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Article

Effect of a Diet Supplemented with Nettle (Urtica dioica L.) or Fenugreek (Trigonella Foenum-Graecum L.) on the Content of Selected Heavy Metals in Liver and Rabbit Meat

by
Sylwia Ewa Pałka
1,*,
Ewa Drąg-Kozak
2,
Łukasz Migdał
1 and
Michał Kmiecik
1
1
Department of Genetics, Animal Breeding and Ethology, University of Agriculture in Krakow, Al. Mickiewicza 24/28, 30-059 Krakow, Poland
2
Department of Animal Nutrition and Biotechnology, and Fisheries, University of Agriculture in Krakow, St. Spiczakowa 6, 30-199 Krakow, Poland
*
Author to whom correspondence should be addressed.
Animals 2022, 12(7), 827; https://doi.org/10.3390/ani12070827
Submission received: 2 February 2022 / Revised: 18 March 2022 / Accepted: 23 March 2022 / Published: 24 March 2022
(This article belongs to the Special Issue Meat Quality and Protein Expression in Livestock and Poultry)
Review Reports Versions Notes

Abstract

:

Simple Summary

Herbs can be a good supplement in an animal diet. With the current increase in the use of herbs and herbal preparations as an animal feed additive, it is very important to monitor the contaminants present in plants, i.e., heavy metals, and to study their content in animal tissues. The toxicity of heavy metals, whether essential or not, depends on several factors including the dose in feed (food), a route of exposure, and sex. Hence, it seems advisable to determine the effect of nettle (Urtica dioica L.) leaves and fenugreek (Trigonella foenum-graecum L.) seeds in the feed on the content of selected heavy metals in the liver and meat of the rabbit, and determine differences in sex in metal accumulation. The experiment was conducted at University of Agriculture in Krakow (Poland) in the Experimental Station of the Department of Genetics, Animal Breeding, and Ethology. The research material consisted of Termond White rabbits. Until weaning (on the 35th day of life), young rabbits with does were housed in wooden cages. From weaning until the 84th day of life, rabbits were kept in wire metal cages. Three experimental groups were created: the control group (n = 20; 10♂ and 10♀) was fed ad libitum with a complete feed. The animals from group N (n = 20; 10♂ and 10♀) were fed a complete mixture with added 1% nettle leaves. The rabbits from the group F (n = 20; 10♂ and 10♀) were fed with a complete mixture with added 1% fenugreek seeds. The experiment lasted 7 weeks (from 35th to 84th day of the rabbits’ life). All rabbits were slaughtered on the 84th day of age, with an average body weight of 2546 ± 47 g. Samples of liver were taken during the slaughter. Then, the carcasses were cooled for 24 h at 4 °C, and after that time, a sample was taken from the right loin (m. longissimus lumborum) of each carcass. The concentration of heavy metals (Zn, Cu, Ni, Mn, Fe, Pb, Cd) was determined by the atomic absorption spectrometry (AAS). The additives to the feed significantly affected the content of elements in both the liver and the meat of the rabbits (p < 0.05). The highest level of the heavy metals, regardless of the used diet, was recorded in the liver. The meat and the liver of rabbits fed with herbal fodder contained less tested metals than in animals fed with fodder without additives. Moreover, more essential metals were found in the liver of rabbits fed with fenugreek than rabbits fed with nettle (p < 0.05). In the meat and liver of rabbits, the permissible content of cadmium and lead was not exceeded. Additionally, male livers had a significantly higher content of copper and manganese compared to female livers (p < 0.05). This experiment helps to explain the interaction between the heavy metal content of nettle and fenugreek and their content in rabbit meat and liver. The meat (m. longissimus lumborum) and liver of rabbits fed with herbal feed contained fewer tested metals than in animals fed with the feed without additives. Concentrations of toxic metals, i.e., Pb and Cd in liver and meat, were so low that meat consumption does not pose a threat to human health. However, more research is needed to determine how the mechanisms and pathways of heavy metal toxicity act on tissue in which these metals are accumulated.

Abstract

The literature on herbal additives for rabbit feed offers little information on the use of nettle and fenugreek. Both of these herbs are valuable sources of vitamins and minerals. These herbs affect the growth, health, and meat quality of rabbits. They regulate the digestive system, stimulate the appetite, have a positive effect on the functioning of the immune system, and exhibit antibacterial activity. The purpose of the present study was to determine the effect of nettle (Urtica dioica L.) leaves or fenugreek (Trigonella foenum-graecum L.) seeds in the feed on the content of selected heavy metals in the liver and meat of the rabbit. The rabbits were divided into three groups: group C (n = 20; 10♂ and 10♀) was fed ad libitum with a complete feed, N group (n = 20; 10♂ and 10♀) was fed a complete mixture with 1% added nettle, and group F (n = 20; 10♂ and 10♀) was fed with a complete mixture with 1% added fenugreek. The experiment lasted 7 weeks (from the 35th to the 84th day of the rabbits’ lives). All the rabbits were slaughtered on the 84th day of age, with a body weight of about 2.6 kg. The concentration of heavy metals (Zn, Cu, Ni, Mn, Fe, Pb, Cd) was determined by the atomic absorption spectrometry (AAS). The additives to the feed significantly affected the content of elements in both the liver and the meat of rabbits (p < 0.05). The highest level of the heavy metals, regardless of the used diet, was recorded in the liver (p < 0.05). The meat (m. longissimus lumborum) and the liver of rabbits fed with herbal fodder contained less tested metals than in animals fed with fodder without additives (p < 0.05). Moreover, more essential metals were found in the liver of rabbits fed with fenugreek than rabbits fed with nettle. In the meat and liver of rabbits, the permissible content of cadmium and lead was not exceeded. Additionally, male livers had a significantly higher content of copper and manganese compared to female livers (p < 0.05). It is important to study the content of heavy metals in the used animal herbal feed additives and their interaction with each other, as they affect the distribution of elements in tissues and organs.

