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Effects of removal of dietary polyunsaturated fatty acids on plasma extravasation and mechanical allodynia in a trigeminal neuropathic pain model.

Martin YB, Avendaño C - Mol Pain (2009)

Bottom Line: When compared with basal levels (in naive and/or sham cases), the net effect of CCI-IoN on ipsilateral extravasation was a reduction in the MD group, but an increase in the RD group, effectively neutralizing the original intergroup differences.In summary, PUFA intake reduces CAP-induced neurogenic plasma extravasation in the trigeminal territory, and their removal significantly alters the mechanical allodynia and the plasma extravasation that result from a unilateral CCI-IoN.It is likely that this "protective" effect of dietary lipids is temporary.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Anatomy, Histology & Neuroscience, Autonoma University of Madrid, Medical School, Madrid, Spain. yasmina.martin@uam.es

ABSTRACT

Background: Neuropathic pain (NP) is partially mediated by neuroinflammatory mechanisms, and also modulates local neurogenic inflammation. Dietary lipids, in particular the total amount and relative proportions of polyunsaturated fatty acids (PUFAs) of the omega-3 and omega-6 families, have been reported to modify the threshold for thermal and mechanical allodynia in the partial sciatic nerve ligation model of NP in rats. The effects of dietary lipids on other popular NP models, such as the chronic constriction injury (CCI), have not yet been examined. It is also unknown whether dietary PUFAs exert any effect on the capsaicin (CAP)-induced neurogenic inflammation under control or NP conditions. In this study we investigated these interrelated phenomena in the trigeminal territory, which has been much less explored, and for which not all data derived from limb nerves can be directly applied.

Results: We studied the effects of a CCI of the infraorbital nerve (IoN) on the development of mechanical allodynia and CAP-induced plasma extravasation in rats fed either a regular diet (RD), or a modified diet (MD) with much lower total content and omega-3:omega-6 ratio of PUFAs. In rats kept on MD, mechanical allodynia following CCI-IoN was more pronounced and developed earlier. Extravasation was substantially increased in naive rats fed MD, and displayed differential diet-depending changes one and four weeks after CCI-IoN. When compared with basal levels (in naive and/or sham cases), the net effect of CCI-IoN on ipsilateral extravasation was a reduction in the MD group, but an increase in the RD group, effectively neutralizing the original intergroup differences.

Conclusion: In summary, PUFA intake reduces CAP-induced neurogenic plasma extravasation in the trigeminal territory, and their removal significantly alters the mechanical allodynia and the plasma extravasation that result from a unilateral CCI-IoN. It is likely that this "protective" effect of dietary lipids is temporary. Also, the presence of contralateral effects of CCI-IoN precludes using the contralateral side as control.

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Diet modifies differently mechanical response thresholds. Nociceptive responses to Von Frey hairs applied to the vibrissal pads in rats fed RD or MD at pre-surgery time point and at three time intervals after a CCI-IoN performed on the left side. Data represent the mean ± SEM of n = 15 (Pre-surgery and 8 dps) and n = 9 (15 and 26 dps) animals. The unilateral constriction evoked in both diet groups a highly significant decrease in response threshold that evolved with time in the ipsilateral (p < 0.001) but not the contralateral side. Differences between diet groups were highly significant ipsilaterally to the surgery at 8 dps (* p = 0.005), and showed statistical tendency at 15 dps (p = 0.059). Side differences were significant (arrows) at all postsurgery testing times (8 dps, p = 0.008; 15 dps, p = 0.01; 26 dps, p = 0.005) in the MD group, but only at 15 dps (p = 0.04) and 26 dps (p = 0.001) in the RD group.
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Figure 1: Diet modifies differently mechanical response thresholds. Nociceptive responses to Von Frey hairs applied to the vibrissal pads in rats fed RD or MD at pre-surgery time point and at three time intervals after a CCI-IoN performed on the left side. Data represent the mean ± SEM of n = 15 (Pre-surgery and 8 dps) and n = 9 (15 and 26 dps) animals. The unilateral constriction evoked in both diet groups a highly significant decrease in response threshold that evolved with time in the ipsilateral (p < 0.001) but not the contralateral side. Differences between diet groups were highly significant ipsilaterally to the surgery at 8 dps (* p = 0.005), and showed statistical tendency at 15 dps (p = 0.059). Side differences were significant (arrows) at all postsurgery testing times (8 dps, p = 0.008; 15 dps, p = 0.01; 26 dps, p = 0.005) in the MD group, but only at 15 dps (p = 0.04) and 26 dps (p = 0.001) in the RD group.

