Skip to main content
Download PDF
Download ePub

Does supplemental zeolite (clinoptilolite) affect growth performance, meat texture, oxidative stress and production of polyunsaturated fatty acid of Turkey poults?

Lipids in Health and Disease volume 17, Article number: 177 (2018) Cite this article

Abstract

Background

Following the ban on the use of growth factors, the use of zeolite in poultry feed could be a solution to obtain healthier food products that are more demanded by the consumer.

Methods

Zeolite (Clinoptilolite) was added to turkey male and female feed at concentrations 1% or 2% and was evaluated for its effectiveness on performance of the production. The turkeys were given free and continuous access to a nutritionally non-limiting diet (in meal form) that was either a basal diet or a ‘Zeolite supplemented-diet’ (the basal diet supplemented with clinoptilolite at a level of 1% or 2%).

Results

It was found that adding zeolite in the turkey diet had a positive effect on growth performance and increased weight gain compared to the control. In addition, zeolite treatment had a positive effect on oxidative stress and organoleptic parameters that were measured. It was found that adding zeolite in the turkey diet reduced the MDA level in the liver and in the meat, as compared to the control. Quality of meat was measured as a significantly increase (p < 0.05) in pH for male meat, indicated that the zeolite could maintain the quality of longer period. The adding of zeolite in the turkey diet increased level of polyunsaturated fatty acid.

Conclusion

This study showed the significance of using zeolite, as a feed additive for turkey, as part of a comprehensive program to improve growth performance and oxidative stress parameters and to increase level of polyunsaturated fatty acid on the turkey body.

Background

Nowadays, the consumption of poultry products will be constantly increasing due to the expected evolution of the world population. For this reason, industries seek to improve production to cover this high consumption. Since the interdiction of the using of antibiotic in commercial poultry production, the use of essential oils and fed additives can improve the intake of compound foods [1,2,3,4,5,6]. Zeolites was used in wide range of agricultural applications and particularly in animal nutrition [7]. Clinoptilolite is a natural zeolite with a particular three-dimensional structure that endows it with specific physicochemical properties that include ion-exchange capacity, absorbency, size-exclusion framework, as well as catalytic properties [8, 9]. Activated and micronized zeolites are detoxifying agents because of their selective binding of heavy metals, O2, and ROS. Various studies have shown that these hydrated aluminosilicates have no toxic effects in either humans or animals [10,11,12]. Activated and micronized zeolites are used as detoxifying agents in humans. Detoxification is attributed to their ability to reduce lipid peroxidation by scavenging free radicals [13].

Mumpton & Fishman was reported that zeolites have the ability to lose or gain water reversibly and to exchange certain constituent atoms without major change of atomic structure [14]. In this context, Onogi revealed that zeolite should be used to economize on the feed and reduce the moisture content of chicken dropping [15]. Muzaffer et al. suggested that zeolites improves feed efficiency, weight gain of fatting and egg production in laying hens [16]. Moreover, Wu-Haan et al. revealed that zeolites is a beneficial feed additive that exhibits a strong preference for binding nitrogenous cations like NH4 + and NH3 emission [17]. In this context, this substance was recommended to absorb various mycotoxins [13, 18] to reduce ammonia production by pullets [17] and to remove ammonium from aqueous solutions [19], since the high atmospheric ammonia in poultry facilities might damage the respiratory tract lining, or even increased ascites and lower performance [20].

In poultry, transport conditions can influence the quality of the meat stress [21] also; the environmental or behavioral can affect reactive oxygen species (ROS). When the generation of these ROS in a system exceeds the ability of the system to neutralize and eliminate them so oxidative stress develops. Malondialdehyde (MDA) is examples of molecules that can be modified by excessive ROS in vivo and could be used as important and significant biomarkers of oxidative stress [22].

The objective of this study is so to examine the influence of natural zeolites, givens as supplement to feed turkey poults on growth performance, meat texture, oxidative stress and the fatty acid composition.

Materials and methods

Turkey management

A total number of 96 forty two- day-old turkey (BUTENA) were selected and divided randomly into three groups housed: control group and two experimental groups (1% zeolite and 2% zeolite), each consisting of 32 turkeys (16 males and 16 females).

Indeed, Feed and water was provided as ad libitum. The experiment was finished when the turkey reached the age of 90 days for females and 110 days for males.

Turkeys received the complete feed mixture BD (0%Z) from the start of the experiment until one week (an adaptation sub-period), followed by the feed mixture BD (0%Z), BD (1%Z) and BD (2%Z) from second week to the end of the experience. All feed mixtures contained the same components; the only difference was that the mixtures designed for the experimental groups (1% zeolite and 2% zeolite) were supplemented with 1 and 2% of natural clinoptilolite (commercial additive ZeoFeed from the company “ROTAMIN”, Turkey).

