Influence of dietary fumonisin B₁ on nutrient utilization by growing pigs

F A Gbore and G N Egbunike^*

Department of Environmental Biology and Fisheries, Adekunle Ajasin University, Akungba Akoko, Ondo State, Nigeria
E-mail: dejiprecious@yahoo.com
^*Animal Physiology Laboratory, Department of Animal Science, University of Ibadan, Ibadan, Nigeria

Abstract

Twenty-four male Large White weanling pigs of 8-9 weeks of age averaging 6.94 ± 0.26kg were used to evaluate the effect of dietary fumonisin B₁ (FB₁) on nutrient digestibility by growing pigs. The animals were randomly assigned in a Completely Randomized Design to 4 diets containing 0.2, 5.0, 10.0 and 15.0mg FB₁/kg constituting the control, diets 1, 2 and 3 respectively, in a 6-month feeding trial. The feeding trial was divided into 3 physiological phases [weanling (starter), peri-pubertal (grower) and pubertal (finisher)]. The proximate chemical compositions of the experimental diets as well as the faecal samples collected from animals in each treatment during the last seven days of each physiological phase were determined using standard methods to calculate the apparent digestibility of dry matter (DM), organic matter (OM), crude protein (CP), ether extract (EE), crude fibre (CF), ash and nitrogen-free extract (NFE).

There was a significant influence of the dietary FB₁ levels on the apparent digestibility of the ether extract (EE) during the weanling phase. Animals on the control diet had significantly (P<0.05) higher apparent digestibility of EE than those on diets 1, 2 and 3 containing higher levels of dietary FB₁. The digestibility of the EE and crude protein (CP) were significantly (P<0.05) lower with increased dietary FB₁ during the peri-pubertal phase. However, the apparent digestibility values observed during the pubertal phase for animals on the control diet were generally (except for ash) higher than those on diets 1, 2 and 3 for each parameter. The significantly (P<0.05) lower values of 55.70, 57.71 and 51.27% for the apparent NFE digestibility of the animals on diets 1, 2 and 3 were only about 83.36, 86.37 and 76.73% of those on the control diet respectively.

The significantly lower nutrient digestibility by animals on diets 1, 2 and 3 suggest adverse effect of FB₁ on intestinal function in nutrient digestibility and absorption of the nutrients in animals. The study revealed that chronic ingestion of dietary FB₁ of >5.0mg kg^-1 generally reduced nutrient utilization in growing Large White pigs.

Key words: Dietary fumonisin B1, nutrient digestibility, pigs

Introduction

Under the prevalent environmental conditions in the tropics, most of the feed ingredients for ration formulation, including grains and nuts which their inclusion in balanced livestock diets are of necessity provide a favourable medium for the growth of food contaminating fungi (Ogunlade et al 2004), which according to Petzinger and Weidenbach (2000) grow on almost every kind of nourishing medium. These saprophytic and endophytic fungi produce secondary metabolites called mycotoxins, which are potential sources of toxins in feeds. The contamination of feeds and feedstuffs with mutagenic and carcinogenic mycotoxins is a major concern for animal and human health.

Mycotoxins are now virtually ubiquitous in livestock diets, causing pathological or physiological changes in animals. The effects of dietary mycotoxins vary in animals, ranging from decreased nutritive value of the feeds, poor feed conversion, reduced growth, hormonal changes to occasional organ damage or even death, depending on the type of mycotoxins. The symptoms depend on the amount of toxin in the feed, the period for which the feed is ingested and the nutritional status of the feed (Marasas and Nelson 1987).

Many species of Fusarium produce a number of mycotoxins, including fumonisin that cause different physiological and pharmacological responses in animals (Harrison et al 1990; Gelderblom et al 1991, 1994). Maize, which is the major cereal utilized in the formulation of livestock feeds has been reported (Shephard et al 1996) as the only commodity that contains significant amounts of fumonisins, and the importance of this ingredient in the food of man and his livestock cannot be overemphasized. Hence, the potential for fumonisins to be found in feeds and foodstuffs is high.

Based on the reviewed effects of fumonisins on the performance and physiology of animals, this study was designed to assess the effect of dietary fumonisin B₁ (FB₁) on nutrient digestibility and utilization by growing pigs.
 

Materials and methods

Experimental site

The feeding trial was carried out at the Physiology Unit of the Teaching and Research Farm, University of Ibadan, Ibadan, Nigeria, and further laboratory analyses carried out at the Animal Physiology Laboratory of the Department of Animal Science, University of Ibadan, Ibadan, Nigeria (7^o20’N, 3^o50’E; 200m above sea level).

Experimental diets

Fusarium verticillioides cultured maize grains to produce FB₁ was generated at the Plant Pathology Laboratory, International Institute of Tropical Agriculture (IITA), Ibadan, Nigeria, according to the method described by Nelson and Ross (1992). Ground cultured maize was substituted for autoclaved, noncultured maize in various proportions to formulate four diets containing 0.2, 5.0, 10.0 and 15.0mg FB₁/kg, as determined using fumonisin quantitative test kit (Neorgen Corp., USA), constituting diets 1 (control), 2, 3 and 4 respectively.

