	Brand C	Fruits	Terengganu	298
6	Pineapple chunks in syrup	Brand C	Fruits	Melaka	287
7	Pineapple chunks in syrup	Brand C	Fruits	JKN P Pinang	251

Table 4 showed some of canned food products by different brands and sampling locations that contain comparatively higher levels of Sn (10.1–249 mg/kg). There were 9 canned pineapple and one canned mushroom sample exhibiting Sn level ranging between 200 and 249 mg/kg. Another 16 canned pineapple and one longan fruit in syrup samples contained Sn between 96 and 187 mg/kg. Four canned food samples other than canned fruits; one each of pasta sauce with mushroom, tomato puree and two samples of sweetened creamer, contained Sn between 10 and 20 mg/kg. The findings of this study revealed a large number of canned pineapples in syrup samples contained Sn at relatively high concentration. A total of 19 samples were from Brand C products, with seven canned fruits exceeding Codex Alimentarius standard, and another 15 canned fruits from the same brand contained high levels of Sn.

Table 4. High levels of Sn (mg/kg) determined in some canned food samples.

No	Sample name	Brand	Categories	Sampling locations	Sn (mg/kg)
1	Pineapple slices in syrup	Brand E	Fruits	Kuala Lumpur	249
2	Pineapple slices	Brand E	Fruits	Selangor	246
3	Pineapple chunks	Brand F	Fruits	JKN P Pinang	244
4	Mushroom slice	Brand G	Vegetables	JKN P Pinang	231
5	Pineapple chunks in syrup	Brand C	Fruits	Johor	221
6	Tropical fruit cocktails	Brand H	Fruits	PKB Limbang	217
7	Pineapple slices	Brand E	Fruits	JKN P Pinang	212
8	Pineapple chunks in syrup	Brand C	Fruits	PK Kinta	208
9	Pineapple chunks in syrup	Brand C	Fruits	PK Kinta	204
10	Pineapple chunks in syrup	Brand C	Fruits	Terengganu	186
11	Pineapple chunks	Brand C	Fruits	JKN Sabah	185
12	Longan	Brand D	Fruits	PKB Kapit	165
13	Pineapple slices	Brand I	Fruits	PKB Betong	155
14	Pineapple chunks in syrup	Brand C	Fruits	Melaka	141
15	Pineapple chunks	Brand C	Fruits	Selangor	127
16	Pineapple chunks	Brand J	Fruits	JKN Sabah	126
17	Pineapple chunks	Brand C	Fruits	Selangor	117
18	Pineapple chunks	Brand I	Fruits	JKN Sarawak	114
19	Pineapple chunks in syrup	Brand C	Fruits	Kuala Lumpur	110
20	Pineapple chunks in syrup	Brand C	Fruits	PK Kinta	110
21	Pineapple chunks in syrup	Brand C	Fruits	Kuala Lumpur	106
22	Pineapple chunks in syrup	Brand C	Fruits	Johor	105
23	Pineapple chunks	Brand C	Fruits	Terengganu	100
24	Pineapple chunks in syrup	Brand C	Fruits	Melaka	98
25	Pineapple chunks in syrup	Brand C	Fruits	Johor	99
26	Mushroom pasta sauce	Brand F	Sauces	Kuala Lumpur	19.3
27	Sweetened creamer	Brand K	Dairy products	PKB Kapit	11.0
28	Tomato puree	Brand L	Sauces	PKB Betong	11.0
29	Sweetened creamer	Brand M	Dairy products	Terengganu	10.1

Discussion

This surveillance study was carried out to determine heavy metal in two different types of food: (1) Pb and Cd levels in internal organs of chicken, cattle, and pig sold in the Malaysian market and (2) Sn in canned food from locally manufactured products. The study was carried out comprehensively, on a wide range of internal organ and canned food samples (378 internal organ and 218 canned foods, respectively) collected from the different geographical areas throughout states in West and East Malaysia, over different periods of time within four months from February to May 2021.

