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. 2022 Jun 3;17(6):e0269131.
doi: 10.1371/journal.pone.0269131. eCollection 2022.

Heat stress modulates the disruptive effects of Eimeria maxima infection on the ileum nutrient digestibility, molecular transporters, and tissue morphology in meat-type chickens

Ahmed F A Ghareeb  1 , Gustavo H Schneiders  1 , Jennifer N Richter  1 , James C Foutz  1 , Marie C Milfort  1 , Albert L Fuller  1 , Jianmin Yuan  2 , Romdhane Rekaya  3 , Samuel E Aggrey  1
Affiliations

Heat stress modulates the disruptive effects of Eimeria maxima infection on the ileum nutrient digestibility, molecular transporters, and tissue morphology in meat-type chickens

Ahmed F A Ghareeb et al. PLoS One. .

Abstract

Eimeria (E.) maxima is one of the most pathogenic Eimeria spp persistently invading the middle jejunum and ileum, damaging the intestinal mucosa of chickens. Heat stress (HS) is a common stressor and equally contributes to inflammation and oxidative stress. We investigated the effect of E. maxima infection and HS on ileal digestibility, mRNA expression of nutrient transporters, and ileal tissue morphology in broiler chickens. There were four treatment groups: thermoneutral control (TNc), thermoneutral infected (TNi), heat stress control (HSc), and heat stress infected (HSi), 6 replicates each of 10 birds per treatment. Chickens were fed a diet containing 0.2% TiO2. At 6-day-post infection, ileal content and tissue were collected to quantify ileal digestibility of crude protein and fat, mRNA levels of nutrient transporters and histopathology. Growth and feed intake were reduced in all treatment groups, compared with the TNc. Contrary to expectation, the combination of two major stressors (E. maxima and HS) in the TNi group exhibited almost normal digestibility while only the TNi birds expressed severe digestibility depression, compared with the TNc group. The TNi group showed the lowest mRNA expression of the transporters: SGLT1, GLUT2-5-8-10-12, FABP1-2-6, and PEPT1 compared with the other treatment groups. The expression of the absorptive enterocytes' gene markers (ACSL5, IAP, and SGLT1) supported by the ileal tissue morphology indicated that the TNi group had the highest enterocytic destruction. The expression of oxidative genes (iNOS and CYBB) dramatically increased only in the TNi group compared with the other treatment groups. Our results showed that exposing broiler chickens to HS can mitigate the disruptive effect of E. maxima on the ileal digestibility and absorption by limiting the parasite-induced tissue injury and suppressing the enterocytic inducible oxidative damage.

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Conflict of interest statement

The authors have declared that no competing interests exist.

Figures

Fig 1
Fig 1. Cloacal temperature.
Cloacal temperature of chickens infected with E. maxima and their uninfected controls that are raised in a thermoneutral or heat stress environment: TNc = thermoneutral control, TNi = thermoneutral infected, HSc = heat stress control, HSi = heat stress infected. Significant differences (p < 0.05) were depicted by different letters. The error bars represent the SEM.
Fig 2
Fig 2. Chickens’ growth, feed intake, and FCR.
The average body weight at 4, 5, 6, 7, and 14 dpi (A), feed intake at 7 and 14 dpi (B), and feed conversion ratio (FCR) at 7 and 14 dpi (C) of chickens infected with E. maxima and their uninfected controls that are raised in a thermoneutral or heat stress environment: TNc = thermoneutral control, TNi = thermoneutral infected, HSc = heat stress control, HSi = heat stress infected. Significant differences (p < 0.05) were depicted by different letters. The error bars represent the SEM.
Fig 3
Fig 3. Chickens’ ileal crude protein and fat digestibility.
The crude protein and crude fat apparent ileal digestibility at 6 dpi of chickens infected with E. maxima and their uninfected controls that are raised in a thermoneutral or heat stress environment: TNc = thermoneutral control, TNi = thermoneutral infected, HSc = heat stress control, HSi = heat stress infected. Significant differences (p < 0.05) were depicted by different letters. The error bars represent the SEM.
Fig 4
Fig 4. The mRNA expression of the ileal hexose transporters.
The mRNA fold expression of the ileal hexose transporters at 6 dpi of chickens infected with E. maxima and their uninfected controls that are raised in a thermoneutral or heat stress environment: TNc = thermoneutral control, TNi = thermoneutral infected, HSc = heat stress control, HSi = heat stress infected. Significant differences (p < 0.05) were depicted by different letters. The error bars represent the SEM.
Fig 5
Fig 5. The mRNA expression of the ileal fatty acid transporters.
The mRNA fold expression of the ileal fatty acid transporters at 6 dpi of chickens infected with E. maxima and their uninfected controls that are raised in a thermoneutral or heat stress environment: TNc = thermoneutral control, TNi = thermoneutral infected, HSc = heat stress control, HSi = heat stress infected. Significant differences (p < 0.05) were depicted by different letters. The error bars represent the SEM.
Fig 6
Fig 6. The mRNA expression of the ileal peptide transporters.
The mRNA fold expression of the ileal peptide transporters at 6 dpi of chickens infected with E. maxima and their uninfected controls that are raised in a thermoneutral or heat stress environment: TNc = thermoneutral control, TNi = thermoneutral infected, HSc = heat stress control, HSi = heat stress infected. Significant differences (p < 0.05) were depicted by different letters. The error bars represent the SEM.
Fig 7
Fig 7. The mRNA expression of the ileal villus absorptive enterocytes’ marker genes.
The mRNA fold expression of marker genes specific for ileal villus absorptive enterocytes at 6 dpi of chickens infected with E. maxima and their uninfected controls that are raised in a thermoneutral or heat stress environment: TNc = thermoneutral control, TNi = thermoneutral infected, HSc = heat stress control, HSi = heat stress infected. Significant differences (p < 0.05) were depicted by different letters. The error bars represent the SEM.
Fig 8
Fig 8. The ileal histopathology and morphological parameters.
The histopathology picture: Photomicrograph of ileum tissue stained with hematoxylin and eosin (H&E), at 100x magnification, of TNc (A), TNi (B), HSc (C), and HSi (D); the villus height (E); the crypt depth (F); the villus height to crypt depth ratio (G); at 6 dpi of chickens infected with E. maxima and their uninfected controls that are raised in thermoneutral or heat stress environment: TNc = thermoneutral control, TNi = thermoneutral infected, HSc = heat stress control, HSi = heat stress infected. Significant differences (p < 0.05) were depicted by different letters. The error bars represent the SEM. The ileum histological components were illustrated (A). The arrow heads point the E. maxima stages (B, D) gametocytes (black arrow heads) and schizonts (green arrowheads).
Fig 9
Fig 9. The mRNA expression of ileum tissue oxidative gene.
The mRNA fold expression of ileum tissue oxidative genes iNOS (A) and CYBB (B) at 6 dpi of chickens infected with E. maxima and their uninfected controls that are raised in a thermoneutral or heat stress environment: TNc = thermoneutral control, TNi = thermoneutral infected, HSc = heat stress control, HSi = heat stress infected. Significant differences (p < 0.05) were depicted by different letters. The error bars represent the SEM.
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