LITERATURE REVIEW

Aflatoxin, deoxynivalenol, and zearalenone in swine diets: Predictions on growth performance^¤

Aflatoxina, deoxynivalenol y zearalenona: predicciones sobre su impacto en el crecimiento de los cerdos

Aflatoxina, deoxinivalenol e zearalenona em dietas de porcos: predições de desempenho no crescimento

Chan Hee Mok, Animal Science, BA; Seung Youp Shin, Animal Science, BA; Beob Gyun Kim^*, Animal Science, PhD.

* Corresponding author: Beob Gyun Kim. Department of Animal Science and Technology, Konkuk University, Seoul 143-701, Korea. Tel +82-2-2049-6255. Email: bgkim@konkuk.ac.kr

Department of Animal Science and Technology, Konkuk University, Seoul 143-701, Republic of Korea.

(Received: March 11, 2013; accepted: October 21, 2013)

Summary

Dietary mycotoxins have been shown to cause detrimental effects in swine health and production. The objective of this study was to develop tools for predicting the effects of aflatoxin (AFL), deoxynivalenol (DON) and zearalenone (ZON) on feed intake (FI) and weight gain (WG) changes using a meta-analysis approach. A total of 80 and 63 observations were extracted from 18 experiments testing the effects of AFL on FI and WG, respectively, and the differences of AFL concentrations between the control and treatment groups ranged from 0.02 to 2.5 mg/kg. A total of 117 and 113 observations from 20 experiments were used for testing the effects of DON on FI and WG, respectively. The differences of DON concentrations between the control and treatment groups ranged from 0.5 to 10.5 mg/kg. A total of 16 and 17 observations from 18 experiments were used for testing the effects of ZON on FI and WG, respectively, and the differences of ZON concentrations between the control and treatment groups ranged from 0.2 to 9.0 mg/kg. Effects of experiment, initial body weight, and experimental period were not significant for developing prediction equations for the changes of FI and WG. The models developed for predicting FI and WG changes (ΔFI and ΔWG) as % by AFL concentrations as mg/kg were: ΔFI = –24.9 × AFL – 1.7 with r² = 0.70 and p<0.001; ΔFI = 0.4 – 51.6 × (1 – e^{–0.947×AFL}) with r² = 0.79 and p<0.001; ΔWG = –22.7 × AFL – 4.0 with r² = 0.62 and p<0.001; and ΔWG = –1.4 – 50.3 × (1 – e^{–0.976×AFL}) with r² = 0.69 and p<0.001. The equations for predicting ΔFI and ΔWG as % by DON concentrations as mg/kg were: ΔFI = –5.64 × DON – 0.13 with r² = 0.60 and p<0.001; and ΔWG = –6.49 × DON + 0.93 with r² = 0.61 and p<0.001. The feed consumption and growth rate of pigs decrease linearly and exponentially by the concentrations of AFL and linearly by the concentrations of DON. The equations provided herein may predict the effects of AFL and DON on swine production performance.

Key words: feed intake, meta-analysis, mycotoxin, pig, weight gain.

Resumen

Las micotoxinas presentes en los alimentos tienen efectos perjudiciales en la salud y la producción porcina. El objetivo de este estudio fue desarrollar herramientas para predecir los efectos de aflatoxinas (AFL), deoxinivalenol (DON) y zearalenona (ZON) sobre el consumo de alimento (FI) y ganancia de peso (WG) mediante un meta-análisis. Un total de 80 y 63 observaciones provenientes de 18 experimentos que evaluaron los efectos de la AFL sobre el FI y WG, respectivamente, fueron tenidas en cuenta. Se encontró que las diferencias de concentración de AFL entre los grupos control y tratados variaron desde 0,02 hasta 2,5 mg/kg. De otro lado, se utilizaron un total de 117 y 113 observaciones de 20 experimentos para probar los efectos de DON en FI y WG, respectivamente. Las diferencias de concentración de DON entre los grupos control y tratados variaron desde 0,5 hasta 10,5 mg/kg. Por último, un total de 16 y 17 observaciones de 18 experimentos se utilizaron para probar los efectos de ZON en FI y GT, respectivamente; las diferencias de concentración de ZON entre los grupos control y tratados variaron desde 0,2 hasta 9,0 mg/kg. Los efectos de Experimento, Peso corporal inicial, y Período experimental no fueron significativos para el desarrollo de las ecuaciones de predicción de cambios en FI y WG. Los modelos desarrollados para predecir cambios porcentuales en FI y WG (ΔFI y ΔWG) según la concentración de AFL (mg/kg) fueron: ΔFI = -24,9 × AFL - 1,7 con r² = 0,70 y p<0,001; ΔFI = 0,4-51,6 × (1 - e^{- 0.947 × AFL}) con r² = 0,79 y p<0,001; ΔWG = -22,7 × AFL - 4,0 con r² = 0,62 y p<0,001, y ΔWG = -1,4 - 50,3 × (1 - e^{- 0.976 × AFL}) con r² = 0,69 y p<0,001. Las ecuaciones para predecir ΔFI y ΔWG (como %) por las concentraciones de DON (mg/kg) fueron: ΔFI = -5,64 × DON - 0,13 con r² = 0,60 y p<0,001; y ΔWG = -6,49 + 0,93 × DON con r² = 0,61 y p<0,001. El consumo de alimento y la tasa de crecimiento de cerdos disminuyen lineal y exponencialmente según la concentración de AFL; mientras que solamente se observa una disminución de tipo lineal en función de las concentraciones de DON. Las ecuaciones obtenidas en este trabajo podrían usarse para predecir los efectos de AFL y DON sobre el desempeño productivo del cerdo.