Several interesting findings arose from this study: The data indicated that Cd and Pb levels differed significantly among different categories of internal organs, but for Sn, this element was the highest in canned fruit especially pineapple in syrup. Results also showed that none of the Cd and Pd levels in the internal organs exceeded the Malaysian Food Regulations 1985. On the other hand, Cd was higher in cattle liver and pig liver, while Pb was higher in cattle internal organ (lung, tripe, liver and spleen). More than 3% of canned foods samples exceeded the maximum level set by Codex Alimentarius for Sn determination. Each of these aspects is covered in detail below.

The whole dataset of this study provides important baseline information on the investigation of Cd and Pb contamination status in internal organs samples collected throughout States in Malaysia. Despite the well-known toxicity of heavy metals in food especially in seafood, these metals have been poorly investigated in these groups of food. Globally, we also found few published articles reported on the level of Sn in canned fish or seafood, fruits and vegetables and other types of food as well, but none were from Malaysian products.

Results from this study revealed that Cd and Pb in internal organ samples were significantly different (p < .001) between different categories and fortunately all samples were below the maximum level in the Malaysian Food Regulations 1985. To be accurate, the highest Cd level was in cattle liver (0.13 mg/kg) while for Pb was in cattle lung (0.11 mg/kg). Overall, the median Cd and Pb levels in internal organs were between 0.00–0.13 mg/kg and 0.01–0.11 mg/kg, respectively. Both Cd and Pb data sets were not normally distributed due to the existence of the outliers.

When we compared levels of both heavy metal in a few earlier studies published by countries in different regions, the results were diverse. Results from this study agreed with a study conducted by Leontopoulos et al. (2015) when they reported that none of the metals in pigs’ internal organ collected around the Pieria-Macedonia region in Greece, exceeded the maximum EU maximum limits. On the other hand, the level of Pb in chicken liver and gizzard in a study conducted in the Philippines (Villar et al. 2005) and Iran (Naseri et al. 2021) were very much higher when compared to the levels in this study. In fact, Pb in chicken liver in the Philippines study was tenfold higher, while its level in chicken gizzard was nearly eightfold higher. Cd level in chicken liver in the Iranian study were higher by nearly three times but its level in chicken gizzard was lower by half. Nevertheless, in the first study, the Cd level was similar for both samples. Besides, levels of both Pb and Cd in cattle offal (Birnin-Yauri et al. 2018; Hillary-Frances and Emmanuel 2019) and chicken liver (Ogwok et al. 2014) from the African region were even higher compared to results from this study.

Animals can be exposed to heavy metals by inhalation and ingestion, and they can act as indicators of Pd and Cd pollution in water, air, and soil (Naseri et al. 2021). The volume of heavy metals in an animal’s food is determined by the volume of heavy metals in its feed, which is largely determined by the ability of agricultural plants to integrate the elements into their tissues and the concentration of heavy metals in the soil (Hejna et al. 2018; Chałabis-Mazurek et al. 2021). Commercial feed combinations containing cereals like corn and green beans, by-products of cereals, fish products, oil plant seed products and by-products of sugar manufacturing, among other things, may contain Cd and Pb (Villar et al. 2005; Hejna et al. 2018). Heavy metals are naturally present in the soil, but they are additionally introduced as a component by the application of minerals and organic fertilizers, animal excrement and urination, and pesticides (Hejna et al. 2018). Animals are also exposed to Pb and Cd through the consumption of contaminated vegetation (Villar et al. 2005; Reis et al. 2010).

Food absorption in the poultry digestive system is predominantly through the intestine and when gizzards receive feed materials it digested them with little absorption. Due to the functions of these two organs, heavy metals are usually absorbed and stored (Villar et al. 2005). When Cd is ingested, it is absorbed by intestinal cells and transported by blood flow to the liver and induces metallothionein synthesis to form Cd-metallothionein complexes. These complexes are released into the bloodstream and filtered by the kidney. Nevertheless, Pb is absorbed as acetate and carbonate to form insoluble complexes in the gastrointestinal tract and is later excreted with feces (Reis et al. 2010). This heavy metal is also known to accumulate mostly in the liver (Birnin-Yauri et al. 2018), where storage, metabolism and biosynthesis activities take place. It is also the principal site of xenobiotic metabolism (Villar et al. 2005). It receives all the material that enters the gastrointestinal tract via the portal vein including toxic elements (Naseri et al. 2021). The liver is the main organ for the accumulation of these two heavy metals in animals as their elimination rate is relatively low due to the formation of protein metallothionein complexes in the organ (Ambushe et al. 2012). Yet, our findings showed that both heavy metals were found in low concentrations or below national requirements in the internal organs of either poultry or cattle, which is an indication of their safety for human consumption.