Experimental animals and feeding trial

After a 2-week physiological adjustment period, 24 male Large White weanling pigs of about 8 - 9 weeks of age averaging 6.94 ± 0.26kg were randomly assigned, in a completely randomized design, to the 4 diets, such that each treatment had 6 animals. The feeding trial, which lasted 6 months, was divided into 3 physiological phases [weanling (starter), peri-pubertal (grower) and pubertal (finisher)]. The animals were placed under hygienic condition throughout the feeding period. The compositions of the diets fed for 6, 10 and 8 weeks during the weanling, peri-pubertal and pubertal phases respectively are shown in Table 1, and satisfied the nutrient requirements of the animals at the various physiological phases as recommended by National Research Council (NRC 1998). The animals were fed their respective diets ad libitum daily at 0800 h and 1600 h.

Data collection

During the last seven days of each physiological phase, faecal droppings from each animal were collected, weighed, mixed and aliquots taken daily. The daily aliquots and the respective feed samples for each animal were oven-dried in an air-circulating oven at 105^oC for 24h (to determine their moisture contents) for further analyses. The chemical compositions of the experimental diets and faecal samples collected, which were used to calculate the apparent digestibility of dry matter (DM), organic matter (OM), crude protein (CP), ether extract (EE), crude fibre (CP), ash and nitrogen-free extract (NFE), were determined by the method of AOAC (1995).

Statistical analyses

The design used for this experiment is Complete Randomization Design (CRD). Data collected were subjected to statistical analysis using analysis of variance (SAS 1999). The treatment means were compared using the Duncan procedure of the same software.
 

Results

The apparent nutrient digestibilities of male weanling pigs exposed to varied dietary FB₁ levels are as shown in Table 2. There was a significant influence (P<0.05) of the dietary FB₁ levels on the apparent digestibility of the EE.

The results showed that the animals on the control diet had significantly (P<0.05) higher apparent digestibility of EE than those on diets 1, 2 and 3 containing higher levels of dietary FB₁. The apparent OM and ash digestibility tended to decrease with increased dietary FB₁, while the digestibility of NFE did not follow any particular trend.

Table 3 is a summary of the apparent nutrient digestibility of peri-pubertal male pigs exposed to varied dietary FB₁ levels.

The digestibility of the EE and CP were significantly (P<0.05) lower with increased dietary FB₁. The apparent CP digestibility was significantly (P<0.05) lower for animals fed diet 3 than for those on diet 1 and the control diet. The results revealed a concentration-dependent decline in the apparent digestibility of the DM and CP. The apparent digestibility of the OM, CF, ash and the NFE however did not follow any particular trend.

The apparent DM, OM, CP, CF, EE, ash and NFE digestibility values of pubertal boars exposed to varied levels of dietary FB₁ were significantly influenced (Table 4).

The results revealed that the apparent digestibility values observed for animals on the control diet were generally (except for ash) higher than those on diets 1, 2 and 3 for each parameter. The significantly (P<0.05) lower values of 55.70, 57.71 and 51.27% for the apparent NFE digestibility of the animals on the test diets 1, 2 and 3 were only about 83.36, 86.37 and 76.73% of those on the control diet respectively. The apparent EE digestibility, though not significantly different across the treatments, appeared to decline with increased dietary FB₁.
 

Discussion

Several biochemical modes of action have been proposed to explain all or some of the fumonisin-induced animal disease. Two of these involve disruption of lipids as initial site of action. Gelderblom et al (1996, 1997) reported that fumonisins were found to create a multitude of changes in liver cholesterol, phospholipids, sphingoid bases and free fatty acid composition. The apparent nutrient digestibility of male weanling pigs fed varied levels of dietary FB₁ in this study showed that the significantly higher apparent EE digestibility by animals fed the control diet than those on diets 1, 2 and 3 could be ascribed to the roles fumonisins play in fatty acid metabolic pathway.

Fumonisin B₁ has been reported to alter n-6 fatty acid metabolic pathway. In a long-term study (2 years), Gelderblom et al (1997) observed significant changes in lipid composition in livers from rats fed 10 and 25 mg FB₁ /kg diet. Similarly, Abel and Gelderblom (1998) reported that fumonisin treatment increased the extent of lipid peroxidation in rat (Fischer-344) liver in vivo in a concentration- and dose - dependent manner.

WHO (2000) reported that the disruption of various aspects of lipid metabolism and signal transduction pathways mediated by lipid second messengers appeared to be an important aspect of all the various proposed mechanisms of action of fumonisin. Yoo et al (1992) had shown that there is a concentration dependent association between the inhibition of sphingolipid biosynthesis and fumonisin intake, which these researchers reported to adversely influence normal epithelial morphology. This could therefore, be responsible for the generally significant lower digestibility of EE and CP by the boars fed diets 1, 2 and 3 compared with the control during the peri-pubertal feeding phase.