1. Introduction

Rabbit meat is characterized by outstanding taste and nutritional and dietary properties. Next to poultry and fish, rabbit meat belongs to the so-called white meats. Like other white meats, rabbit meat contains little iron (1.1–1.3 mg/100 g of meat) and zinc (0.55 mg/100 g of meat) [1]. It also has low sodium content (37–47 mg/100 g of meat). Excess sodium being one of the main causes of hypertension, this makes it an ideal meat for people at risk thereof. Rabbit meat also contains more potassium (428–431 mg/100 g edible fraction) and phosphorus (222–234 mg/100 g edible fraction) than pork, beef, veal, or poultry [2]. Due to the benefits of eating rabbit meat, efforts continue to improve its quality by using more and more new nutritional components in their diet. Attempts are being made to increase the level of nutrients that have a beneficial effect on the human body and to eliminate those causing negative effects [3,4,5].
There have been many publications on the use of herbs and spices (i.e., nettle and fenugreek) in rabbit nutrition and their effect on growth, health, and meat quality [6,7,8]. Nettle leaves are a source of easily digestible minerals, such as calcium (853–1050 mg/100 g dry weight), phosphorus (50–265 mg/100 g dry weight), iron (2–200 mg/100 g dry weight), sulfur (400 mg/100 g DM), potassium (532–613 mg/100 g DM), and sodium (16–58 mg/100 g DM). In addition, they contain vitamin C (20–60 mg/100 g dry weight), vitamin K (0.16–0.64 mg/100 g dry weight), and B vitamins [9,10]. The high content of chlorophyll (0.6–1% DM) and xanthophylls (0.12% DM) is proof of the presence of large amounts of beta carotene, from which vitamin A is produced. In addition, nettle is rich in organic acids (i.e., formic, acetic, pantothenic) and inorganic (silicic) acid, as well as protoporphyrins, tannins, phytosterols, and glycokinins [10,11,12]. This herb can improve biochemical, hematological, and immunological parameters [13]. Further, nettle boasts anti-allergic properties and has a strong detoxifying effect on the body thanks to its mild diuretic and blood purifying properties [10,11,12].
Fenugreek seeds contain 45–60% carbohydrates, 20–30% proteins rich in lysine and tryptophan, 5–10% oils (lipids), pyridine alkaloids, mainly trigonelline (0.2–0.38%), choline (0.5%), flavonoids, free amino acids (4-hydroxyisoleucine (0.09%), arginine, histidine, lysine), calcium and iron, saponins (0.6–1.7%), glycosides, cholesterol and sitosterol, vitamins (A, B1, C), nicotinic acid, and 0.015% volatile oils (n-alkanes and sesquiterpenes) [14,15,16]. Fenugreek stimulates the body to produce mucus (galactomannans), which allows the removal of allergens from the respiratory system and toxins from the urinary tract, and it is useful both in the prevention and treatment of neurodegenerative diseases and metabolic diseases. Numerous studies have shown that fenugreek can also have anti-inflammatory, analgesic, and antipyretic properties [15,17].
In addition to very important macroelements—calcium (Ca), potassium (K), sodium (Na), magnesium (Mg)—and microelements—iron (Fe), nickel (Ni), zinc (Zn), manganese (Mn), copper (Cu)—herbs also contain toxic metals such as cadmium (Cd) and lead (Pb) [9,18,19]. With the current increase in the use of herbs and herbal preparations as an animal feed additive, it is very important to monitor the contaminants present in plants, i.e., heavy metals, and to study their content in animal tissues. Moreover, it must be highlighted that herb addition may also cause problems in the digestive system and intestine. The toxicity of heavy metals, whether essential or not, depends on several factors including the dose in feed (food), a route of exposure, and sex [20,21]. Hence, it seems advisable to determine the effect of nettle leaves and fenugreek seeds in the feed on the content of selected heavy metals in the liver and meat of the rabbit, and determine differences in sex in metal accumulation.

2. Materials and Methods

2.1. The Animals

The experiment was conducted at the University of Agriculture in Krakow (Poland) in the Experimental Station of the Department of Genetics, Animal Breeding and Ethology. The research material consisted of Termond White rabbits. Until weaning (on the 35th day of life), young rabbits with does were housed in wooden cages. From weaning until the 84th day of life, rabbits were kept in wire metal cages (2 rabbits per cage). The experiment was conducted in a hall equipped with a lighting installation (14 L:10 D), a water trough installation, and a forced ventilation system. In the experiment, we used 10 does and from each litter, one female and one male were randomly assigned to each group. Three experimental groups were created. The control group (n = 20; 10♂ and 10♀) was fed ad libitum with a complete feed. The mixture for this group is presented in Table 1. The animals from the group N (n = 20; 10♂and 10♀) were fed a complete mixture with 1% added nettle leaves. The rabbits from the group F (n = 20; 10♂and 10♀) were fed with a complete mixture with 1% added fenugreek seeds. The experiment lasted 7 weeks (from the 35th to the 84th day of the rabbits’ lives). The nettle leaves (crude protein: 28%, crude fat: 3.3%, crude fiber: 26%) and fenugreek seeds (crude protein: 28.5%, crude fat: 6.5%, crude fiber: 10.2%) were bought from a feed manufacturer, FHP Barbara Ltd. (Poland). These additives were mashed, mixed with all ingredients, and then pelleted. The metal content of these herbs is presented in Table 2.

2.2. The Slaughter

All rabbits were slaughtered on the 84th day of age, with an average body weight of 2546 ± 47 g, after 24 h fasting with the access to water. The processes of slaughter were conducted using the methods described by Blasco et al. [22]. Liver samples were taken during the slaughter. Then, the carcasses were cooled for 24 h at 4 °C, and after that time, a sample from the right loin (m. longissimus lumborum) of each carcass was taken. The experiment was conducted under a permit from the Local Ethics Commission (agreement no 267/2018).

2.3. Determining the Concentration of Metals

Samples of meat and liver of rabbits as well as nettle and fenugreek weighing about 5 g were placed in test tubes. They were then pre-mineralized with 10 mL of a mixture of perchloric acid (70% HClO4) and nitric acid (65% HNO3) in a ratio of 1:3 for about 24 h. The samples were then subjected to thermal mineralization with the Velp 20/26 mineralizer, gradually increasing the temperature from 100 °C to 180 °C for 6–7 h. The resulting clear liquid was then diluted to 10 mL with deionized water. The concentration of metals (Zn, Cu, Ni, Mn, Fe, Pb, Cd) was determined by the atomic absorption spectrometry (AAS apparatus Unicam 929 spectrometer) [23]. The results were read on the standard curve using the standards based on the atomic absorption standards developed at the Weights and Measures Office in Warsaw. Results are shown in milligrams per kilogram of wet weight (w.w.) for muscles and liver, and dry weight (d.w.) for herbs.

2.4. Statistical Analysis

The statistical analysis was performed using the SAS package [24]. Statistically significant differences between the means were tested using Tukey–Kramer test at the significance level of p < 0.05.
The following linear model was used:
Yijk = µ + DIi + SEXj + (DI × SEX)ij + εijk
where:
  • Yijk—analyzed traits,
  • μ—overall mean,
  • DIi—effect of i-th diet (i = 1, 2, 3),
  • SEXj—effect of j-th sex (j = 1, 2),
  • (DI × SEX)ij—effect of interaction between diet and gender,
  • εijk—residual effect.
Pearson’s phenotypic correlation coefficients were determined using PROC CORR.

