Modulation of Intestinal Functions Following Mycotoxin Ingestion: Meta-Analysis of Published Experiments in Animals
Abstract
:Abbreviations
AF | Aflatoxins |
APC | Antigen-Presenting Cell |
DON | Deoxynivalenol |
FB | Fumonisins |
FUS | Fusarium toxins |
GALT | Gut-Associated Lymphoid Tissue |
GIT | Gastrointestinal Tract |
GLUT2 | facilitated glucose transporter |
GLUT5 | fructose transporter |
IEC | Intestinal Epithelial Cell |
OTA | Ochratoxin A |
PP | Peyer’s Patches |
SGLT1 | sodium-dependent glucose cotransporter 1 |
TCT | Trichothecenes |
TEER | Transepithelial Electrical Resistance |
TJ | Tight Junction |
T-2 | T-2 toxin |
UC | Ussing Chamber |
ZEA | Zearalenone |
1. Introduction
2. Intestinal Absorption and Fate of Mycotoxins with the Gut
Nutrient digestibility | Enzyme activities | Nutrient uptake 1 | Digestive microflora | Barrier integrity | Mucosal immunity 2 | Pathogen clearance | Total 3 | ||
---|---|---|---|---|---|---|---|---|---|
Experiments | 13 | 5 | 17 | 5 | 16 | 13 | 14 | 83 | |
in vitro / ex vivo / in vivo 4 | 0/0/13 | 0/0/5 | 1/10/12 | 1/2/4 | 13/2/5 | 7/1/10 | 1/1/13 | 23/16/62 | |
Aflatoxin (AF) | 5 | 4 | 1 | 0 | 2 | 1 | 1 | 14 | |
Ochratoxin A (OTA) | 0 | 0 | 0 | 0 | 3 | 0 | 3 | 6 | |
Deoxynivalenol (DON) | 1 | 0 | 11 | 3 | 8 | 7 | 2 | 32 | |
T-2 toxin (T-2) | 0 | 0 | 1 | 1 | 0 | 0 | 3 | 5 | |
Zearalenone (ZEA) 5 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | |
Fumonisin (FB) | 2 | 1 | 2 | 1 | 2 | 4 | 2 | 14 | |
Multi-contamination | 5 | 0 | 2 | 0 | 1 | 1 | 3 | 12 | |
References | |||||||||
Aflatoxin (AF) | [17,18,19,20,21] | [17,19,22,23] | [24] | [25,26] | [27] | [28] | |||
Ochratoxin A (OTA) | [29,30,31] | [32,33,34] | |||||||
Deoxynivalenol (DON) | [35] | [36,38,39,40,41,42,43,44,45,46] | [47,48,49] | [50,51,52, 53,54,55,56,57] | [51,53,58,59,60,61,62] | [58,63] | |||
T-2 toxin (T-2) | [64] | [65] | [28,66,67] | ||||||
Fumonisin (FB) | [68,69] | [70] | [70,71] | [72] | [51,73] | [51,74,75,76] | [75,77] | ||
Multi-contamination | [21,78,79,81] | [82,83] | [51] | [51] | [84,85,86] |
Deoxynivalenol | T-2 Toxin | Zearalenone | Fumonisins | Aflatoxin | Ochratoxin A | ||
---|---|---|---|---|---|---|---|
(DON; mg/kg) | (T-2; mg/kg) | (ZEA; mg/kg) | (FB; mg/kg) | (AF; mg/kg) | (OTA; mg/kg) | ||
Realistic doses (RD) 1 | <5 | <0.5 | <1 | <10 | <0.3 | <0.3 | |
Representative of field conditions | |||||||
Occasional doses (OD) 1 | >5 | >0.5 | >1 | >10 | >0.3 | >0.3 | |
Unfavorable weather conditions | <25 | <2 | <5 | <40 | <2 | <2 | |
Unrealistic doses (UD) 1 | >25 | >2 | >5 | >40 | >2 | >2 | |
Unlikely to occur in nature | |||||||
EU Limits (EC guidance) 2 | |||||||
Pig (young) | 0.9 (0.9) | no advisory or guidance levels established | 0.25 (0.1) | 5 (5) | 0.02 | 0.05 (0.05) | |
Poultry | 5 | - | 20 | 0.02 | 0.1 | ||
Ruminant (young) | 5 (2) | 0.5 (0.5) | 50 (20) | 0.02 (0.01) | - | ||
USA Limits (FDA guidance) 3 | |||||||
Pig (young) | 1 | no advisory or guidance levels established | no advisory or guidance levels established | 10 | 0.1 (0.02) | no advisory or guidance levels established | |
Poultry (young) | 5 | 50 4 | 0.1 (0.02) | ||||
Ruminant (young) | 5 | 30 4 | 0.3 (0.02) |
3. Consequence of Mycotoxins for Nutrient Metabolism