Nutrient digestibility, which appeared to decline with increased dietary FB₁ levels in rabbits in an 8-week feeding trial was reported by Ewuola et al (2003). Significant decline in digestibility values for all nutrients apart from the minerals, by the pubertal boars with increased dietary FB₁ suggests progressive erosion of the epithelial lining of the small intestine resulting from chronic exposure to dietary FB₁ as observed in rabbits by Ewuola et al (2003) or the adverse influence of dietary FB₁ on normal epithelial morphology observed by Yoo et al (1992). The significant differences in nutrient digestibility in pubertal boars fed varied levels of dietary FB₁ could be attributed to the toxin. Reduced intestinal tunica mucosa in rabbits fed F. verticillioides culture material containing 1.69 - 1.90mg fumonisin/kg for 8 weeks has been observed by Ewuola et al (2003).
 

Conclusions

• The significantly lower nutrient digestibility by animals on diets containing Fusarium-inoculated grains might be an indication of the roles fumonisin could play in intestinal hypofunction with respect to nutrient digestibility and subsequent absorption of the nutrients by the animals.

• Based on the findings in this study, diets containing >5.0mg FB₁ kg^-1 generally reduced nutrient utilization in growing Large White pigs.
  

References

AOAC 1995 Official Methods of Analysis. 16^th edition, Association of Official Analytical Chemists, Washington DC.

Abel S and Gelderblom W C A 1998 Oxidative damage and fumonisin B₁-induced toxicity in primary rat hepatocytes and rat liver in vivo. Toxicology 131(2-3): 121-131.

Ewuola E O, Ogunlade J T, Gbore F A , Salako A O, Idahor K O and Egbunike G N 2003 Performance evaluation and organ histology of rabbits fed Fusarium verticillioides culture material. Tropical Animal Production Investigations 6: 111 - 119.

Gelderblom W C A, Kriek N P J, Marasas W F O and Thiel P G 1991 Toxicity and carcinogenicity of the Fusarium moniliforme metabolite, fumonisin B₁, in rats. Carcinogenesis 12: 1247 - 1251.

Gelderblom W C A, Cawood M E, Snyman S D and Marasas W F O 1994 Fumonisin B₁ dosimetry in relation to cancer initiation in rat liver. Carcinogenesis 15: 209 - 214.

Gelderblom W C A, Smuts C M, Abel S, Snyman S D, Cawood M A, van der Westhuizen L and Swanevelder S 1996 Effect of fumonisin B₁ on protein and lipid synthesis in primary rat hepatocytes. Food and Chemical Toxicology 34: 361 - 369.

Gelderblom W C A, Smuts C M, Abel S, Snyman, S D, van der Westhuizen L, Huber W W and Swanevelder S 1997 Effect of fumonisin B₁ on the levels and fatty acid composition of selected lipids in rat liver, in vivo. Food and Chemical Toxicology 35: 647 - 656.

Harrison L R, Colvin B M, Greene J T, Newman L E and Cole J R Jr 1990 Pulmonary edema and hydrothorax in swine produced by fumonisin B₁, a toxic metabolite of Fusarium moniliforme. Journal of Veterinary Diagnostic Investigations 2: 217 - 221.

Marasas W F O and Nelson P E 1987 Mycotoxicology: Introduction to the Mycology, Plant pathology, Chemistry, Toxicology and Pathology of Naturally occurring Mycotoxicoses in Animals and Man. The Pennsylvania State University Press, University Park. 102pp.

National Research Council 1998 Nutrient Requirements of Swine. 10^th edition, National Academy Press, Washington DC.

Nelson P E and Ross P F 1992 Fumonisin production by Fusarium species on solid substrates Abstract 104, 106^th AOAC Annual Meeting, Cincinnati, OH., August 31- September 2.

Ogunlade J T, Gbore F A, Ewuola E O, Idahor K O, Salako A O and Egbunike G N 2004 Biochemical and haematological response of rabbits fed diets containing micro doses of fumonisin. Tropical Journal of Animal Science 7 (1) 169-176

Petzinger E and Weidenbach A 2002 Mycotoxins in the food chain: the role of ochratoxins. Livestock Production Science 76: 245 - 250

SAS 1999 SAS/STAT User's Guide. Version 8 for Windows. SAS Institute Inc., SAS Campus Drive, Cary, North Carolina, USA

Shephard G S, Thiel P G, Stockenström S and Sydenham E W 1996 Worldwide survey of fumonisin contamination of corn and corn - based products. Journal of the Association of Official Analytical Chemists 79: 671 - 687

WHO 2000 Fumonisin B₁. Environmental Health Criteria 219. World Health Organization, Geneva

Yoo H-S, Norred W P, Wang E, Merril A H Jr and Riley R T 1992 Fumonisin inhibition of de novo sphingolipid biosynthesis and cytotoxicity are correlated in LLC - PK_I cells. Toxicology and Applied Pharmacology 114: 9 - 15.