3. Results

A statistically significant decrease in the tested heavy metals content was found in the liver of rabbits fed with nettle leaves and fenugreek seeds in comparison with the control group (p < 0.05) (Table 3). Fe, Zn, Cu, and Mn showed the highest levels of accumulation in the rabbits’ liver fed with fenugreek (70.34 mg/kg, 32.55 mg/kg, 4.27 mg/kg, and 1.96 mg/kg, respectively) compared to rabbits fed with nettle (49.70 mg/kg, 24.19 mg/kg, 3.40 mg/kg, and 1.39 kg/kg, respectively) (p < 0.05) (Table 3). The order of essential metals in meat according to their concentrations was: Zn > Fe > Cu > Ni > Mn (Table 4). In addition, no statistically significant differences were discovered between the content of the examined metals in the meat of rabbits that were fed with nettle leaves and those fed with fenugreek seeds, except for Zn (p > 0.05) (Table 4).
The rabbits’ liver contained higher properties of all the examined elements in comparison with their meat (p < 0.05) (Table 3 and Table 4).
The analysis of lead content in the meat and liver of the studied rabbit population in all groups showed properties below the sensitivity of the method (Table 3 and Table 4).
In the case of cadmium, in the present study, its content in the meat was also below the sensitivity of the method, while in the liver, the content of this element ranged from 0.02 to 0.17 mg/kg (Table 3 and Table 4). The highest amount of cadmium was recorded in the liver of rabbits fed with fodder containing nettle (0.17 mg/kg). The analysis showed significant differences in the cadmium content in the liver among the groups: the one fed with nettle (0.17 mg/kg), the one fed with fenugreek (0.02 mg/kg), and the control group (0.03 mg/kg) (p < 0.05) (Table 3).
The phenotypic correlation coefficients among metals in the liver and meat are presented in Table 5. Zinc in the liver was positively correlated with copper (rp = 0.36), iron (rp = 0.76), and manganese (rp = 0.61) in the liver and zinc (rp = 0.54), copper (rp = 0.66), iron (rp = 0.36), and manganese (rp = 0.57) in the meat (p < 0.05). This metal was negatively correlated with nickel and cadmium in the liver and nickel in the meat (respectively: −0.73, −0.44, and −0.44) (p < 0.05). Moreover, a positive correlation was found among copper and manganese in the liver (rp = 0.46) (p < 0.05). Correlations among copper in the liver and cadmium in the liver and manganese in the meat were negative (respectively: −0.32 and −0.28) (p < 0.05). Nickel in the liver was negatively correlated with iron and manganese in the liver (respectively: −0.65 and −0.65) and zinc, copper, iron, and manganese in the meat (respectively: −0.46, −0.52, −0.39, and −0.49) (p < 0.05). This metal was positively correlated with cadmium in the liver (rp = 0.39) and nickel in the meat (rp = 0.40) (p < 0.05). Positive correlations were noticed among iron and manganese in the liver (rp = 0.46) and zinc, copper, iron, and manganese in the meat (respectively: 0.39, 0.63, 0.35, and 0.54) (p < 0.05). Iron in the liver was negatively correlated with cadmium in the liver and nickel in the meat (respectively: −0.34 and −0.39) (p < 0.05). Manganese in the liver was significantly and negatively correlated with cadmium in the liver and nickel in the meat (respectively: −0.30 and −0.40) and positively correlated with zinc, copper, and manganese in the meat (respectively: 0.51, 0.39, and 0.26) (p < 0.05). Cadmium in the liver was significantly and negatively correlated with zinc in the meat (rp = −0.31) (p < 0.05). Moreover, a positive correlation was found among zinc and copper in the meat (rp = 0.38) (p < 0.05). Copper in the meat was significantly and negatively correlated with nickel in the meat (rp = −0.36) and positively correlated with iron and manganese in the meat (respectively: 0.48 and 0.79) (p < 0.05). Manganese in the meat was significantly and negatively correlated with nickel in the meat and positively correlated with iron in the meat (respectively: −0.41 and 0.57) (p < 0.05) (Table 5).
The phenotypic correlation coefficients among metals in the nettle and liver and rabbit meat are presented in Table 6. Zinc in the nettle was positively correlated with the cadmium in the liver (rp = 0.68) and negatively correlated with iron in the meat (rp = −0.30) (p < 0.05). Positive correlations were found among copper in the nettle and manganese (rp = 0.37) and cadmium (rp = 0.44) in the liver (p < 0.05). A correlation among copper in nettle and manganese in the meat was negative (rp = −0.40) (p < 0.05). Nickel in the nettle was positively correlated with manganese and cadmium in the liver and copper in the meat (respectively: 0.27, 0.52, and 0.27) (p < 0.05). This metal was negatively correlated with manganese in the meat (rp = −0.28) (p < 0.05). Positive correlations were found among iron in the nettle and cadmium in the liver (rp = 0.63) and manganese in the meat (rp = 0.38) (p < 0.05). Manganese in the nettle was significantly and positively correlated with iron in the liver and zinc in the meat (respectively: 0.38 and 0.29) (p < 0.05). Cadmium in the nettle was significantly and negatively correlated with manganese and cadmium in the liver (respectively: −0.40 and −0.27) (p < 0.05) (Table 6).
The phenotypic correlation coefficients among metals in the fenugreek and liver and rabbit meat are presented in Table 7. Zinc in the fenugreek was positively correlated with the iron in the liver (rp = 0.28) (p < 0.05). Positive correlations were found among copper in the fenugreek and zinc in the liver (rp = 0.31) and in the meat (rp = 0.28) (p < 0.05). A correlation among copper in the fenugreek and cadmium in the liver was negative (rp = −0.32) (p < 0.05). Nickel in the fenugreek was positively correlated with nickel in the liver (rp = 0.29) (p < 0.05). Manganese in the fenugreek was significantly and positively correlated with zinc in the liver and in the meat (respectively: 0.47 and 0.28) (p < 0.05). Cadmium in the fenugreek was significantly and positively correlated with nickel in the liver (rp = 0.28) (p < 0.05) (Table 7).
In this study, the content of elements with respect to the rabbit’s sex was also analyzed. Male livers had a significantly higher content of copper and manganese (3.95 mg/kg and 1.88 mg/kg, respectively) compared to female livers (3.60 mg/kg and 1.63 mg/kg, respectively) (p < 0.05). There were no statistically significant differences in the content of other tested elements (p > 0.05) (Table 8).

