Jump to ContentJump to Main Navigation
Show Summary Details
More options …
New at De Gruyter

Scandinavian Journal of Pain

Official Journal of the Scandinavian Association for the Study of Pain

Editor-in-Chief: Breivik, Harald

4 Issues per year


CiteScore 2017: 0.84

SCImago Journal Rank (SJR) 2017: 0.401
Source Normalized Impact per Paper (SNIP) 2017: 0.452

Online
ISSN
1877-8879
See all formats and pricing
More options …
Volume 17, Issue 1

The impact of the Standard American Diet in rats: Effects on behavior, physiology and recovery from inflammatory injury

Stacie K. Totsch / Tammie L. Quinn / Larissa J. Strath / Laura J. McMeekin / Rita M. Cowell / Barbara A. Gower / Robert E. Sorge
Published Online: 2017-10-01 | DOI: https://doi.org/10.1016/j.sjpain.2017.08.009

Abstract

Background and aims

Obesity is a significant health concern in the Western world and the presence of comorbid conditions suggests an interaction. The overlapping distributions of chronic pain populations and obesity suggests that an interaction may exist. Poor quality diet (high carbohydrates, saturated fats, omega-6 polyunsaturated fatty acids) can lead to increased adiposity which can activate immune cells independent of the activating effect of the diet components themselves. This dual action can contribute to chronic inflammation that may alter susceptibility to chronic pain and prolong recovery from injury. However, traditional examinations of diet focus on high-fat diets that often contain a single source of fat, that is not reflective of an American diet. Thus, we examined the impact of a novel human-relevant (high-carbohydrate) American diet on measures of pain and inflammation in rats, as well as the effect on recovery and immune cell activation.

Methods

We developed a novel, human-relevant Standard American Diet (SAD) to better model the kilocalorie levels and nutrient sources in an American population. Male and female rats were fed the SAD over the course of 20 weeks prior to persistent inflammatory pain induction with Complete Freund’s Adjuvant (CFA). Mechanical and thermal sensitivity were measured weekly. Spontaneous pain, open field locomotion and blood glucose levels were measured during diet consumption. Body composition was assessed at 20 weeks. Following full recovery from CFA-induced hypersensitivity, blood was analyzed for inflammatory mediators and spinal cords were immunohistochemically processed for microglial markers.

Results

Chronic consumption of the SAD increased fat mass, decreased lean mass and reduce bone mineral density. SAD-fed rats had increased leptin levels and pro-inflammatory cytokines in peripheral blood serum. Following CFA administration, mechanical sensitivity was assessed and recovery was delayed significantly in SAD-fed animals. Sex differences in the impact of the SAD were also observed. The SAD increased body weight and common T-cell related inflammatory mediators in female, but not male, animals. In males, the SAD had a greater effect on bone mineral density and body composition. Long-term consumption of the SAD resulted in elevated microglial staining in the dorsal horn of the spinal cord, but no sex differences were observed.

Conclusions

We demonstrate the negative effects of an American diet on physiology, behavior and recovery from injury. SAD consumption elevated pro-inflammatory mediators and increased microglial activation in the spinal cord. While there were sex differences in weight gain and inflammation, both sexes showed prolonged recovery from injury.

Implications

These data suggest that poor quality diet may increase susceptibility to chronic pain due to persistent peripheral and central immune system activation. Furthermore, consumption of a diet that is high in carbohydrates and omega-6 polyunsaturated fatty acid is likely to lead to protracted recovery following trauma or surgical procedures. These data suggest that recovery of a number of patients eating a poor quality diet may be expedited with a change in diet to one that is healthier.

Keywords: Diet; Pain; Inflammation; Sex differences; Recovery

References

  • [1]

    McCarthy LH, Bigal ME, Katz M, Derby C, Lipton RB. Chronic pain and obesity in elderly people: results from the Einstein aging study. J Am Geriatr Soc 2009;57:115–9, http://dx.doi.org/10.1111/j.1532-5415.2008.02089.x. PMID: 19054178; PMCID: 2763486.CrossrefPubMed

  • [2]

    Narouze S, Souzdalnitski D. Obesity and chronic pain: systematic review of prevalence and implications for pain practice. Reg Anesth Pain Med 2015;40:91–111, http://dx.doi.org/10.1097/AAP.0000000000000218. PMID: 25650632.PubMedCrossref

  • [3]

    Smuck M, Kao MC, Brar N, Martinez-Ith A, Choi J, Tomkins-Lane CC. Does physical activity influence the relationship between low back pain and obesity? Spine J 2014;14:209–16, http://dx.doi.org/10.1016/j.spinee.2013.11.010. PMID: 24239800.CrossrefPubMed

  • [4]