The basal diet or control diet was a commercial feed that contained yellow corn, soybean meal, calcium carbonate and a mineral-vitamin mixture (Table 1). The turkeys were housed in there compartments with ambient temperature of about 20 °C. Water was provided ad libitum intake throughout the trial period.

Table 1 Composition of basal diet (%) and the content of basic nutrients (g/kg)
Full size table

Data collection

All the turkeys were weighted individually weekly at the same time of day and at the same order of groups to determine the weight gain changes and average daily gain. In addition, feed consumption was measured weekly to estimate the feed conversion ratio.

Intramuscular ash and fatty acid composition

At the end of the experiment, the turkeys were slaughtered (n = 96). Thighs turkey from each groups (10/32, 5 male and 5 female) were selected and harvested at random. The muscular part was used to determine the composition of fatty acids (FA).

In preparation, samples from the 5 male and 5 female from each group were cut from all external fats and were ground by an ultra turrax homogenizer. The total lipids for the analysis of the fatty acids were extracted from alipotent samples of 1 g of the thigh according to Folch et al. [23, 24]. Fatty acid methyl esters (FAME) were prepared, and measured by gas chromatography of FAME in a Chrompack CP 900 apparatus fitted with a flame ionization detector [25]. The results were expressed as a percentage of individual fatty acids in the lipid fraction as described by Pordomingo et al. [20].

Texture meat color, drip loss and pH 24 h measurement

Texture profile analysis were done on fragments of thigh from each groups (10/32, 5 male and 5 female), stored at least for 24 h at 4 °C. Texture of samples was performed by the determination of Hardness, elasticity and chewiness were using a texturometer (Texture Analyses, TA Plus, LLOYD instruments, England) [26].

Five male and five female samples from each groups (10/32) cleared of fat and cut into a net kept at 4 °C for 24 h were used for determination of the color of meat by a colorimeter.

A section of the pectoralis muscle from five male and five female samples from each groups (10/32) was collected and weighed subsequently. The pectoralis muscle were put in a tightly sealed plastic bag and cooked in water bath at 80 °C for 10 min and the sample were reweighed and drip loss was calculated.

pH value of five male and five female samples from each groups (10/32) was measured after 24 h hours using a solid pH-meter.

Biochemical assays

Measurement of lipid peroxidation levels in meat and liver

Liver and meat homogenate was prepared from each groups (10/32, 5 male and 5 female) to test the enzymatic activity of glutathione peroxidase (GPX), total superoxide dismutase (SOD), catalase (CAT) and content of malondialdehyde (MDA).

Malondialdehyde

Lipid peroxidation (LPO) levels in the meat and the liver tissue from five male and five female samples from each groups (10/32) were measured with thiobarbituric acid (TBA) reaction [27]. This method was used to obtain a spectrophotometric measurement of the color produced during the reaction to TBA with malondialdehyde (MDA) at 535 nm.

According to Ben Slima et al. 0.25 ml of sample homogenate was mixed with 0.5 ml of loroacetic acid solution (TCA) and centrifuged at 2500 g for 10 min.0.5 ml of a solution containing 0.67% thiobarbituric acid (TBA) and 0.5 ml of supernatant were incubated for 10 min at 100 °C and cooled. Absorbance of TBA-MDA complex was measured at 532 nm. Lipid peroxidation is expressed as nmoles MDA/g tissue [28].

Determination of meat and liver enzymatic antioxidants

The meat and the liver tissue superoxide dismutase (SOD) activities were determined from five male and five female samples from each groups (10/32) by the method of Beauchamp and Fridovich [29]. The reaction mixture contained 50 mM of tissue homogenates in potassium phosphate buffer (pH = 7.4), 0.1 mM methionine, 2 μM riboflavine and 75 μM Nitro Bleu Tetrazoluim (NBT). The developed blue color reaction was measured at 560 nm. Units of SOD activity were expressed as the amount of enzyme required to inhibit the reduction of NBT by 50% and the activity was expressed as U/ mg protein.

Catalase activities were determined in the meat and the liver homogenates, as described by Aebi [30] by the decomposition of hydrogen peroxide and converts it to water and molecular oxygen.

Protein determination in meat and liver

According to Lowry et al. the total protein concentration of supernatant was determined using bovine serum albumin BSA as a standard [31].

Statistical evaluation

Data analysis was undertaken using SPSS for Windows 20.0 statistical software (SPSS Inc., Chicago, IL, USA).

All results are presented as the mean ± standard deviation (± SD). Means ± S.D. were calculated for normalizing the control as 100%. Differences among treatment and control groups were tested by one way analysis of variance (ANOVA), followed by pair-wise comparisons between group using Student test. P-value < 0.05 was considered statistically significant.

Differences at p < 0.05 were considered significant.