4. Discussion

In the literature on herbal additives in rabbit feed, there is little information about enriching the feed with herbal additives, such as on the content of selected elements in rabbit tissues.
The study indicated that nettle leaves and fenugreek seeds were a good source of essential metals that are useful for the animal body. The metal contents in the fenugreek seeds and nettle leaves were found in the following decreasing order: Fe > Zn > Mn > Cu > Ni. In this study, nettle was the most abundant source of metals. The trace element with the highest concentration in nettle leaves was iron (380.80 mg/kg). Other authors have also confirmed the high concentration of this element in nettle [9,25]. Unfortunately, herbs can also contain toxic substances such as heavy metals such as lead or cadmium. However, Cd was found in nettle leaves and fenugreek seeds at a concentration of 2.29 mg/kg d.w and 0.48 mg/kg, respectively. The presented findings are similar to the results reported by Hagos and Chandravanshi [18] and Raimova et al. [26]. Based on the statistical analysis, the authors noticed differences in the content of heavy metals between the liver and muscles depending on the feed additive. The essential metal contents in the liver of rabbits fed with nettle and fenugreek was found in the following descending order: Fe > Zn > Cu > Mn > Ni, whereas the order of essential metals in meat according to their concentrations was Zn > Fe > Cu > Ni > Mn. In addition, no differences were found between the content of the examined metals in the meat of rabbits fed with nettle leaves and fenugreek seeds, except for Zn.
The recommended daily consumption of metals such as zinc, copper, iron, manganese, and nickel in an adult human is 12.7 mg/day, 1.6 mg/day, 6 mg/day, 3 mg/day, and 150 μg/day, respectively [27,28,29,30,31]. The consumption of rabbits in the world depends on the culinary traditions of countries. Overall, the consumption of rabbit meat in the EU is 0.5 kg per person a year. Taking into account the average content of these micronutrients in the meat of the tested rabbits, the average annual consumption in the EU and the absorption from food on the level of about a few percent may suggest that their content does not pose a risk to the health of the consumer.
According to our research, the liver contained higher values of all the examined elements in comparison with the meat. These results are consistent with the studies of Cygan-Szczegielniak et al. [32] and Kalafova et al. [33]. A liver is the primary target organ for heavy metals principally because it serves as a store for metals, redistribution, and detoxification. Therefore, a liver is regarded as a more sensitive indicator of environmental pollution than other tissues [34].
In studies on the contamination of food of animal origin, it was found that in the group of toxic metals (mercury, arsenic, lead, and cadmium), cadmium and lead are more harmful, taking into account both a number of exceedances in the permissible content and the scale of the associated risks [35,36,37]. A liver and, to a lesser extent, muscles, apart from micronutrients, also accumulate heavy metals, i.e., lead and cadmium [35,36].
In the applicable legal regulations (European Commission Regulation [38,39]), the permissible cadmium content in the meat of slaughtered animals was set at 0.05 mg/kg, and lead at 0.10 mg/kg. The maximum content of both of these elements in the liver was determined at 0.50 mg/kg.
The analysis of lead content in the meat and a liver of the studied rabbit population in all groups showed properties below the sensitivity of the method. None of the obtained results exceeded the limit value for lead (European Commission Regulation [38]). The obtained results were much lower than the properties obtained by Szkoda et al. [37] for the meat of rabbits from Poland, where the average value of lead in the meat was 0.03 mg/kg (w.w) and 0.17 mg/kg (w.w) in the liver.
Cadmium in the meat and the liver did not exceed the limits in force in the European Union (European Commission Regulation [39]). The concentrations of toxic metals, i.e., Pb and Cd in the liver and meat, were low enough to assume that meat consumption is not a threat to human health.
There are various interactions between metals in a living organism [40,41]. Numerous studies indicate interactions between cadmium and other elements (Cu, Zn, Fe). These occur during their absorption, distribution, and excretion in the body, and on the level of their biological functions in cells [41,42]. There were many studies on the interaction of Cd with Zn, Cu, and Fe, which showed Cd to be poisonous and to affect the homeostasis of these metals, mainly by causing their secondary deficiency [41,43]. Our own research also showed a decrease in microelements, i.e., Zn, Cu, Fe, and Mn, in the liver of the group fed with fodder containing nettle, in which cadmium content was the highest. Moreover, the livers of rabbits fed with nettle had the highest cadmium concentration. This was confirmed by the analysis of interactions between metals, showing a negative correlation between the content of Cd and Zn, Cu, Fe, and Mn in the liver. Similar results were obtained by other authors investigating various animal species [44,45]. An association between Cd and Ni has been faintly described and its exact mechanisms are not well understood. In the liver of rabbits fed with nettle, Ni concentrations increased compared to other groups. In the case of nickel, in contrast to other micronutrients, a positive correlation was observed between its level and the level of Cd in the liver.
The interaction between cadmium and zinc, copper, or iron results from their affinity for metallothionein, and their ability to synthesize this protein in the liver [46,47]. Elements such as zinc and copper protect cells against the toxic effects of cadmium [48]. The protective function is to reduce the accumulation of cadmium and iron inside the cells. The reduction in the content of this metal in cells is due to the antagonism among copper, iron, zinc, and cadmium in cellular transport. Moreover, zinc protects cells induced by cadmium and iron against apoptosis [48,49].
In the literature, there is no information on the correlation among the metals contained in nettle and fenugreek and the content of metals in rabbit tissues. Analyzing the correlations between the concentration of the examined metals in the tissues and their content in herbs obtained in this study, a positive relationship was shown in most cases. Positive correlations were found among Zn, Cu, Ni, and Fe in the nettle and Cd in the liver. In the case of fenugreek, this relationship was observed among Cu, Mn, and Zn in the liver and the meat.
In this study, the content of elements in respect to rabbit gender was also analyzed. Based on the statistical analysis, differences were found in the content of two elements in the liver of female versus male rabbits. Sikora et al. [50] found that the content of copper in female livers was higher than in male livers (5.10 mg/kg and 4.79 mg/kg, respectively). In our research, no statistically significant differences were found in the content of the examined metals in the meat of male and female loin. Sikora et al. [44] found no significant differences between the content of copper and manganese in the muscles of males and females; however, they noted differences in the content of iron (11.93 mg/kg and 17.21 mg/kg, respectively). Similarly, studies by Hermoso de Mendoza García et al. [20] and Bortey-Sam et al. [51] indicated that sex could represent an important source of variation in the bioaccumulation of metals in animals.
The purpose of our work was to investigate whether heavy metals contained in popular and easily available plant additives such as nettle and fenugreek accumulate in rabbit tissues. Our results are the first in the field and will allow us to plan further research on the mechanism of heavy metals in rabbit tissues, including antioxidant enzyme activity and histopathology analysis of tissues. The mechanisms and pathways of toxic effects of heavy metals, mainly cadmium and lead, at the cell and tissue level are not fully understood in biological systems, including rabbits. The results obtained by some authors clearly show that heavy metal toxicity induces a state of oxidative stress reflected in reduced O2 consumption at the tissue level in the liver and kidneys. In addition, Cd and Pb induce oxidative stress by reducing the activity of antioxidant enzymes due to changes in gene expression mechanisms and exposure of the living organism to these metals stimulates damage to kidney and liver tissues caused by lipid peroxidation. The disruption of a cellular oxidoreductive balance can lead to serious damage, both on the level of tissues and organs, leading to an impaired function [52,53].

