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Abstract
Recent findings from rodent studies suggest that high-fat diet (HFD) increases hyperalgesia independent of obesity status. Furthermore, weight loss interventions such as voluntary physical activity (PA) for adults with obesity or overweight was reported to promote pain reduction in humans with chronic pain. However, regardless of obesity status, it is not known whether HFD intake and sedentary (SED) behavior is underlies chronic pain susceptibility. Moreover, differential gene expression in the nucleus accumbens (NAc) plays a crucial role in chronic pain susceptibility. Thus, the present study used an adapted model of the inflammatory prostaglandin E2 (PGE2)-induced persistent hyperalgesia short-term (PH-ST) protocol for mice, an HFD, and a voluntary PA paradigm to test these hypotheses. Therefore, we performed an analysis of differential gene expression using a transcriptome approach of the NAc. We also applied a gene ontology enrichment tools to identify biological processes associated with chronic pain susceptibility and to investigate the interaction between the factors studied: diet (standard diet vs. HFD), physical activity behavior (SED vs. PA) and PH-ST (PGE vs. saline). Our results demonstrated that HFD intake and sedentary behavior promoted chronic pain susceptibility, which in turn was prevented by voluntary physical activity, even when the animals were fed an HFD. The transcriptome of the NAc found 2,204 differential expression genes and gene ontology enrichment analysis revealed 41 biologic processes implicated in chronic pain susceptibility. Taking these biological processes together, our results suggest that genes related to metabolic and mitochondria stress were up-regulated in the chronic pain susceptibility group (SED-HFD-PGE), whereas genes related to neuroplasticity were up-regulated in the non-chronic pain susceptibility group (PA-HFD-PGE). These findings provide pieces of evidence that HFD intake and sedentary behavior provoked gene expression changes in the NAc related to promotion of chronic pain susceptibility, whereas voluntary physical activity provoked gene expression changes in the NAc related to prevention of chronic pain susceptibility. Finally, our findings confirmed previous literature supporting the crucial role of voluntary physical activity to prevent chronic pain and suggest that low levels of voluntary physical activity would be helpful and highly recommended as a complementary treatment for those with chronic pain.
Highlights
Obesity and chronic pain are two highly prevalent conditions associated with a modern lifestyle in both developed and developing countries
Post hoc analysis revealed from the 12th to 18th weeks of age that the PA-high-fat diet (HFD) and sedentary/high-fat diet (SED-HFD) groups had significantly higher body mass when compare to the PA-standard diet (SD) and SED-SD groups (Week 12: 32.25 ± 2.72 g and 32.82 ± 3.14 g vs. 24.59 ± 1.41 g, p = 0.0001 and 24.37 ± 1.47 g, p = 0.0001; Week 18: 40.24 ± 3.71 g and 38.22 ± 3.44 g vs. 26.74 ± 1.45 g, p = 0.0001 and 26.0 ± 1.83 g, p = 0.0001, respectively) (Figure 3A)
The analysis of interaction factors of the differential gene expression in the nucleus accumbens (NAc) of the chronic pain susceptibility group (SEDHFD-PGE) and non-chronic pain susceptibility group (PAHFD-PGE) suggested that these gene expression changes may be implicated in chronic pain susceptibility
Summary
Obesity and chronic pain are two highly prevalent conditions associated with a modern lifestyle in both developed and developing countries. A cross-sectional study from low- and middle-income countries showed that sedentary behavior is strongly related to obesity and chronic pain and suggested that interventions focusing on reducing sedentary behavior should be considered for these chronic conditions (Koyanagi et al, 2018). A recent study in adults with obesity or overweight demonstrated that weight loss interventions such as voluntary physical activity promoted significant pain reduction (Cooper L. et al, 2018), adding to the known effects and growing literature relating the benefits of increased physical activity for treatment of chronic pain (Geneen et al, 2017; Lima et al, 2017a,b) and obesity (Paley and Johnson, 2016). Studies investigating the interactions between high-fat diet (HFD), sedentary behavior, voluntary physical activity in chronic pain susceptibility are limited
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