Results and discussion

Measurements of Turkey performance indicators

The effect of zeolite incorporation in the turkey diet on weight gain, on average daily gain and on feed conversion ratio are shown in the Table 2a for female turkey and Table 2b for male turkey. With zeolite, turkey in the experimental group was positively reflected in performance indicators. The results reveal that the average daily gain had increase significantly (p = 0.000) both for male and female turkey poults with zeolite. In addition, for male turkey, weight gain in the 2% zeolite group compared to control group was improved significantly (9.36 kg vs. 9.80 kg, p = 0.030). Nevertheless, with 1% zeolite there was no significantly different (p > 0. 05) for weight gain. Even though, the weight gain tended to be improved for female turkey when zeolite was supplemented to the diets but no significantly different (p > 0. 05). In contrary, the differences were not significant (p > 0. 05) for the feed conversion ratio for male and female.

Table 2 Effect of supplemental zeolite on growth performance of female and male turkey poults
Full size table

Feed intake was significantly increase by zeolite withe 1% or 2%, even for male and female, so the diet consumed by these two groups was significantly more than that of the control groups (Table 2a, b).

In this study and according to Shariatmadari et al., the zeolite has a positive effect on growth performance of broiler [32]. These results are consistent with those of Eleroglu et al. and Karamanlis et al. in which it indicate that zeolite added to broiler feed increased body weight and growth rate performance [33, 34]. According to Mallek et al., the average growth of broilers were significantly (p < 0.05) different between different groups; broilers that were fed on the ‘zeolite diet’ were growing to a faster rate (p < 0.05) compared with those of the control group [35]. However, suchy et al. indicate that zeolite increased the feed conversion ratio [36] which not agree with the studies of Jand et al. and Ortatatli et al. [37, 38]. This positive effect of zeolite reported by suchy et al. can be explained by the ability of zeolite to reduce the toxic effects of materials such as aflatoxins [5, 6, 36].

According to Mallek et al., the average growth of broilers were significantly (p < 0.05) different between different groups; broilers that were fed on the ‘zeolite diet’ were growing to a faster rate (p < 0.05) compared with those of the control group [35]. In addition, with 1% zeolite broilers were significantly heavier from those fed the basal diet at the age of 45 days [37].

Intramuscular fatty acid composition

In the present experiment, addition of the zeolite has not significantly (p > 0. 05) affect on the centration of saturated and poly-unsaturated fatty acids in intramuscular fat (Table 3). However, an increase of the oleic acid (C 18:1) was observed (p = 0.005) between control group and 1% Zeolite group (Table 4). However, a decreased of the percentage of palmitoleic acid C: 16:1 (p > 0. 05) was observed without reaching the significance rate. These results may be due of a reduction in Δ9 desaturase activity. This hypothesis could be confirmed by the demonstration of the decrease of mRNA expression level of the Δ9 desaturase gene using quantitative-qPCR. Juárez et al. have reported similar results. There is also a significant decrease in the percentage of the Lignoceric acid (C24:0) (p = 0.034) [39]. Mallek et al. was reported similar result about the effects of zeolite on two monounsaturated fatty acids (MUFA) [35]. Zeolite was increased the percentage of 18:1 oleic acid and however decreased 16:1 palmitoleic acid percentage, likely because of a reduction in Δ9 desaturase activity.

Table 3 Effect of supplemental zeolite on meat Fatty acids (%) of turkey poult
Full size table
Table 4 Effect of supplemental zeolite on meat Fatty acids (%) of turkey poult (test student)
Full size table

In addition zeolite reduced the level of total saturated fatty acids (SFA) in intramuscular fat but without reaching the significance rate (p > 0.05). This decrease was attributed to the reduction in 16:0 palmitic acid and in 18:0 stearic acid levels. The increase of the level of poly-unsaturated fatty acid could be the direct result of the decrease level of SFA.

It is important to note that PUFAs (Linoleic Acid) have displayed protection against lipid peroxidation increasing the levels of several cellular antioxidants [40].

Effect of zeolite addition on textural parameters of thigh muscle

The evolution of textural parameters of the thigh muscle as a function of the level of zeolite added is shown in fig. 1 for female meat and fig. 2 for male meat. The addition of 2% of zeolite was shown that chewiness increases significantly (p = 0.004 for female and p = 0.024 for male) compared to control group. In addition, elasticity was also increases significantly with 2% of zeolite, from 5.83 to 6.99 for female meat (p = 0.034) and from 5.88 to 6.75 for male meat (p = 0.022). In contrast, hardness was also increased but without reach significance. Such an evolution of textural parameters can be explained by the change in the water holding capacity. When zeolite was added, a reduction in the compactness of protein gel network allows more binding of water and makes meat tender.