3.1. Nutrient Digestibility and Metabolizable Energy
MYCOTOXIN CONCENTRATION IN STUDIES | |||||||
---|---|---|---|---|---|---|---|
Realistic doses | Occasional doses | Unrealistic doses | |||||
Digestive processes | |||||||
Enzyme activities | AF (hen): amlysase activity ↗ in pancreas and ↘ in duodenum, lipase activity ↘ in pancreas and duodenum, trypsin and chymotrypsin activity ↗ in pancreas [22]. | FB1 (pig): aminopeptidase activity ↘ in jejunum [70]. | |||||
AF (duck): protease, amlysase, trypsin and chymotrypsin activity ↗ in duodenum [17]. | AF (hen): disaccharidase, maltase activity ↗ in jejunum [19]. | ||||||
AF (mouse): alkaline phosphatase activity ↘ in isolated duodenal enterocytes [23]. | |||||||
Nutrient digestibility | AF (duck): reduced apparent digestibility of crude protein [17,18]. | FUS (hen): slightly depressed nutrient digestibility & metabolizable energy [78]. | |||||
FUS (dog): improved nutrient digestibility [81]. | FUS (chicken): increased protein digestibility & net protein utilization [80]. | ||||||
FB1 (pig): reduced digestibility of ether extract [68]. | FB1 (rat, pig): reduced nutrient digestibility [68,69]. | ||||||
DON (chicken): reduced intestinal viscosity [35]. | AF (chicken/hen): reduced apparent digestibility, digestible & metabolizable energy [19,20,21]. | ||||||
Absorptive processes | |||||||
Sugar transport | DON (HT-29 cells): strong inhibition of SGLT1 & | DON (chicken-hen/UCj 1): reduced Isc after glucose addition [42,43], inhibition of intestinal SGLT1 [45]. | T-2 toxin (rat/explant): reduced glucose absorption in jejunum and its rate of appearance in venous plasma [64]. | ||||
GLUT5 [44]. | FB1 (pig/UCj 1): enhanced Isc after glucose | AF (UCj 2): reduced Isc after glucose addition [24]. | |||||
DON (chicken): reduced intestinal expression of SGLT1, GLUT2 [40] & GLUT5 [46]. | addition [70]. | OTA (HT-29 cells): strong inhibition of SGLT1 [29]. | |||||
Amino-acid transport | DON (HT-29 cells): inhibition of active and passive | DON (UCj 2): reduced Isc after proline addition [41]. | |||||
L-serine transporters [44]. | |||||||
Lipid transport | DON (HT-29 cells): increase of palmitate transport [44]. | ||||||
DON (chicken): reduced expression of palmitate transporter in jejunum [46]. | |||||||
Other essential nutrients | DON (mouse/explant): reduced uptake and transfer of folate [36]. |
3.2. Digestive and Absorptive Processes
3.2.1. Activity of Digestive Enzymes
3.2.2. Morphology of Intestinal Villi
3.2.3. Nutrient Uptake
3.3. Connection between Intestinal Nutrient Metabolism and Animal Growth
4. Consequence of Mycotoxins on Intestinal Defense
4.1. Pathogen Clearance
4.1.1. Parasitic Infections
Microorganism in Contact with the Intestinal Epithelium | |||||
---|---|---|---|---|---|
Parasite | Bacteria | Virus | |||
Realistic doses 1 | |||||
FUS (chicken): impaired recovery of duodenal villi from coccidial lesions [84], upregulation of IFN-γ expression in CT [85]. | FB1 (pig): increased intestinal colonization by | ||||
E. coli [77]. | |||||
DON (porcine cells & ileal loop): enhanced | |||||
S. typhimurium invasion and translocation, potentiation of pro-inflammatory cytokines [58]. | |||||
Occasional doses 1 | |||||