5. Conclusions

This experiment helps to explain the interaction between the heavy metal content of nettle and fenugreek and their content in rabbit meat and liver. The meat (m. longissimus lumborum) and liver of rabbits fed with herbal feed contained fewer tested metals than in animals fed with the feed without additives. Concentrations of toxic metals, i.e., Pb and Cd in liver and meat, were so low that meat consumption does not pose a threat to human health. However, more research is needed to determine how the mechanisms and pathways of heavy metal toxicity act on tissue in which these metals are accumulated.

Author Contributions

Conceptualization, S.E.P.; methodology, S.E.P.; formal analysis, S.E.P.; investigation, S.E.P., Ł.M., M.K. and E.D.-K.; resources, S.E.P. and E.D.-K.; writing—original draft preparation, S.E.P.; writing—review and editing, Ł.M., M.K. and E.D.-K.; visualization, Ł.M. All authors have read and agreed to the published version of the manuscript.

Funding

The research was financed by the Ministry of Science and Higher Education of the Republic of Poland—SUB.215-D201 and National Centre for Research and Development (Poland) decision number LIDER/27/0104/L-9/17/NCBR/2018.

Institutional Review Board Statement

Experiment was conducted as a part of project the National Centre for Research and Development (Poland) decision number LIDER/27/0104/L-9/17/NCBR/2018 “Increasing of meat rabbits technology efficiency by development of new way of selection” under a permit from the Local Ethics Commission (agreement no 267/2018).

Informed Consent Statement

Not applicable.