Results of this study revealed a significant variations of Sn levels existed in different canned food categories with an extreme level of this heavy metal recorded in canned fruits especially canned pineapple chunks in syrup. Out of 36 canned foods with comparatively higher Sn content, 78% were canned pineapple. The maximum acceptable level of Sn, 250 mg/kg, was exceeded in six samples of canned pineapple (251.3–937.1 mg/kg) and one sample of longan in syrup (302.2 mg/kg). Four of these canned food samples were from Brand C. Higher amounts of Sn were observed in many other canned pineapples throughout states in the country and other products as well for example canned mushroom, sources, tomato puree and sweetened creamers. Highly significant differences (p < .000) were shown for Sn level in canned fruits compared to all other canned food categories.

Results obtained from this study can be directly compared to results reported by Knápek et al. (2009) in their study on heavy metals in canned fruits from the Czech market. Their study showed many local canned fruits products which exceeded permissible levels of Sn (200 mg/kg) such as canned pineapple (238 mg/kg), mushroom (189 mg/kg), apricot (154 mg/kg), fruit cocktail (166 mg/kg), peach (209 mg/kg), grapefruits (311 mg/kg), mandarin (142 mg/kg), lychee (138 mg/kg) and beans (352 mg/kg) which they categorized as sour products and products in uncoated cans (Knápek et al. 2009). On the other hand, Rončević et al. (2012) reported a lower range of Sn in canned fruits and vegetables from the commercially available Croatian market with no exceedances compared to the country maximum permissible level. In their study, Sn was determined at levels between <5 and 200) mg/kg with only 5 samples showed levels of more than 100 mg/kg (range 106–199 mg/kg). The highest level was in pineapple compote (199 mg/kg) canned in partially protected tinplate (Rončević et al. 2012). Other samples such as apricot compote (116 mg/kg), fruit cocktail (109–117 mg/kg) and mandarin oranges (106 mg/kg) were also canned in partially protected tinplate. They confirmed that protected cans may lead to lower concentrations of Sn by ten times compared to non- or partially-protected tinplate. Results from other studies such as Korfali & Hamdan (2013), Munteanu et al. (2010), and Yabanli et al. (2021) showed levels of Sn at a very much less or below detection limits in canned fruits, vegetables and seafood samples collected from their local markets when compared to this study.

It has been claimed that using simple uncoated internal tinplate surfaces can cause some tin to dissolve into the food (Rončević et al. 2012). When metallic tin from the inside of the can body dissolves, the divalent form of tin, Sn 2+, tin (II), or stannous tin, is frequently present in the food and its liquid (Blunden and Wallace 2003). These oxidation states are likely to have a major influence on its ability to cause an acute toxicological response. However, the specific species will vary depending on the circumstances involved, one of which being the presence of tin-corroding oxidizing agents or depolarizers. Nitrates are the most frequently found oxidizing agents, followed by anthocyanins (Blunden and Wallace 2003; Ismail et al. 2018). These two chemicals, that possibly originate from food ingredients, have been suggested to accelerate the dissolution of tin (Blunden and Wallace 2003). Other factors involved were the temperature used for storage, can size, types of base steel and the level of hydrogen in the base steel (Blunden and Wallace 2003; Ismail et al. 2018). Low pH values of canned liquid may boost the oxidizing agent to cause dissolution of metal by oxidation reaction (Ismail et al. 2018).