FUS (chicken): delayed recruitment of CD4+ and CD8+ cells in jejunum [86]. | FB1 (pig): longer shedding of E. coli, reduction of in vivo APC maturation (MHC-II, IL-12p40), T cell stimulatory capacity, specific Ig in PP [75]. | ||||
Unrealistic doses 1 | |||||
OTA (turkey, chicken): bloody diarrhea, higher lesions and oocyst in intestine [32,33], duodenal hemorrhages [32]. | OTA (chicken): higher number of S. typhimurium in duodenum & cecum, acute enteritis [34]. | T-2 (mouse): inability to clear reovirus from intestine, increased fecal shedding of the virus, suppression of IFN-γ expression in PP [67]. | |||
DON (mouse): increased fecal shedding of reovirus, elevated intestinal virus-specific IgA, suppressed Th1 & enhanced Th2 cytokine expression [63]. |
4.1.2. Digestive Bacterial Infections
4.1.3. Enteric Viral Infections
4.2. Mucosal Immunity—Cytokine Balance
4.2.1. Deoxynivalenol (DON) Interaction with the Gut Epithelium
4.2.2. Mycotoxin Interaction with the Gut Epithelium
4.2.3. Implications
5. Consequence of Mycotoxins on Barrier Integrity
Teer | Paracellular Flux | Junction Proteins | ||||
---|---|---|---|---|---|---|
DON | (RD) | IPEC-1: reduced TEER [54]. | Caco-2: increased paracellular flux of mannitol [55]. | IPEC-J2: reduced expression of ZO-1 [50,57] and claudin 3 [50]. | ||
IPEC-J2: reduced TEER [50]. | IPEC-1: disappearance of ZO-1 [57]. | |||||
Caco-2: reduced TEER [54,55]. | Caco-2: reduced expression of claudin 4 but not occludin [55]. | |||||
Pig: reduced expression of claudin 4 in jejunum [54], occludin & | ||||||
E-cadherin in ileum [51]. | ||||||
(OD) | IPEC-1: reduced TEER [52,54,56]. | IPEC-1: increased paracellular flux of 4-kDa dextran [54,56] and pathogenic E.coli [54]. | IPEC-1: reduced expression of claudins 4 [52,54,56] & 3 but not ZO-1 and occludin [54]. | |||
Pig explant: increased paracellular flux of | ||||||
4-kDa dextran [54]. | ||||||
OTA | (UD) | Caco-2: reduced | Caco-2: increased in the paracellular flux of | Caco-2: disappearance of claudins 3 & 4 but not claudin 1 [30,31], ZO-1 and occludin [30]. | ||
TEER [29,30,31]. | 4- and 10-kDa dextrans, but not 20- and | |||||
HT-29: reduced TEER [29]. | 40-kDa dextrans [30]. | |||||
AF | (RD) | Caco-2: slightly reduced TEER [25]. | ||||
(UD) | Caco-2: reduced TEER [26]. | |||||
FB | (RD) | Pig: reduced expression of occludin & E-cadherin in ileum [51]. | ||||
(OD) | IPEC-1: reduced TEER [73]. |
6. Consequence of Mycotoxins on Intestinal Microflora
7. Conclusions
Acknowledgments
Conflict of Interest
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Grenier, B.; Applegate, T.J. Modulation of Intestinal Functions Following Mycotoxin Ingestion: Meta-Analysis of Published Experiments in Animals . Toxins 2013, 5, 396-430. https://doi.org/10.3390/toxins5020396
Grenier B, Applegate TJ. Modulation of Intestinal Functions Following Mycotoxin Ingestion: Meta-Analysis of Published Experiments in Animals . Toxins. 2013; 5(2):396-430. https://doi.org/10.3390/toxins5020396
Chicago/Turabian StyleGrenier, Bertrand, and Todd J. Applegate. 2013. "Modulation of Intestinal Functions Following Mycotoxin Ingestion: Meta-Analysis of Published Experiments in Animals " Toxins 5, no. 2: 396-430. https://doi.org/10.3390/toxins5020396