Data Availability Statement

Data and statistical analysis are available upon request from the corresponding author.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Lombardi-Boccia, G.; Lanzi, S.; Aguzzi, A. Aspects of meat quality: Trace elements and B vitamins in raw and cooked meats. J. Food Compos. Analysis 2005, 18, 39–46. [Google Scholar] [CrossRef]
  2. Dalle Zotte, A. Avantage diététiques. Le lapin doit apprivoiser le consommateur. Viandes Prod. Carnés 2004, 23, 1–7. [Google Scholar]
  3. Dokoupilova, A.; Marounek, M.; Skrivanova, V.; Brezina, P. Selenium content in tissues and meat quality in rabbits fed selenium yeast. Czech J. Anim. Sci. 2007, 52, 165–169. [Google Scholar] [CrossRef] [Green Version]
  4. Kowalska, D.; Bielański, P.; Chełmińska, A. Effect of linseed & fish oil supplements in feed on fatty acid profile and intramuscular fat oxidation in rabbits. Żywność Nauka Technol. Jakość 2011, 2, 148–159. [Google Scholar]
  5. Wei Liu, H.; Gai, F.; Gasco, L.; Brugiapaglia, A.; Lussiana, C.; Guo, K.J.; Tong, J.M.; Zoccarato, I. Effects of chestnut tannins on carcass characteristics, meat quality, lipid oxidation and fatty acid composition of rabbits. Meat Sci. 2009, 83, 678–683. [Google Scholar] [CrossRef] [PubMed]
  6. Ayala, L.; Silvana, N.; Zoccarato, I.; Gomez, S. Use of vulgar oregano (Origanum vulgare) as phytobiotic in fatting rabbits. Cuba J. Agric. Sci. 2011, 45, 159–161. [Google Scholar]
  7. Dalle Zotte, A.; Celia, C.; Szendrő, Z.s. Herbs and spices inclusion as feedstuff or additive in growing rabbit diets and as additive in rabbit meat: A review. Livest. Sci. 2016, 189, 82–90. [Google Scholar] [CrossRef]
  8. Frankič, T.; Volič, M.; Salobir, J.; Rezar, V. Use of herbs and spice and their extracts in animals nutrition. Acta Agric. Slov. 2009, 94, 95–102. [Google Scholar]
  9. Dimitrijević, V.D.; Krstić, N.S.; Stanković, M.N.; Arsić, I. Biometal and heavy metal content in the soil-nettle (Urtica dioica L.) system from different localities in Serbia. Adv. Technol. 2016, 5, 17–22. [Google Scholar] [CrossRef]
  10. Jan, K.N.; Zarafshan, K.; Singh, S. Stinging nettle (Urtica dioica L.): A reservoir of nutrition and bioactive components with great functional potential. Food Meas. 2017, 11, 423–433. [Google Scholar] [CrossRef]
  11. Rafajlovska, V.; Rizova, V.; Djarmati, Z.; Tesevic, V.; Cvetkov, L. Contents of fatty acid in stinging nettle extracts (Urtica dioica L.) obtained with supercritical carbon dioxide. Acta Pharm. 2001, 51, 45–51. [Google Scholar]
  12. Upton, R. Stinging nettles leaf (Urtica dioica L.): Extraordinary vegetable medicine. J. Herb. Med. 2013, 3, 9–38. [Google Scholar] [CrossRef]
  13. Herrera, S.B.; Leonor Rodriguez, L.; García, M.C.; Flores, J.L.; Velasco, R. Effects of extract of Urtica dioica L. (stinging nettle) on the immune response of rats with severe malnutrition. J. Complement. Med. Res. 2018, 9, 63–73. [Google Scholar] [CrossRef]
  14. Król-Kogus, B.; Krauze-Baranowska, M. Fenugreek (Trigonella foenum-graecum L.)—traditional herb on the background of the research studies. Post. Fitoter. 2011, 3, 185–190. [Google Scholar]
  15. Hossain, M.M.; Begum, M.; Kim, I.H. Effects of fenugreek (Trigonella foenum-graecum L.) seed extract supplementation in different energy density diets on growth performance. nutrient digestibility. blood characteristics. fecal microbiota. and fecal gas emission in growing pigs. Can. J. Anim. Sci. 2018, 98, 289–298. [Google Scholar] [CrossRef] [Green Version]
  16. Moradi Kor, N.; Bagher Didarshetaban, M.; Pour, H.R.S. Fenugreek (Trigonella foenum-graecum L.) as a valuable medicinal plant. Int. J. Adv. Biol. Biom. Res. 2013, 1, 922–931. [Google Scholar]
  17. Wani, S.A.; Kumar, P. Fenugreek: A review on its nutraceutical properties and utilization in various food products. J. Saudi Soc. Agric. Sci. 2018, 17, 97–106. [Google Scholar] [CrossRef] [Green Version]
  18. Hagos, M.; Chandravanshi, B.S. Levels of essential and toxic metals in fenugreek seeds (Trigonella Foenum-Graecum L.) cultivated in different parts of Ethiopia. Braz. J. Food Technol. 2016, 19, e2015059. [Google Scholar] [CrossRef] [Green Version]
  19. Winiarska-Mieczana, A.; Kwiecień, M.; Kwiatkowska, K. Lead and cadmium content in herbal teas. Probl. Hig. Epidemiol. 2011, 92, 667–670. [Google Scholar]
  20. Hermoso de Mendoza García, M.; Hernández Moreno, D.; Soler Rodríguez, F.; López Beceiro, A.; Fidalgo Alvarez, L.E.; Pérez López, M. Sex- and age-dependent accumulation of heavy metals (Cd, Pb and Zn) in liver, kidney and muscle of roe deer (Capreolus capreolus) from NW Spain. J. Environ. Sci. Health A Tox. Hazard Subst. Environ. Eng. 2011, 46, 109–162. [Google Scholar] [CrossRef]
  21. Hejna, M.; Gottardo, D.; Baldi, A.; Dell’Orto, V.; Cheli, F.; Zaninelli, M.; Rossi, L. Review: Nutritional ecology of heavy metals. Animal 2018, 12, 2156–2170. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  22. Blasco, A.; Ouhayoun, J.; Masoero, G. Harmonization of criteria and terminology in rabbit meat research. World Rabbit Sci. 1993, 1, 3–10. [Google Scholar] [CrossRef]
  23. Agemian, H.; Sturtevant, D.P.; Austen, K.D. Simultaneous acid extraction of six trace metals from fish tissue by hot-block digestion and determination by atomic-absorption spectrometry. Analyst 1980, 105, 125–130. [Google Scholar] [CrossRef] [PubMed]
  24. SAS Institute INC. The SAS System for Windows, Version 9.4; SAS Institute INC: Cary, NC, USA, 2014. [Google Scholar]
  25. Adhikari, B.M.; Bajracharya, A.; Shrestha, A.K. Comparison of nutritional properties of Stinging nettle (Urtica dioica) flour with wheat and barley flours. Food Sci. Nutr. 2016, 4, 119–124. [Google Scholar] [CrossRef]
  26. Raimova, K.V.; Abdulladjanova, N.G.; Kurbanova, M.A.; Makhmanov, D.M.; Kadirova, S.O.; Tashpulatov, F.N.; Juraev, S.S.; Matchanov, A.D.; Rakhimov, R.N. Comprehensive study of the chemical composition of Urtica dioica L. J. Crit. Rev. 2020, 7, 750–755. [Google Scholar]
  27. EFSA. Scientific Opinion on Dietary Reference Values for manganese. EFSA J. 2013, 11, 3419. [Google Scholar]
  28. EFSA. Scientific Opinion on Dietary Reference Values for zinc. EFSA J. 2014, 12, 3844. [Google Scholar] [CrossRef] [Green Version]