Fig. 1
figure 1

Effect of zeolite addition on textural parameters of thigh muscle female. a: chewiness, b: hardness, c:elasticity

Full size image
Fig. 2
figure 2

Effect of zeolite addition on textural parameters of thigh muscle male. a: chewiness, b: hardness, c:elasticity

Full size image

The influence of the presence of natural zeolite on the gelling process of the protein may be the reason of these changes in texture. According to Mallek et al. (2012), zeolite-muscle proteins interaction leads to a change in texture and microstructure of the formulated thigh [35].

Effect of zeolite addition on meat color, drip loss and pH 24 h

The effect of zeolite on drip loss, pH 24 h, and CIELab color of turkey breast meat booth for female and male is shown in Table 5 (a, b). The supplement of 2% of zeolite significantly increased the pH 24 h (p < 0.05) compared to control group only for the breast meat of male (5.80 ± 0.08 vs. 5.94 ± 0.08). However, there were no significant differences (p > 0.05) for drip loss, lightness L*, redness a* value and yellowness b* value among the three groups.

Table 5 Effect of zeolite addition on meat color, drip loss and pH 24 h for female (3a) and male (3b) meat
Full size table

An increase in pH indicated that the zeolite could maintain the quality of longer period. In the literature, the variation of food additives, animal management and slaughter environment could result in different pH values of the meat. Dietary supplementation with citrus pulp (10%) appeared to decrease the ultimate pH of broiler meat [3]. On the other hand, Jang et al. [4] have reported that supplementation with a mixture of dietary herb extracts (mulberry leaf, Japanese honeysuckle and goldthread) increased the pH values of broiler meat directly after slaughter [4]. However, feeding a diet supplemented with oregano (3%) (Young et al.), grape seed extract (2500 ppm), green tea extract (2500 ppm) (Rababah et al.), or a cranberry extract at concentrations between 40 and 160 mg kg− 1 feed (Leunisk et al.) did not affect the pH values of broiler meat [41,42,43].

Effect of zeolite addition on oxidative stress

Activated and micronized zeolites are used as detoxifying agents in humans. Detoxification is attributed to their ability to reduce lipid peroxidation by scavenging free radicals [13]. In the present study, the effect of supplemental zeolite on antioxidant status of turkey are shown in Table 6a and Table 6b.

Table 6 Redox status in the liver (a) and the meat (b) of turkey poults fed diets with supplemental zeolite
Full size table

As they eliminate superoxide, hydrogen peroxide and hydroxyl radicals, antioxidant enzymes (SOD, GPX and catalase) play an important role in defense mechanisms against free radicals [44]. Malondialdehyde (MDA), used as the best existing measure of universal ROS, is an aldehyde produced fromlipid peroxidation, which is estimated based on its reaction with thiobarbituric acid [43]. In the present study, the addition of 2% of zeolite for experimental group significantly, (p < 0. 05) decrease the MDA level for female liver (1. 17 vs. 1. 00), male liver (1. 05 vs.0. 90), female meat (0.62 vs. 0.48) and male meat (0. 47 vs.0. 35) compared with the control group. In contrast, SOD and GPX are increase for meat and liver but the differences were not significant (p > 0.05). Moreover, dietary zeolite supplementation has an effect on CAT level (decrease from 0.341 for control group to 0.246 for experimental groups (2% zeolite)) only for male meat. The antioxidant capacity of turkey poult could be improved by supplemental zeolite. The results proved that supplementation of zeolite at all treatment concentration did not increase the activities of SOD and GPX but decrease the MDA content in meat and liver under normal condition.

There are growing evidences supporting that oxidative stress and free radical injury are the causative agents during the pathophysiological processes of alcoholic liver disease (ALD) related to excessive alcohol consumption [45, 46]. However, in our experimental model, supplemental zeolite led to a non-significant increase in liver and meat SOD activity. Some studies have shown increases SOD activity after zeolite administration [47], while others have shown decrease [48].

On the other hand, zeolite administration (5 mg/kg) orally for 10 days, in rats with partial hepatectomy decreased oxidant activity through elevation of liver tissue copper-zinc SOD activity and glutathione (GSH) levels and reduction of plasma and liver tissue MDA levels [49]. It has been reported that mice exposed to zeolite at the time of initial plaque accumulation had a significant increase in SOD activity in their hippocampi compared with age-matched control mice [50]. According to Zarcovic et al. and Basha et al. [51, 52], the supplementation of zeolite reduce lipid peroxidation levels and recovered the levels of catalase, SOD and GPX activity during pb2+ toxicity.

Recently, Hossein Nia et al. [53] have reported that zeolite (CLN) and nanoparticle of zeolite (NCLN) administration for STZ-induced diabetic rats compared with the healthy animals has no significant difference in the activity of SOD and GPX. In against part, CLN reduced MDA levels more than NCLN in the normal group (p < 0.05).