There are studies reflecting on differences of tin concentration between syrup and fruits; these showed that Sn concentration reached higher amounts in the solid parts compared to syrup (Knápek et al. 2009). The corrosion of the tinplate surface was enhanced by air where the amount of dissolved Sn in fruits and syrups were increased after the can was open and refrigerated for a few days (Knápek et al. 2009). Another study by Rončević et al. (2012) had shown the concentration of tin in protected cans was less by ten times compared to nonprotected or partially protected tinplate. Foods such as canned vegetables that are stored and preserved in liquid media which enhances the leaching of tin from the can, are better stored in cans with less Sn and/or be more carefully lacquered so leaching of Sn into food is minimal (Korfali and Hamdan 2013). A study on corrosive performance of aluminum (Al) and Sn as beverages packaging showed the corrosive rates of Sn are much higher than Al and clearly proved that corrosion resistance of Al is higher than tinplate in acidic solutions (Ismail et al. 2018). These are good reasons why Al is replacing tin for industrial purposes and is applicable for food preserved or soaked in liquid media or syrup at pH 4.6 and lower (McGlynn 2016; Blunden and Wallace 2003). Even though tinplate cans are cheaper than the Al, both may react to become toxic to humans but they are not inherently toxic. Al is corrosion-resistant, has light weight and density, high electrical and thermal conductivity, and high ductility and is easily deformable. For this reason, it has replaced tin in the packaging and food industries and widely used in many other industries for example aerospace and transportation industries, building and construction and so forth (Rahimzadeh et al. 2022). To avoid dissolution of Sn, fruits and vegetables in syrup/liquid with a lower pH should be canned in a fully protected tinplate or an Al can despite the greater cost.

Conclusions

This study assessed the heavy metal content (Pb, Cd and Sn) in two different types of food, heavy metals (Pb and Cd) in internal organs of chicken, cattle, and pig from Malaysian market and Sn in canned food from locally manufactured products. Results showed that none of the internal organ samples surpassed the maximum level under the Malaysian Food Regulations 1985 for Pb and Cd at level of 2 mg/kg and 1 mg/kg respectively. Therefore, the internal organs from the local market, in general, are safe for human consumption. However, findings revealed that levels of Pb and Cd in various organs differed significantly. Pb was found significantly higher in cattle internal organs (lung, stomach, liver and spleen) while Cd was very much higher in cattle liver and pig liver.

Results of this study revealed that Sn levels varied significantly among canned food categories, with the highest levels of this heavy metal found in canned fruits, particularly canned pineapple chunks in syrup. A number of samples exceeded the maximum level and several were from the same brand name. Higher levels of Sn were observed in many canned pineapples. It is worth noting that if canned fruits are consumed in large quantities, the possibility of Sn contamination may still pose a threat to human health. This is especially true when it comes to canned foods that have been shown to contain medium to extremely high levels of Sn contamination. Thus, these data are an essential part of assessing potential health hazards from Sn contamination to the population in Malaysia.

Authors contributions

Zurahanim Fasha and Nurul Izzah wrote the main manuscript text. Zurahanim Fasha and Cathrinena were involved in laboratory analysis, format and data cleaning. Nurul Izzah Ahmad, Laila Rabaah Ahmad Suhaimi, Nurul Hidayati Surawi, Kasumawaty Sudin, Ani Fadhlina Mustaffa, Anida @ Azhana Husna Zainudeen, Shazlina Mohd Zaini and Nor Azmina Mamat assisted in QC check and data analysis. All authors reviewed the manuscript.

Acknowledgements

A special thanks to the Director General of Health Malaysia and Senior Director for Food Safety and Quality, Ministry of Health Malaysia for giving permission to publish this article. The authors acknowledge support and assistance provided by staff of the Environmental Health Research Center, Institute for Medical Research and State Food Safety and Quality Division as well as State Health Department for assistance in sample collection throughout the commencement of the project.

Disclosure statement

The authors declare that there is no competing interest.

Data availability statement

The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.

Additional information

Funding

This study was supported by the Food Safety and Quality Division, Ministry of Health Malaysia.