Mentions: The baseline response threshold to mechanical stimuli was similar in both diet groups (2.25 ± 0.32 g in RD vs. 1.94 ± 0.35 g in MD, expressed as bending force needed to elicit 50% of positive responses), and exhibited a highly significant decrease after CCI on the ipsilateral (Kruskal-Wallis, p < 0.001) but not the contralateral side in both. However, this decline in threshold appeared earlier and was more pronounced in the MD group, which differed very significantly from the RD group at 8 days postsurgery (0.43 ± 0.16 g vs. 1.96 ± 0.45 g; p = 0.005). At 15 days the difference showed statistical tendency (0.22 ± 0.11 g vs. 0.61 ± 0.26 g; p = 0.059), and by 26 days after surgery a small difference was still observed (0.10 ± 0.04 g vs. 0.32 ± 0.15 g), which did not reach significance. Side comparisons for each force tested also revealed a different time course of mechanical allodynia for RD and MD groups, showing an earlier onset of higher responsiveness in rats fed MD (at day 8 postsurgery), but the same pattern of side differences in MD and RD 26 days after surgery (Fig. 1). In the right side, contralateral to the CCI, the response threshold after surgery was somewhat lower in rats fed MD compared to those fed RD, although this difference did not reach statistical significance.


Effects of removal of dietary polyunsaturated fatty acids on plasma extravasation and mechanical allodynia in a trigeminal neuropathic pain model.

Martin YB, Avendaño C - Mol Pain (2009)

Diet modifies differently mechanical response thresholds. Nociceptive responses to Von Frey hairs applied to the vibrissal pads in rats fed RD or MD at pre-surgery time point and at three time intervals after a CCI-IoN performed on the left side. Data represent the mean ± SEM of n = 15 (Pre-surgery and 8 dps) and n = 9 (15 and 26 dps) animals. The unilateral constriction evoked in both diet groups a highly significant decrease in response threshold that evolved with time in the ipsilateral (p < 0.001) but not the contralateral side. Differences between diet groups were highly significant ipsilaterally to the surgery at 8 dps (* p = 0.005), and showed statistical tendency at 15 dps (p = 0.059). Side differences were significant (arrows) at all postsurgery testing times (8 dps, p = 0.008; 15 dps, p = 0.01; 26 dps, p = 0.005) in the MD group, but only at 15 dps (p = 0.04) and 26 dps (p = 0.001) in the RD group.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2651866&req=5