Palabras clave: cerdo, consumo de alimento, ganancia de peso, meta-análisis, micotoxinas.

Resumo

As micotoxinas presentes nos alimentos tem efeitos prejudiciais na saúde e na produção porcina. O objetivo deste estudo foi desenvolver ferramentas para a predição dos efeitos da aflatoxina (AFL), deoxinivalenol (DON) e zearalenona (ZON) sobre o consumo de alimento (FI) e ganho de peso (WG) mediante uma metaanálise. Um total de 80 e 63 observações extraídas de 18 experimentos que avaliaram os efeitos da AFL sobre o FI e WG, respectivamente, encontraram que as diferenças de concentração de AFL entre os grupos controle e tratados variaram desde 0,02 até 2,5 mg/kg. Por outro lado, foram utilizados um total de 117 e 113 observações de 20 experimentos para provar os efeitos de DON em FI e WG, respectivamente. As diferenças de concentração de DON entre os grupos controle e tratados variaram desde 0.5 até 10,5 mg/kg. Por fim, um total de 16 e 17 observações de 18 experimentos foram utilizados para provar os efeitos de ZON em FI e GT, respectivamente, e as diferenças de concentração de ZON entre os grupos controle e tratados variaram desde 0,2 até 9,0 mg/kg. Os efeitos de Experimento, Peso corporal inicial e Período experimental não foram significativos para o desenvolvimento das equações de predição de mudanças em FI e WG. Os modelos desenvolvidos para predizer mudanças percentuais em FI e WG (ΔFI e ΔWG) segundo a concentração de AFL (mg/kg) foram: ΔFI = -24,9 × AFL - 1,7 com r² = 0,70 e p<0,001; ΔFI = 0,4-51,6 × (1 - e^{- 0.947 × AFL}) com r² = 0,79 y p<0,001; ΔWG = -22,7 × AFL - 4,0 com r² = 0,62 e p<0,001, e ΔWG = -1,4 - 50,3 × (1 - e^{- 0.976 × AFL}) con r² = 0,69 e p<0,001. As equações para predizer ΔFI e ΔWG (como %) pelas concentrações de DON (mg/kg) foram: ΔFI = -5,64 × DON - 0,13 com r² = 0,60 e p<0,001; e ΔWG = -6,49 + 0,93 × DON com r² = 0,61 e p<0,001. Conclusão: o consumo de alimento e a taxa de crescimento de porcos diminuem linearmente e exponencialmente segundo a concentração de AFL, e linearmente segundo a concentração de DON. As equações obtidas neste trabalho são de utilidade para predizer os efeitos de AFL e DON sobre o desempenho porcino.

Palavras chave: consumo de alimento, ganho de peso, meta-análise, micotoxinas, porco.

Introduction

Contamination of mycotoxin in feed causes problems in livestock production processes by reducing growth performance. Mycotoxins in swine feed generally cause feed intake (FI) and weight gain (WG) reductions (Lindemann et al., 1993). The detrimental effects of dietary mycotoxins result in significant economic losses (Shull and Cheeke, 1983). If a dietary mycotoxin causes growth retardation due to decreased FI, this production loss can be at least partially prevented by formulating diets with greater concentration of nutrients. The nutrient requirements for swine are based on the daily intake amount (NRC, 2012). Thus, an estimation of FI reduction based on the mycotoxin concentration is important.