Zeolite was used in our study for the following reasons: zeolite is capable of adsorbing many different types of gas, moisture, petrochemicals, heavy metals and radioactive elements and a multitude of various compounds; it has a total cation-exchange capacity of about 200 mEq. The exchange capacity plays an important role in the therapeutic use of zeolite, accounting for its ability to release useful elements while capturing and binding others [54, 55].

The exact mechanisms of zeolites ‘antioxidant effects are not well known. In effect, zeolite is not absorbed into the blood from the gut. The effects of zeolite may be due to an indirect interaction with biochemical systems, removal of waste and toxins from the gut, improvement of the immune system through the mucosal-related intestinal lymphoid tissue, and an increase in the bioavailability of minerals that are important co-factors for some enzymes [56,57,58].

Conclusion

The results of this study showed that the use of zeolite at a dose of 2% as feed additive had a beneficial effect on turkey’s growth, breast meat antioxidative capacity and led to the improvement of their meat quality. The present experiment shows also the significance of using zeolite, as a feed additive for turkeys, as part of a comprehensive program to increase level of polyunsaturated fatty acids on the turkey body. Hence, it is concluded that the use of alternative management strategies can include natural zeolites, however, other factors such as the type of the natural zeolite or its inclusion ratio, need further investigation.

References

  1. Hume ME, Clemente-Hernández S, Oviedo-Rondón EO. Effects of feed additives and mixed eimeria species infection on intestinal microbial ecology of broilers. Poult Sci. 2006;85(12):2106–11.

    Article  PubMed  CAS  Google Scholar 

  2. Jørgensen H, Zhao XQ, Theil PK, Jakobsen K. Effect of graded levels of rapeseed oil in isonitrogenous diets on the development of the gastrointestinal tract, and utilisation of protein, fat and energy in broiler chickens. Arch Anim Nutr. 2008;62(4):331–42.

    Article  PubMed  CAS  Google Scholar 

  3. Mourao JL, Pinheiro VM, Prates JAM, Bessa RJB, Ferreira LMA, Fontes CMGA, Ponte PIP. Effect of dietary dehydrated pasture and citrus pulp on the performance and meat quality of broiler chickens. Poult Sci. 2008;87:733–43.

    Article  PubMed  CAS  Google Scholar 

  4. Jang A, Liu XD, Shin MH, Lee BD, Lee SK, Lee JH, Jo C. Antioxidative potential of raw breast meat from broiler chicks fed a dietary medicinal herb extract mix. Poult Sci. 2008;87:2382–9.

    Article  PubMed  CAS  Google Scholar 

  5. Attia Y. A., H. F. Allakany, , A. E. Abd Al-Hamid, , A. A. Al-Saffar, , R. A. Hassan, N. A. Mohamed, (2013). Capability of different non-nutritive feed additives on improving productive and physiological traits of broiler chicks fed diets with or without aflatoxin during the first 3 weeks of life. J of Animal Physiology and Animal Nutrition 97 (4): 754–772.

    Article  CAS  Google Scholar 

  6. Attia YA, A E, Abd Al-Hamid HF, Allakany MA, Al-Harthi, Mohamed NA. Necessity of continuing of supplementation of non-nutritive feed additive during day 21-42 of age following three weeks of feeding aflatoxin to broiler chickens. J of Applied Animal Res. 2016;44(1):87–98.

    Article  CAS  Google Scholar 

  7. Altop A, Erener G, Duru ME, Isik K. Effects of essential oils from Liquidambar orientalis Mill. leaves on growth performance, carcass and some organ traits, some blood metabolites and intestinal microbiota in broilers. Br Poult Sci. 2018;59(1):121–7.

    Article  PubMed  CAS  Google Scholar 

  8. Papaioannou D, Katsoulos PD, Panousis N, Karatzias H. The role of natural and synthetic zeolites as feed additives on the prevention and/or the treatment of certain farm animal diseases: a review. Micropor Mesopor Mat. 2005;84:161–70.

    Article  CAS  Google Scholar 

  9. Sersale R. Natural zeolites: processing, present and possible applications. Stud Surf Sci Catal. 1985;24:503–12.

    Article  CAS  Google Scholar 

  10. Naber JE, De Jong KP, Stork WHJ, Kuipers HPCE, Post MFM. Industrial applications of zeolite catalysis. Stud Surf Sci Catal. 1994;84:2197–219.

    Article  CAS  Google Scholar 

  11. Rodríguez-Fuentes G, Barrios MA, Iraizoz A, Perdomo I, Cedré B: Enterex: anti-diarrheic drug based on purified natural clinoptilolite. Zeolites Volume 19, Issues 5–6, November–December 1997, 441–448.