    Stone AA, Broderick JE. Obesity and pain are associated in the United States. Obesity 2012;20:1491–5, http://dx.doi.org/10.1038/oby.2011.397. PMID: 22262163.Crossref

  • [5]

    Janke EA, Collins A, Kozak AT. Overview of the relationship between pain and obesity: what do we know? Where do we go next? J Rehabil Res Dev 2007;44:245–62. PMID: 17551876.CrossrefPubMedGoogle Scholar

  • [6]

    Sibille KT, Steingrimsdottir OA, Fillingim RB, Stubhaug A, Schirmer H, Chen H, McEwen BS, Nielsen CS. Investigating the burden of chronic pain: an inflammatory and metabolic composite. Pain Res Manag 2016;2016:7657329, http://dx.doi.org/10.1155/2016/7657329. PMID: 27445627; PMCID:PMC4909918.PubMed

  • [7]

    Beggs S, Salter MW. Microglia-neuronal signalling in neuropathic pain hypersensitivity 2. 0.Curr Opin Neurobiol 2010;20:474–80, http://dx.doi.org/10.1016/j.conb.2010.08.005. PMID: 20817512; PMCID:3589562.Crossref

  • [8]

    Beggs S, Salter MW. The known knowns of microglia-neuronal signalling in neuropathic pain. Neurosci Lett 2013;557(Pt A):37-42, http://dx.doi.org/10.1016/j.neuIet.2013.08.037. PMID: 23994389.CrossrefPubMed

  • [9]

    Grace PM, Hutchinson MR, Maier SF, Watkins LR. Pathological pain and the neuroimmune interface. Nat Rev Immunol 2014;14:217–31, http://dx.doi.org/10.1038/nri3621. PMID: 24577438.CrossrefPubMed

  • [10]

    Sorge RE, LaCroix-Fralish ML, Tuttle AH, Sotocinal SG, Austin JS, Ritchie J, Chanda ML, Graham AC, Topham L, Beggs S, Salter MW, Mogil JS. Spinal cord Toll-like receptor 4 mediates inflammatory and neuropathic hypersensitivity in male but not female mice. J Neurosci 2011;31:15450–4, http://dx.doi.org/10.1523/JNEUROSCI.3859-11.2011. PMID: 22031891; PMCID: 3218430.PubMedCrossref

  • [11]

    Sorge RE, Mapplebeck JC, Rosen S, Beggs S, Taves S, Alexander JK, Martin LJ, Austin JS, Sotocinal SG, Chen D, Yang M, Shi XQ, Huang H, Pillon NJ, Bilan PJ, Tu Y, Klip A, Ji RR, Zhang J, Salter MW, Mogil JS. Different immune cells mediate mechanical pain hypersensitivity in male and female mice. Nat Neurosci 2015, http://dx.doi.org/10.1038/nn.4053. PMID: 26120961.PubMed

  • [12]

    Trang T, Beggs S, Salter MW. ATP receptors gate microglia signaling in neuropathic pain. Exp Neurol 2012;234:354–61, http://dx.doi.org/10.1016/j.expneurol.2011.11.012. PMID: 22116040; PMCID: 3748033.CrossrefPubMed

  • [13]

    Watkins LR, Maier SF. Glia: a novel drug discovery target for clinical pain. Nat Rev Drug Discov 2003;2:973–85, http://dx.doi.org/10.1038/nrd1251. PMID: 14654796.Crossref

  • [14]

    Watkins LR, Milligan ED, Maier SF. Glial activation: a driving force for pathological pain. Trends Neurosci 2001;24:450–5. PMID: 11476884.CrossrefPubMedGoogle Scholar

  • [15]

    Lee JY, Sohn KH, Rhee SH, Hwang D. Saturated fatty acids, but not unsaturated fatty acids, induce the expression of cyclooxygenase-2 mediated through Toll-like receptor 4. J Biol Chem 2001;276:16683–9, http://dx.doi.org/10.1074/jbc.M011695200. PMID: 11278967.PubMedCrossref

  • [16]

    Milanski M, Degasperi G, Coope A, Morari J, Denis R, Cintra DE, Tsukumo DM, Anhe G, Amaral ME, Takahashi HK, Curi R, Oliveira HC, Carvalheira JB, Bordin S, Saad MJ, Velloso LA. Saturated fatty acids produce an inflammatory response predominantly through the activation of TLR4 signaling in hypothalamus: implications forthe pathogenesis of obesity. J Neurosci 2009;29:359–70, http://dx.doi.org/10.1523/JNEUROSCI.2760-08.2009. PMID: 19144836.Crossref

  • [17]

    Calder PC. Polyunsaturated fatty acids and inflammatory processes: new twists in an old tale. Biochimie 2009;91:791–5, http://dx.doi.org/10.1016/j.biochi.2009.01.008. PMID: 19455748.Crossref