The most frequently found mycotoxins in swine feedstuffs are Aflatoxin (AFL), deoxynivalenol (DON) and zearalenone (ZON). Many studies have investigated the influences of AFL, DON and ZON on growth performance of swine. However, responses reported in the literature vary considerably. The reasons for this variation are likely due to the differences of experimental conditions, such as pig age, concentration of mycotoxins, and type of feed, among others. Therefore, the present study was conducted to overview the effects of dietary mycotoxins on performance and physiological responses and to develop tools for predicting the effects of mycotoxins on FI and WG changes by integrating and summarizing the quantitative data were available. The information data in the literature.

Aflatoxin

Aflatoxins are toxic metabolites produced by Aspergillus flavus-parasiticus (Marin et al., 2002) and their effects on pig performance have been investigated in many studies. Most researchers concluded that dietary AFL affect FI and WG without affecting gain:feed or organ weight. In some studies, however, liver weight, liver-specific enzyme activity, and serum globulin patterns were influenced by dietary AFL (Table 1).

For the compilation of data from the literature, experiments with growth data were selected. Data for dietary AFL concentrations, FI, and WG from the experiments were collected when the quantitative data were available. The information recorded included AFL concentration in diet, initial age, initial BW, final BW, sex, number of pigs, FI, WG, gain:feed, and experimental period. When possible, WG was calculated based on BW changes and gain:feed was calculated using FI and WG.

Data from 18 experiments were extracted and included 80 observations for FI and 63 observations for WG. The difference of AFL concentrations between the control diet and the treatment diets in these 18 experiments ranged from 0.02 to 2.5 mg/kg. The sources of AFL were rice (12 studies) and corn (9 studies). Purified AFL was used in 1 study. The source of AFL was unknown in 2 studies. In some studies multiple sources were used. Reductions of FI and WG were the major response to AFL. The changes (%) of WG, FI, and gain:feed by additional AFL relative to the control group were calculated from each treatment group (Table 2).

Collected data were analyzed using the REG and NLIN procedures of SAS (SAS Institute Inc., Cary, NC, USA). When values for REG procedures exceeded 0.20 in Cook's distance, data were considered as outliers and not used for further analysis. After excluding outliers, variations of FI and WG were predicted in equations by the REG procedures and regression equations by the NLIN procedures.

Effects of experiment, BW, and experimental period were not significant for developing prediction equations for the changes of FI and WG. The models developed for predicting FI and WG changes (ΔFI and ΔWG) as % by AFL concentrations as mg/kg were: ΔFI = –24.9 × AFL – 1.7 with r² = 0.70 and p<0.001; ΔFI = 0.4 – 51.6 × (1 – e^{–0.947×AFL}) with r² = 0.79 and p<0.001; ΔWG = –22.7 × AFL – 4.0 with r² = 0.62 and p<0.001; and ΔWG = –1.4 – 50.3 × (1 – e^{–0.976×AFL}) with r² = 0.69 and p<0.001 (Figure 1). Theoretically, the changes of FI and WG cannot be less than -100%, and thus, exponential models were also used. However, exponential models did not have large improvements in r-square compared with linear models. The linear response in WG changes was also reported by Andretta et al. (2012). However, they reported that the slope was -3.95 which was much less steeper than -22.7 in the present work. In our equation, if the negative intercept were forced to zero, the steepness of the slope would become even greater. The reason for the difference in the slopes is unknown.

In conclusion, feed consumption and growth rate of pigs decline linearly and exponentially with AFL concentration.

Deoxynivalenol

Deoxynivalenol is one of the secondary metabolites of Fusarium (Accensi et al., 2006). As dietary DON commonly causes vomiting in pigs, DON is often called vomitoxin. Deoxynivalenol mainly affects FI and WG in swine, and DON has been reported to accumulate in liver and kidney (Table 1). Also, dietary DON results in reduced fetal weight and osmolality of allantoic fluid.

As for AFL experimental data compilation, experiments with growth data were selected. Data for dietary DON concentrations, FI, and WG from the experiments were collected when quantitative data was available. The information recorded included DON concentration in diet, initial age, initial BW, final BW, sex, number of pigs, FI, WG, gain:feed, and experimental period. When possible, WG was calculated based on BW changes and gain:feed was calculated using FI and WG.

Data from 20 experiments were extracted and included 117 observations for FI and 113 observations for WG. The difference of DON concentrations between the control diet and the treatment diets in these 20 experiments ranged from 0.5 and 10.5 mg/kg (Table 3).

Collected data were analyzed using the REG procedures and the NLIN procedures of SAS (SAS Institute Inc., Cary, NC, USA). Using the REG procedures, data were considered as outliers and not used for further analysis when values exceeded 0.20 in Cook's distance. After excluding outliers, variations of FI and WG were predicted in linear equations by the REG procedures.