Figure 1: Diet modifies differently mechanical response thresholds. Nociceptive responses to Von Frey hairs applied to the vibrissal pads in rats fed RD or MD at pre-surgery time point and at three time intervals after a CCI-IoN performed on the left side. Data represent the mean ± SEM of n = 15 (Pre-surgery and 8 dps) and n = 9 (15 and 26 dps) animals. The unilateral constriction evoked in both diet groups a highly significant decrease in response threshold that evolved with time in the ipsilateral (p < 0.001) but not the contralateral side. Differences between diet groups were highly significant ipsilaterally to the surgery at 8 dps (* p = 0.005), and showed statistical tendency at 15 dps (p = 0.059). Side differences were significant (arrows) at all postsurgery testing times (8 dps, p = 0.008; 15 dps, p = 0.01; 26 dps, p = 0.005) in the MD group, but only at 15 dps (p = 0.04) and 26 dps (p = 0.001) in the RD group.
Mentions: The baseline response threshold to mechanical stimuli was similar in both diet groups (2.25 ± 0.32 g in RD vs. 1.94 ± 0.35 g in MD, expressed as bending force needed to elicit 50% of positive responses), and exhibited a highly significant decrease after CCI on the ipsilateral (Kruskal-Wallis, p < 0.001) but not the contralateral side in both. However, this decline in threshold appeared earlier and was more pronounced in the MD group, which differed very significantly from the RD group at 8 days postsurgery (0.43 ± 0.16 g vs. 1.96 ± 0.45 g; p = 0.005). At 15 days the difference showed statistical tendency (0.22 ± 0.11 g vs. 0.61 ± 0.26 g; p = 0.059), and by 26 days after surgery a small difference was still observed (0.10 ± 0.04 g vs. 0.32 ± 0.15 g), which did not reach significance. Side comparisons for each force tested also revealed a different time course of mechanical allodynia for RD and MD groups, showing an earlier onset of higher responsiveness in rats fed MD (at day 8 postsurgery), but the same pattern of side differences in MD and RD 26 days after surgery (Fig. 1). In the right side, contralateral to the CCI, the response threshold after surgery was somewhat lower in rats fed MD compared to those fed RD, although this difference did not reach statistical significance.

Bottom Line: When compared with basal levels (in naive and/or sham cases), the net effect of CCI-IoN on ipsilateral extravasation was a reduction in the MD group, but an increase in the RD group, effectively neutralizing the original intergroup differences.In summary, PUFA intake reduces CAP-induced neurogenic plasma extravasation in the trigeminal territory, and their removal significantly alters the mechanical allodynia and the plasma extravasation that result from a unilateral CCI-IoN.It is likely that this "protective" effect of dietary lipids is temporary.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Anatomy, Histology & Neuroscience, Autonoma University of Madrid, Medical School, Madrid, Spain. yasmina.martin@uam.es

ABSTRACT

Background: Neuropathic pain (NP) is partially mediated by neuroinflammatory mechanisms, and also modulates local neurogenic inflammation. Dietary lipids, in particular the total amount and relative proportions of polyunsaturated fatty acids (PUFAs) of the omega-3 and omega-6 families, have been reported to modify the threshold for thermal and mechanical allodynia in the partial sciatic nerve ligation model of NP in rats. The effects of dietary lipids on other popular NP models, such as the chronic constriction injury (CCI), have not yet been examined. It is also unknown whether dietary PUFAs exert any effect on the capsaicin (CAP)-induced neurogenic inflammation under control or NP conditions. In this study we investigated these interrelated phenomena in the trigeminal territory, which has been much less explored, and for which not all data derived from limb nerves can be directly applied.

Results: We studied the effects of a CCI of the infraorbital nerve (IoN) on the development of mechanical allodynia and CAP-induced plasma extravasation in rats fed either a regular diet (RD), or a modified diet (MD) with much lower total content and omega-3:omega-6 ratio of PUFAs. In rats kept on MD, mechanical allodynia following CCI-IoN was more pronounced and developed earlier. Extravasation was substantially increased in naive rats fed MD, and displayed differential diet-depending changes one and four weeks after CCI-IoN. When compared with basal levels (in naive and/or sham cases), the net effect of CCI-IoN on ipsilateral extravasation was a reduction in the MD group, but an increase in the RD group, effectively neutralizing the original intergroup differences.

Conclusion: In summary, PUFA intake reduces CAP-induced neurogenic plasma extravasation in the trigeminal territory, and their removal significantly alters the mechanical allodynia and the plasma extravasation that result from a unilateral CCI-IoN. It is likely that this "protective" effect of dietary lipids is temporary. Also, the presence of contralateral effects of CCI-IoN precludes using the contralateral side as control.

Show MeSH
Related in: MedlinePlus