  12. Papaioannou DS, Kyriakis SC, Papasteriadis A, Roumbies N, Yannakopoulos A, Alexopoulos C. Effect of in-feed inclusion of a natural zeolite (clinoptilolite) on certain vitamin, macro and trace element concentrations in the blood, liver and kidney tissues of sows. Res Vet Sci. 2002;72(1):61–8.

    Article  PubMed  CAS  Google Scholar 

  13. Atitlán-Gil A, Bretón-de la Loza MM, Jiménez-Ortega JC, Belefant-Miller H, Betanzos-Cabrera G. Activated and micronized zeolite in the modulation of cellular oxidative stress in Mexican smokers: a randomized clinical trial. Rev Inves Clin. 2017;69:146–51.

    Google Scholar 

  14. Mumpton FA, Fishman PH. The application of natural zeolites in animal science and aquaculture. J Anim Sci. 1977;45:1188–203.

    Article  CAS  Google Scholar 

  15. Onogi T. Treating experiments of chicken droppings with zeolite-tuff. Experimental use of zeolite-tuff as dietary supplements for chickens. Rep Yamagata Stock Raising lnst. 1966:7.

  16. Muzaffer T, Demirel R, Şentürk D, Kurt D, Bacinoglu S, Cirit Ü, Ketani MA. Effects of dietary natural zeolite on the testicular weight, body weight and spermatological characteristics in rats. J Fac Vet Med. 2007;33:33–42.

    Google Scholar 

  17. Wu-Haan W, Powers WI, Angel CR, Hale CE III, Applegate TJ. Effect of an acidifying diet combined with zeolite and slight protein reduction on air emissions from laying hens of different ages. Poult Sci. 2007;86:182–90.

    Article  PubMed  CAS  Google Scholar 

  18. Wen T, Zhang X, Zhang HQ, Liu JD. Ammonium removal from aqueous solutions by zeolite absorption together with chemical precipitation. Water Sci Technol. 2010;61:1941–7.

    Article  PubMed  CAS  Google Scholar 

  19. Beker A, Vanhooser SL, Swartzlander JH, Teeter RG. Atmospheric ammonia concentration effects on broiler growth and performance. J Appl Poult Res. 2004;13:5–9.

    Article  CAS  Google Scholar 

  20. Pordomingo AJ, García TP, Volpi Lagreca G. Effect of feeding treatment during the backgrounding phase of beef production from pasture on: II. Longissimus muscle proximate composition, cholesterol and fatty acids. Meat Sci. 2012;90:947–55.

    Article  PubMed  CAS  Google Scholar 

  21. Bonou GA, Ahounou SG, Arikè Salifou CF, Paraïso FH, Bachabi K, Konsaka BM, Dahouda M, Dougnon JT, Farougou S, IAK Y. Influence of pre-slaughter transportation duration stress on carcass and meat quality of indigenous chicken reared under traditional system in Benin. Livest Res Rural Dev. 2018;30(4)

  22. Ho E, Galougahi KK, Liu CC, Bhindi R, Gemma A. Figtree biological markers of oxidative stress: applications to cardiovascular research and practice. Redox Biol. 2013;1(1):483–91.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  23. Folch J, Lees M, Sloane Stanley GH. A simple method for the isolation and purification of total lipids from animal tissues. J Biol Chem. 1957;226:497–509.

    PubMed  CAS  Google Scholar 

  24. Cherif S, Mnif S, Hadrich F, Abdelkafi S, Sayadi S. Strategy for improving extracellular lipolytic activities by a novel thermotolerant Staphylococcus sp. strain. Lipids Health Dis. 2011;10:209.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  25. Wang Y, Sunwoo H, Cherian G, Sim JS. Fatty acid determination in chicken egg yolk: a comparison of different methods. Poult Sci. 2000;79:1168–71.

    Article  PubMed  CAS  Google Scholar 

  26. Cameron ND, Wood JD, Enser M, Whittington FM, Penman JC, Robinson AM. Sensitivity of pig genotypes to short-term manipulation of plasma fatty acids by feeding linseed. Meat Sci. 2000;56:379–86.

    Article  PubMed  CAS  Google Scholar 

  27. Draper HH, Hadley M. Malondialdehyde determination as index of lipid peroxidation. Methods Enzymol. 1990;86:421–31.

    Article  Google Scholar 

  28. Ben Slima A, Ben Ali M, Barkallah M, Traore AI, Boudawara T, Allouche N, Gdoura R. Antioxidant properties of Pelargonium graveolens L’Her essential oil on the reproductive damage induced by deltamethrin in mice as compared to alpha-tocopherol. Lipids Health Dis. 2013;11:35.