  • [18]

    Ceriello A. Postprandial hyperglycemia and diabetes complications: is it time to treat? Diabetes 2005;54:1–7. PMID: 15616004.CrossrefPubMedGoogle Scholar

  • [19]

    Levitan EB, Cook NR, Stampfer MJ, Ridker PM, Rexrode KM, Buring JE, Manson JE, Liu S. Dietary glycemic index, dietary glycemic load, blood lipids, and C-reactive protein. Metabolism 2008;57:437–43, http://dx.doi.org/10.1016/j.metabol.2007.11.002. PMID: 18249220; PMCID: 2262400.CrossrefPubMed

  • [20]

    Liu S, Manson JE, Buring JE, Stampfer MJ, Willett WC, Ridker PM. Relation between a diet with a high glycemic load and plasma concentrations of high-sensitivity C-reactive protein in middle-aged women. Am J Clin Nutr 2002;75:492–8. PM1D: 11864854.CrossrefPubMedGoogle Scholar

  • [21]

    Kintscher U, Hartge M, Hess K, Foryst-Ludwig A, Clemenz M, Wabitsch M, Fischer-Posovszky P, Barth TF, Dragun D, Skurk T, Hauner H, Bluher M, Unger T, Wolf AM, Knippschild U, Hombach V, Marx N. T-lymphocyte infiltration in visceral adipose tissue: a primary event in adipose tissue inflammation and the development of obesity-mediated insulin resistance. Arterioscler Thromb Vasc Biol 2008;28:1304–10, http://dx.doi.org/10.1161/ATVBAHA.108.165100. PM1D: 18420999.PubMedCrossref

  • [22]

    Rocha VZ, Folco EJ, Sukhova G, Shimizu K, Gotsman L, Vernon AH, Libby P. 1nterferon-gamma, a Th1 cytokine, regulates fat inflammation: a role for adaptive immunity in obesity. Circ Res 2008;103:467–76, http://dx.doi.org/10.1161/C1RCRESAHA.108.177105. PMID: 18658050; PMCID: 2740384.PubMedCrossref

  • [23]

    Fernandez-Riejos P, Najib S, Santos-Alvarez J, Martin-Romero C, Perez-Perez A, Gonzalez-Yanes C, Sanchez-Margalet V. Role of leptin in the activation of immune cells. Mediators 1nflamm 2010;2010:568343, http://dx.doi.org/10.1155/2010/568343. PMID: 20368778; PMCID: 2846344.

  • [24]

    Fisher G, Hyatt TC, Hunter GR, Oster RA, Desmond RA, Gower BA. Markers of inflammation and fat distribution following weight loss in African-American and white women. Obesity 2012;20:715–20, http://dx.doi.org/10.1038/oby.2011.85. PMID: 21527894; PMCID: 3687549.Crossref

  • [25]

    Fontana L, Eagon JC, Trujillo ME, Scherer PE, Klein S. Visceral fat adipokine secretion is associated with systemic inflammation in obese humans. Diabetes 2007;56:1010–3, http://dx.doi.org/10.2337/db06-1656. PMID: 17287468.PubMedCrossref

  • [26]

    Verdam FJ, Fuentes S, deJonge C, Zoetendal EG, Erbil R, Greve JW, Buurman WA, de Vos WM, Rensen SS. Human intestinal microbiota composition is associated with local and systemic inflammation in obesity. Obesity 2013;21:E607-15, http://dx.doi.org/10.1002/oby.20466. PMID: 23526699.Crossref

  • [27]

    Wellen KE, Hotamisligil GS. Obesity-induced inflammatory changes in adipose tissue. J Clin Investig 2003;112:1785–8, http://dx.doi.org/10.1172/JC120514. PMID: 14679172; PMCID: 297006.Crossref

  • [28]

    Buckman LB, Hasty AH, Flaherty DK, Buckman CT, Thompson MM, Matlock BK, Weller K, Ellacott KL. Obesity induced by a high-fat diet is associated with increased immune cell entry into the central nervous system. Brain Behav 1mmun 2014;35:33–42, http://dx.doi.org/10.1016/j.bbi.2013.06.007. PMID: 23831150; PMCID:3858467.Crossref

  • [29]

    De Souza CT, Araujo EP, Bordin S, Ashimine R, Zollner RL, Boschero AC, Saad MJ, Velloso LA. Consumption of a fat-rich diet activates a proinflammatory response and induces insulin resistance in the hypothalamus. Endocrinology 2005;146:4192–9, http://dx.doi.org/10.1210/en.2004-1520. PMID: 16002529.PubMedCrossref

  • [30]