The equations for predicting ΔFI and ΔWG (as %) by DON concentrations (as mg/kg) were: ΔFI = –5.64 × DON – 0.13 with r² = 0.60 and p<0.001; and ΔWG = –6.49 × DON + 0.93 with r² = 0.61 and p<0.001 (Figure 2). Exponential models were not significant perhaps due to concentrations of DON were not high enough to cause greater responses. Similarly to the AFL data, the steepness of the slope in the present study was greater than the slope reported by Andretta et al. (2012).

In conclusion, feed consumption and growth rate of pigs decline linearly with DON concentrations.

Zearalenone

Zearalenone was detected in bile of sows and piglets fed ZON contaminated diets (Dänicke et al., 2007; Goyarts et al., 2007). In a study by Young et al. (1981), when a diet containing ZON more than 6 mg/kg was fed to gilts, swelling and redness of the vulvae were observed (Table 1). With an increase of dietary ZON concentrations, uterine weight and the thickness of the vaginal epithelium increased (Young et al., 1981). Recently, Wang et al. (2012) reported that dietary ZON resulted in decreased nutrient digestibility, increased oxidative stress, and reduced growth rate of pigs.

In the present work, a meta-analysis for the effects of ZON on FI and WG was not conducted due to the lack of data reported in the literature. Available data to date are summarized in table 4. Detrimental effects of dietary ZON on growth performance of pigs are clear. Dietary ZON (mean 3.8 mg/kg in diet) resulted in 15.8% FI reductions and 28.8% WG reductions on average. However, more data are needed to develop a model for precise prediction of dose-dependent growth responses.

Strategies to alleviate damages from mycotoxins

To avoid detrimental effects of mycotoxins, several decontamination or detoxification methods are available such as thermal inactivation and irradiating (physical methods), treatment with acid/base solutions, ozonation, and ammoniation (chemical methods), and degradation of toxins by microorganisms (biological methods) (Diaz and Smith, 2005). Supplementation with toxinsequestering agents is the most frequently used method by the swine feed industry because of its economic feasibility and suitability from a nutritional perspective.

Mycotoxin sequestering agents available to the feed industry include silicate clays, activated carbons, and yeast-derived products (NRC, 2012). Zeolites, bentonites, and hydrated sodium calcium aluminosilicates (HSCAS) are representative types of silicate clays. These clays generally have high affinity for AFL, but have little sequestering effect on other mycotoxins (Diaz and Smith, 2005). While in some studies activated carbon reduced or eliminated the effects of AFL (Hatch et al., 1982; Dalvi and McGowan, 1984; Galvano et al., 1996), other researchers failed to find the effect of activated charcoal on animals fed mycotoxincontaminated diets (Kubena et al., 1990; Edrington et al., 1997; Cabassi et al., 2005). Glucomannan polymers derived from yeast cell walls are also used as mycotoxin binders (NRC, 2012).

Several studies have been conducted to investigate the efficacy of sequestering agents to a single specific mycotoxin using in vitro and in vivo methods (Lindemann et al., 1993; Diaz et al., 2002, 2004; Marroquín-Cardona et al., 2009). However, swine diets could potentially be contaminated with multiple species of mycotoxins because those diets typically consist of a mixture of multiple ingredients (van Heugten, 2001). Nevertheless, to the best of our knowledge, no single sequestering agent is available that can effectively sequester multiple mycotoxins (i.e., AFL, DON, and ZON). Thus, a strategy to use multiple sequestering agents has been inevitably used. It is important to determine the sequestering efficiency of an agent for each toxin to obtain the optimum formula of sequestering agents.

Several in vitro methods are available to predict the in vivo efficacy of sequestering agents (Diaz et al., 2002; Marroquín-Cardona et al., 2009). However, these methods may not be applicable to the intestinal environment of pigs. Thus, research with a more precise in vitro method to mimic the digestive processes of pigs is needed.

In the present work, feed consumption and growth rate of pigs decline linearly and exponentially by the concentrations of AFL and linearly by the concentrations of DON. Detrimental effects of dietary ZON on growth performance of pigs are also clear. The equations provided herein may predict the effects of AFL and DON on swine production performance. Further experiments are warranted to confirm the accuracy of the models suggested in this work.

¤ To cite this article: Mok CH, Shin SY, Kim BG. Aflatoxin, deoxynivalenol, and zearalenone in swine diets: Predictions on growth performance. Rev Colomb Cienc Pecu 2013; 26:243-254.

Acknowledgements

The authors are grateful for the support by the Rural Development Administration (Suwon, Republic of Korea; PJ008405).

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