  29. EFSA. Scientific Opinion on Dietary Reference Values for copper. EFSA J. 2015, 13, 4253. [Google Scholar] [CrossRef]
  30. EFSA. Scientific Opinion on Dietary Reference Values for iron. EFSA J. 2015, 13, 4254. [Google Scholar] [CrossRef]
  31. EFSA. Scientific Opinion on Dietary Reference Values for nickel. EFSA J. 2015, 13, 4002. [Google Scholar]
  32. Cygan-Szczegielniak, D.; Stasiak, K.; Janicki, B.; Buczkowska, J. Impact of food type on the content of minerals in rabbit meat and liver. Med. Water. 2012, 68, 422–425. [Google Scholar]
  33. Kalafova, A.; Kovacik, J.; Capcarova, M.; Kolesarova, A.; Lukac, N.; Stawarz, R.; Formicki, G.; Laciak, T. Accumulation of zinc, nickel, lead and cadmium in some organs of rabbits after dietary nickel and zinc inclusion. J. Environ. Sci. Health A Tox. Hazard. Subst. Environ. Eng. 2012, 47, 1234–1238. [Google Scholar] [CrossRef]
  34. Hedayati, A. Liver as a Target Organ for Eco-Toxicological Studies. J. Coast. Zone Manag. 2016, 19, e118. [Google Scholar] [CrossRef] [Green Version]
  35. Damerau, A.; Venäläinen, E.R.; Peltonen, K. Heavy metals in meat of Finnish city rabbits. E3S Web Conf. 2016, 1, 15011. [Google Scholar] [CrossRef] [Green Version]
  36. Omoyakhi, J.M.; Edo-Taiwo, O.; Aleke, J.I.; John, T.J. Distribution of some heavy metals in the tissues of arm, thigh, kidney and liver after continuous feeding of rabbits with diet contaminated with crude oil. J. Adv. Biol. Biotechnol. 2017, 16, 1–8. [Google Scholar] [CrossRef]
  37. Szkoda, J.; Nawrocka, A.; Kmiecik, M.; Żmudzki, J. Monitoring study of toxic elements in food of animal origin. Ochr. Śr. Zasobów Nat. 2011, 48, 475–484. [Google Scholar]
  38. European Commission. Regulation no. 1881/2006 of 19 December 2006 setting maximum levels for certain contaminants in foodstuffs. Off. J. Eur. Union 2006, L634, 5–24. [Google Scholar]
  39. European Commission. Regulation no. 488/2014 of 12 May 2014 amending Regulation (EC) No 1881/2006 as regards maximum levels of cadmium in foodstuffs. Off. J. Eur. Union 2006, L138, 75–79. [Google Scholar]
  40. Piontek, M.; Fedyczak, Z.; Łuszczyńska, K.; Lechów, H. Toxicity of some trace metal. Uniwersytet Zieleniogórski Zesz. Nauk 2014, 155, 70–85. [Google Scholar]
  41. Bulat, Z.; Dukić-Ćosić, D.; Antonijević, B.; Buha, A.; Bulat, P.; Pavlović, Z.; Matović, V. Can zinc supplementation ameliorate cadmium-induced alterations in the bioelement content in rabbits? Arh. Hig. Rada Toksikol. 2017, 68, 38–45. [Google Scholar] [CrossRef] [Green Version]
  42. Skibniewski, M.; Skibniewska, E.M.; Kośla, T.; Olbrych, K. Relationship between Cd and Zn concentration in the kidneys, liver, and muscles of moose (Alces alces) from north-eastern Poland. Environ. Sci. Pollut. Res. 2017, 24, 598–604. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  43. Andjelkovic, M.; Djordjevic, A.B.; Antonijevic, E.; Antonijevic, B.; Stanic, M.; Kotur-Stevuljevic, J.; Spasojevic-Kalimanovska, V.; Jovanovic, M.; Boricic, N.; Wallace, D.; et al. Toxic Effect of Acute Cadmium and Lead Exposure in Rat Blood, Liver, and Kidney. Int. J. Environ. Res. Public Health 2019, 16, 274. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  44. Erdem, O.; Yazihan, N.; Kocak, M.K.; Sayal, A.; Akcil, E. Influence of chronic cadmiumexposure on the tissue distributionof copper and zinc and oxidativestress parameters in rats. Toxicol. Ind. Health 2015, 32, 1505–1514. [Google Scholar] [CrossRef] [PubMed]
  45. Lane, E.A.; Canty, M.J.; More, S.J. Cadmium exposure and consequence for the health and productivity of farmed ruminants. Res. Vet. Sci. 2015, 101, 132–139. [Google Scholar] [CrossRef]
  46. Isani, G.; Carpenè, E. Metallothioneins, Unconventional Proteins from Unconventional Animals: A Long Journey from Nematodes to Mammals. Biomolecules 2014, 4, 435–457. [Google Scholar] [CrossRef] [Green Version]
  47. Zhang, C.C.; Volkmann, M.; Tuma, S.; Stremmel, W.; Merle, U. Metallothionein is elevated in liver and duodenumof Atp7b(2/2)mice. Biometals 2018, 31, 617–625. [Google Scholar] [CrossRef] [Green Version]
  48. Genchi, G.; Sinicropi, M.S.; Lauria, G.; Carocci, A.; Catalano, A. The Effects of Cadmium Toxicity. Int. J. Environ. Res. Public Health 2020, 17, 3782. [Google Scholar] [CrossRef]
  49. Czeczot, H.; Majewska, M. Cadmium—exposure and its effects on health. Farm. Pol. 2010, 66, 243–250. [Google Scholar]
  50. Sikora, T.; Kruk, D.; Serwin, K. Zawartość niektórych pierwiastków w mięsie i wątrobie królików wybranych ras. Żywność Technol. Jakość 1996, 1, 13–22. [Google Scholar]
  51. Bortey-Sam, N.; Nakayama, S.M.M.; Ikenaka, Y.; Akoto, O.; Baidoo, E.; Mizukawa, H.; Ishizuka, M. Heavy metals and metalloid accumulation in livers and kidneys of wild rats around gold-mining communities in Tarkwa, Ghana. J. Environ. Chem. Ecotoxicol. 2016, 7, 58–68. [Google Scholar]
  52. Assi, M.A.; Hezmee, M.N.M.; Haron, A.W.; Sabri, M.Y.; Rajion, M.A. The detrimental effects of lead on human and animal health. Vet. World 2016, 9, 660–671. [Google Scholar] [CrossRef]
  53. Poli, V.; Madduru, R.; Aparna, Y.; Kandukuri, V.; Motireddy, S.R. Amelioration of Cadmium-Induced Oxidative Damage in Wistar Rats by Vitamin C, Zinc and N-Acetylcysteine. Med. Sci. 2022, 10, 7. [Google Scholar] [CrossRef]
Table
Table 1. Ingredients and chemical composition of the control and experimental feed (according to feed manufacturer FHP Barbara Ltd.).
Table 1. Ingredients and chemical composition of the control and experimental feed (according to feed manufacturer FHP Barbara Ltd.).
ComponentsC1N2F3
Ingredients (% per kg)
Dicalcium phosphate0.620.620.62
Calcium carbonate0.800.800.80
Corn24.5024.5024.50
Bran15.0015.0015.00
Wheat29.5828.5828.58
Dried alfalfa10.0010.0010.00
Soybean meal7.007.007.00
Sunflower meal11.0011.0011.00
Vitamin-mineral premix1.501.501.50
Nettle leaves010
Fenugreek seeds001
Chemical composition (% per kg)
Crude protein16.4016.5516.50
Crude fiber9.229.129.15
Crude fat2.702.752.80
Crude ash4.844.934.87
Lysine0.660.660.68
Methionine0.290.290.30
Calcium0.770.770.77
Sodium0.240.240.24
Phosphorus0.630.630.63
Metabolic energy (MJ/kg)10.1110.1610.19