    Google Scholar 

  29. Beauchamp C, Fridovich I. Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal Biochem. 1971;44:276–87.

    Article  PubMed  CAS  Google Scholar 

  30. Aebi H. Catalase in vitro. Methods Enzymol. 1984;105:121–6.

    Article  PubMed  CAS  Google Scholar 

  31. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ. Protein measurement with Folin phenol reagent. J Biol Chemi. 1951;193:265–70.

    CAS  Google Scholar 

  32. Shariatmadari F. The application of zeolite in poultry production. World’s Poultry Sci J. 2008;64:76–84.

    Article  Google Scholar 

  33. Eleroglu H, Yalcin H. Use of natural zeolite supplemented litter increased broiler production. Afr J Anim Sci. 2005;35:90–7.

    CAS  Google Scholar 

  34. Karamanlis X, Fortomaris P, Arsenos G, Dosis I, Papaionnou D, Batzios C, Kamarianos A. The effect of a natural zeolite (clinoptilolite) on the performance of broiler chickens and the quality of their litter. Asian-Aust J Anim Sci. 2008;21:1642–50.

    Article  CAS  Google Scholar 

  35. Mallek Z, Fendri I, Khannous L, Ben Hassena A, Traore AI, Ayadi MA, Gdoura R. Effect of zeolite (clinoptilolite) as feed additive in Tunisian broilers on the total flora, meat texture and the production of omega 3 polyunsaturated fatty acid. Lipids Health Dis. 2012;11:35.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  36. Suchy P, Strakova E, Vecerek V, Klouda Z. Kracmarova E the effect of a clinoptilolite-based feed supplement on the performance of broiler chickens. Czech J Anim Sci. 2006;51:168–73.

    Article  CAS  Google Scholar 

  37. Jand SK, Paviter K, Sharma NS. Mycoses and mycotoxicoses in poultry: a review. J Anim Sci. 2005;75:465–76.

    Google Scholar 

  38. Ortatatli M, Oguz H, Hatipojlu F, Karaman M. Evaluation of pathological changes in broilers during chronic afflatoxin (50 and 100 ppb) and clinoptilolite exposure. Res Vet Sci. 2005;78:61–8.

    Article  PubMed  CAS  Google Scholar 

  39. Juárez M, Dugan MER, Aalhus JL, Aldai N, Basarab JA, Baron VS, McAllister TA. Effects of vitamin E and flaxseed on rumen-derived fattyacid intermediates in beef intramuscular fat. Meat Sci. 2011;88:434–40.

    Article  PubMed  CAS  Google Scholar 

  40. Nagao T, Komine Y, Soga S, Meguro S, Hase T, Tanaka Y, Tokimitsu I. Ingestion of a tea rich in catechins leads to a reduction in body fat and malondialdehyde-modified LDL in men. Am J Clin Nutr. 2005;81:122–9.

    Article  PubMed  CAS  Google Scholar 

  41. Young JF, Stagsted J, Jensen SK, Karlsson AH, Henckel P. Ascorbic acid, a-tocopherol and oregano supplements reduce stress-induced deterioration of chicken meat quality. Poult Sci. 2003;82:1343–51.

    Article  PubMed  CAS  Google Scholar 

  42. Rababah TM, Ereifej KI, Al-Mahasneh MA, Al- Rababah MA. Effect of plant extracts on physiochemical properties of chicken breast meat cooked using conventional electric oven or microwave. Poult Sci. 2006;85:148–54.

    Article  PubMed  CAS  Google Scholar 

  43. Leunisk G, Rempel H, Skura B, Berkyto M, White W, Yang Y, Rhee JY, Xuan SY, Chiu S, Silversides F, Fitzpatrick S, Diarra MS. Growth performance, meat quality, and gut microflora of broiler chickens fed with cranberry extract. Poult Sci. 2010;89:1514–23.

    Article  CAS  Google Scholar 

  44. Samarghandian S, Borji A, Delkhosh MB, Samini F. Safranal treatment improves hyperglycemia, hyperlipidemia and oxidative stress in streptozotocin-induced diabetic rats. J Pharm Pharm Sci. 2013;16:352–62.

    Article  PubMed  Google Scholar 

  45. Qujeq D, Habibinudeh M, Daylmkatoli H, Rezvani T. Malondialdehyde and carbonyl contents in the erythrocytes of streptozotocin-induced diabetic rats. Int J Diabetes Metab. 2005;13:96–8.

    CAS  Google Scholar 

  46. Purohit V, Russo D, Salin M. Role of iron in alcoholic liver disease: introduction and summary of the symposium. Alcohol. 2003;30:93–7.

    Article  PubMed  Google Scholar 

  47. Calabrese V, Renis M, Calderone A, Russo A, Barcellona ML, Rizza V. Stress proteins and SH-groups in oxidant-induced cell damage after acute ethanol administration in rat. Free Radic Biol Med. 1996;20:391–7.

    Article  PubMed  CAS  Google Scholar 

  48. Kakkar R, Kalra J, Mantha SV, Prasad K. Lipid peroxidation and activity of antioxidant enzymes in diabetic rats. Mol Cell Biochem. 1995;151:113–9.

    Article  PubMed  CAS  Google Scholar 

  49. Wohaieb SA, Godin DV. Alterations in free radical tissue-defense mechanisms in streptozocin-induced diabetes in rat: Effects of insulin treatment. Diabetes. 1987;36:1014–8.

    Article  PubMed  CAS  Google Scholar 

  50. Saribeyoglu K, Aytac E, Pekmezci S. Effects of clinoptilolite treatment on oxidative stress after partial hepatectomy in rats. Asian J Surg. 2011;34:153–7.

    Article  PubMed  Google Scholar 

  51. Montinaro M, Uberti D, Maccarinelli G, Bonini SA, Ferrari-Toninelli G, Memo M. Dietary zeolite supplementation reduces oxidative damage and plaque generation in the brain of an Alzheimer’s disease mouse model. Life Sci. 2013;92:903–10.

    Article  PubMed  CAS  Google Scholar 

  52. Zarcovic N, Zarcovic K, Kralj M. Anticancer and antioxidative effects of micronized zeolite clinoptilolite. Anticancer Res. 2003;23:1589–96.

    Google Scholar 

  53. Basha MP, Begum S, Mir BA. Neuroprotective actions of clinoptilolite and ethylenediaminetetraacetic acid against lead-induced toxicity in mice Mus musculus. Toxicol Int. 2013;20:201–7.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  54. Behnoosh HN, Khorram S, Rezazadeh H, Safaiyan A, Tarighat-Esfanjani A. The effects of natural Clinoptilolite and Nano-sized Clinoptilolite supplementation on glucose levels and oxidative stress in rats with type 1 diabetes. Can J Diabetes. 2018;42:31–5.

    Article  Google Scholar 

  55. Kubena LF, Huff WE, Harvey RB, Yersin AG, Ellissalde MH, Witzel DA, Corrier DE, Phillips TD, Petersen HD. Effects of a hydrated sodium calcium alüminosilicate on growing Turkey poults during aflatoxicosis. Poult Sci. 1991;70:1823–30.

    Article  PubMed  CAS  Google Scholar 

  56. Dogliotti G, Malavazos AE, Giacometti S. Natural zeolites chabazite/ phillipsite/analcime increase blood levels of antioxidant enzymes. J Clin Biochem Nutr. 2012;50:195–8.

    Article  PubMed  CAS  Google Scholar 

  57. Pavelic´ K, Hadžija M, Bedrica L. Natural zeolite clinoptilolite: new adjuvant in anticancer therapy. J Mol Med. 2001;78:708–20.

    Article  PubMed  Google Scholar 

  58. Ivkovic S, Deutsch U, Silberbach A. Dietary supplementation with the tribomechanically activated zeolite clinoptilolite in immunodeficiency: effects on the immune system. Adv Ther. 2004;21:135–47.

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

Particular thanks were addressed to Mr. Mohamed Makni for CPG analyses. This work received financial support from “Ministère de l’enseignement supérieur et de la recherche et de la technologie” granted to the «Unité de recherche Toxicologie - Microbiologie environnementale et santé, Faculté des Sciences de Sfax, Université de Sfax-Tunisie ».

Author information

Authors and Affiliations

  1. Laboratory of Toxicology and Environmental Health LR11ES06, Sciences Faculty of Sfax, University of Sfax, Sfax, Tunisia

    Emna Hcini, Ahlem Ben Slima, Imen Kallel, Sonia Zormati & Radhouane Gdoura

  2. National Laboratory of Public Health, Ouagadougou, Burkina Faso

    Al Ibrahim Traore

Authors
  1. Emna Hcini
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ahlem Ben Slima
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Imen Kallel
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Sonia Zormati
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Al Ibrahim Traore
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Radhouane Gdoura
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

EH, ABS, IK, SZ and AT designed the experiments, analyzed the data and drafted the manuscript. and RG conceived research and approaches and have given final approval of the manuscript to be published. All authors read and approve the final manuscript.

Corresponding author

Correspondence to Al Ibrahim Traore.

Ethics declarations

Ethics approval and consent to participate

Not applicable.

Consent for publication

All authors read and approve the final manuscript.

Competing interests

The authors declare that they have no competing interests.

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hcini, E., Ben Slima, A., Kallel, I. et al. Does supplemental zeolite (clinoptilolite) affect growth performance, meat texture, oxidative stress and production of polyunsaturated fatty acid of Turkey poults?. Lipids Health Dis 17, 177 (2018). https://doi.org/10.1186/s12944-018-0820-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1186/s12944-018-0820-7

Keywords

Lipids in Health and Disease

ISSN: 1476-511X