C1—control group, N2—diet with nettle leaves, F3—diet with fenugreek seeds.
Table
Table 2. The content of heavy metal in nettle and fenugreek in mg/kg (d.w.).
Table 2. The content of heavy metal in nettle and fenugreek in mg/kg (d.w.).
Heavy MetalN1F2
Zn25.80 ± 3.1024.48 ± 2.18
Cu3.85 ± 0.094.45 ± 0.13
Ni0.57 ± 0.220.26 ± 0.56
Fe380.8 ± 47.6754.74 ± 1.86
Mn23.05 ± 0.559.14 ± 0.86
Cd2.29 ± 0.0630.48 ± 0.057
Pbu.l.d.u.l.d.
d.w.—dry weight; u.l.d.—under the limit of detection; N1—diet with nettle leaves, F2—diet with fenugreek seeds.
Table
Table 3. The effect of diet on the content of selected heavy metals in rabbit liver in mg/kg (w.w.).
Table 3. The effect of diet on the content of selected heavy metals in rabbit liver in mg/kg (w.w.).
Heavy MetalC (n = 20) 1N (n = 20) 2F (n = 20) 3
Zn37.34 a ± 2.54 424.19 b ± 3.1832.55 c ± 2.55
Cu3.65 a ± 0.263.40 a ± 0.474.27 b ± 0.46
Ni0.04 a ± 0.010.11 b ± 0.030.06 c ± 0.01
Fe82.99 a ± 10.7849.70 b ± 7.8870.34 c ± 15.26
Mn1.93 a ± 0.211.39 b ± 0.321.96 a ± 0.27
Cd0.03 a ± 0.010.17 b ± 0.230.02 a ± 0.01
Pbu.l.d.u.l.d.u.l.d.
w.w.—wet weight; u.l.d.—under the limit of detection; 1—control group, 2—diet with nettle leaves, 3—diet with fenugreek seeds; 4—results are presented as mean ± SD. a,b,c—means in rows with different letters are significantly different (p ≤ 0.05).
Table
Table 4. The effect of diet on the content of selected heavy metals in rabbit meat (m. longissimus. lumborum) in mg/kg (w.w.).
Table 4. The effect of diet on the content of selected heavy metals in rabbit meat (m. longissimus. lumborum) in mg/kg (w.w.).
Heavy MetalC (n = 20) 1N (n = 20) 2F (n = 20) 3
Zn5.62 a ± 0.48 45.02 b ± 0.345.51 a ± 0.36
Cu0.50 a ± 0.050.35 b ± 0.040.39 b ± 0.03
Ni0.22 a ± 0.040.26 b ± 0.030.24 b ± 0.03
Fe3.08 a ± 0.342.59 b ± 0.322.56 b ± 0.33
Mn0.08 ± 0.010.03 ± 0.010.02 ± 0.01
Cdu.l.d.u.l.d.u.l.d.
Pbu.l.d.u.l.d.u.l.d.
w.w.—wet weight; u.l.d.—under the limit of detection; 1—control group, 2—diet with nettle leaves, 3—diet with fenugreek seeds; 4—results are presented as mean ± SD. a,b—means in rows with different letters are significantly different (p ≤ 0.05).
Table
Table 5. Phenotypic correlations between metals in the liver and meat (m. longissimus lumborum).
Table 5. Phenotypic correlations between metals in the liver and meat (m. longissimus lumborum).
Heavy MetalZnliverCuliverNiliverFeliverMnliverCdliverZnl.l. 1Cul.l.Nil.l.Fel.l.Mnl.l.
Znliver10.36 *−0.73 *0.76 *0.61 *−0.44 *0.54 *0.66 *−0.44 *0.36 *0.57 *
Culiver 1−0.250.170.46 *−0.32 *0.12−0.06−0.14−0.15−0.28 *
Niliver 1−0.65 *−0.65 *0.39 *−0.46 *−0.52 *0.40 *−0.39 *−0.49 *
Feliver 10.46 *−0.34 *0.39 *0.63 *−0.39 *0.35 *0.54 *
Mnliver 1−0.30 *0.51 *0.39 *−0.40 *0.160.26 *
Cdliver 1−0.31 *−0.170.18−0.24−0.14
Znl.l. 10.38 *−0.150.240.25
Cul.l. 1−0.36 *0.48 *0.79 *
Nil.l. 1−0.24−0.41 *
Fel.l. 10.57 *
Mnl.l. 1
*—significant correlation (p < 0.05); 1 l.l.—m. longissimus lumborum.
Table
Table 6. The phenotypic correlation coefficients among metals in the nettle and liver and rabbit meat.
Table 6. The phenotypic correlation coefficients among metals in the nettle and liver and rabbit meat.
Heavy MetalZnliverCuliverNiliverFeliverMnliverCdliverZnl.l. 1Cul.l.Nil.l.Fel.l.Mnl.l.
Zn0.040.08−0.130.28 *−0.03−0.110.080.21−0.010.04−0.01
Cu0.31 *0.200.040.070.09−0.32 *0.28 *0.20−0.14−0.010.06
Ni−0.11−0.110.29 *−0.180.05−0.060.02−0.07−0.190.130.11
Fe−0.110.08−0.080.20−0.06−0.190.030.17−0.010.120.03
Mn0.470.230.09−0.110.20−0.190.280.03−0.17−0.140.05
Cd0.03−0.060.28−0.200.08−0.080.09−0.06−0.190.060.09
*—significant correlation (p < 0.05); 1 l.l.—m. longissimus lumborum.
Table
Table 7. The phenotypic correlation coefficients among metals in the fenugreek and liver and rabbit meat.
Table 7. The phenotypic correlation coefficients among metals in the fenugreek and liver and rabbit meat.
Heavy MetalZnliverCuliverNiliverFeliverMnliverCdliverZnl.l. 1Cul.l.Nil.l.Fel.l.Mnl.l.
Zn−0.06−0.180.020.240.070.68 *−0.190.090.19−0.30 *−0.12
Cu0.11−0.080.20−0.010.37 *0.44 *0.240.37 *0.06−0.11−0.40 *
Ni0.06−0.150.140.100.27 *0.52 *0.070.27 *0.20−0.16−0.28 *
Fe−0.03−0.06−0.100.050.040.63 *−0.140.070.01−0.090.38 *
Mn0.10−0.10−0.140.38 *−0.04−0.040.29 *0.130.120.130.13
Cd−0.090.180.070.03−0.40 *−0.27 *−0.20−0.20−0.24−0.01−0.05
*—significant correlation (p < 0.05); 1 l.l.—m. longissimus lumborum.
Table
Table 8. The content of elements in the liver and meat (m. longissimus lumborum) of females and males in mg/kg (w.w.).
Table 8. The content of elements in the liver and meat (m. longissimus lumborum) of females and males in mg/kg (w.w.).
Heavy MetalLiverMeat
♂(n = 30)♀(n = 30)♂(n = 30)♀(n = 30)
Zn32.05 ± 5.99 130.67 ± 3.455.36 ± 0.435.41 ± 0.52
Cu3.95 a ± 0.553.60 b ± 0.490.40 ± 0.060.43 ± 0.08
Ni0.07 ± 0.040.07 ± 0.030.24 ± 0.030.24 ± 0.04
Fe66.21 ± 15.8069.14 ± 20.122.77 ± 0.372.72 ± 0.44
Mn1.88 a ± 0.371.63 b ± 0.340.04 ± 0.030.05 ± 0.01
Cd0.05 ± 0.040.09 ± 0.02u.l.d.u.l.d.
Pbu.l.d.u.l.d.u.l.d.u.l.d.
w.w.—wet weight; u.l.d.—under the limit of detection; 1—results are presented as mean ± SD. a,b—means in rows with different letters are significantly different (p ≤ 0.05).
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Pałka, S.E.; Drąg-Kozak, E.; Migdał, Ł.; Kmiecik, M. Effect of a Diet Supplemented with Nettle (Urtica dioica L.) or Fenugreek (Trigonella Foenum-Graecum L.) on the Content of Selected Heavy Metals in Liver and Rabbit Meat. Animals 2022, 12, 827. https://doi.org/10.3390/ani12070827

AMA Style

Pałka SE, Drąg-Kozak E, Migdał Ł, Kmiecik M. Effect of a Diet Supplemented with Nettle (Urtica dioica L.) or Fenugreek (Trigonella Foenum-Graecum L.) on the Content of Selected Heavy Metals in Liver and Rabbit Meat. Animals. 2022; 12(7):827. https://doi.org/10.3390/ani12070827

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Pałka, Sylwia Ewa, Ewa Drąg-Kozak, Łukasz Migdał, and Michał Kmiecik. 2022. "Effect of a Diet Supplemented with Nettle (Urtica dioica L.) or Fenugreek (Trigonella Foenum-Graecum L.) on the Content of Selected Heavy Metals in Liver and Rabbit Meat" Animals 12, no. 7: 827. https://doi.org/10.3390/ani12070827

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