    Maysami S, Haley MJ, Gorenkova N, Krishnan S, McColl BW, Lawrence CB. Prolonged diet-induced obesity in mice modifies the inflammatory response and leads to worse outcome after stroke. J Neuroinflammation 2015;12:140, http://dx.doi.org/10.1186/s12974-015-0359-8. PMID: 26239227; PMCID: 4524371.PubMed

  • [31]

    Pohl J, Luheshi GN, Woodside B. Effect of obesity on the acute inflammatory response in pregnant and cycling female rats. J Neuroendocrinol 2013;25:433–45, http://dx.doi.org/10.1111/jne.12023. PMID: 23331909.PubMedCrossref

  • [32]

    Pohl J, Sheppard M, Luheshi GN, Woodside B. Diet-induced weight gain produces a graded increase in behavioral responses to an acute immune challenge. Brain Behav 1mmun 2014;35:43–50, http://dx.doi.org/10.1016Zj.bbi.2013.09.002. PMID: 24026015.Crossref

  • [33]

    Sampey BP, Vanhoose AM, Winfield HM, Freemerman AJ, Muehlbauer MJ, Fueger PT, Newgard CB, Makowski L. Cafeteria diet is a robust model of human metabolic syndrome with liver and adipose inflammation: comparison to high fat diet. Obesity 2011;19:1109–17, http://dx.doi.org/10.1038/oby.2011.18. PMID: 21331068; PMCID: 3130193.Crossref

  • [34]

    Totsch SK, Waite ME, Tomkovich A, Quinn TL, Gower BA, Sorge RE. Total western diet alters mechanical and thermal sensitivity and prolongs hypersensitivity following Complete Freund’s Adjuvant in mice. J Pain 2016;17:119–25, http://dx.doi.org/10.1016/jjpain.2015.10.006. PMID: 26597348.PubMedCrossref

  • [35]

    Last AR, Wilson SA. Low-carbohydrate diets. Am Fam Physician 2006;73:1942–8. PMID: 16770923.PubMedGoogle Scholar

  • [36]

    Daniel CR, McCullough ML, Patel RC, Jacobs EJ, Flanders WD, Thun MJ, Calle EE. Dietary intake of omega-6 and omega-3 fatty acids and risk of colorectal cancer in a prospective cohort of U. S.men and women. Cancer Epidemiol Biomarkers Prev 2009;18:516–25, http://dx.doi.org/10.1158/1055-9965.EP1-08-0750. PMID: 19190143.Crossref

  • [37]

    Allison DB, Egan SK, Barraj LM, Caughman C, Infante M, Heimbach JT. Estimated intakes of trans fatty and other fatty acids in the US population. J Am Diet Assoc 1999;99:166–74, http://dx.doi.org/10.1016/S0002-8223(99)00041-3,quiz756. PMID: 9972183.PubMedCrossref

  • [38]

    Hintze KJ, Benninghoff AD, Ward RE. Formulation of the Total Western Diet (TWD) as a basal diet for rodent cancer studies. J Agric Food Chem 2012;60:6736–42, http://dx.doi.org/10.1021/jf204509a. PMID: 22224871.PubMedCrossref

  • [39]

    Dixon WJ. Staircase bioassay: the up-and-down method. Neurosci Biobehav Rev 1991;15:47–50. PMID: 2052197.CrossrefPubMedGoogle Scholar

  • [40]

    Hargreaves K, Dubner R, Brown F, Flores C, Joris J. A new and sensitive method for measuring thermal nociception in cutaneous hyperalgesia. Pain 1988;32:77–88. PMID: 3340425.PubMedCrossrefGoogle Scholar

  • [41]

    Sotocinal SG, Sorge RE, Zaloum A, Tuttle AH, Martin LJ, Wieskopf JS, Mapplebeck JC, Wei P, Zhan S, Zhang S, McDougall JJ, King OD, Mogil JS. The Rat Grimace Scale: a partially automated method for quantifying pain in the laboratory rat via facial expressions. Mol Pain 2011;7:55, http://dx.doi.org/10.1186/1744-8069-7-55. PMID: 21801409; PMCID: 3163602.

  • [42]

    Toblin RL, Mack KA, Perveen G, Paulozzi LJ. A population-based survey of chronic pain and its treatment with prescription drugs. Pain 2011;152:1249–55, http://dx.doi.org/10.1016/j.pain.2010.12.036. PMID:21397401.PubMedCrossref

  • [43]

    Andorsen OF, Ahmed LA, Emaus N, Klouman E. A prospective cohort study on risk factors of musculoskeletal complaints (pain and/or stiffness) in a general population.The Tromso study. PLOS ONE 2017;12:e0181417, http://dx.doi.org/10.1371/journal.pone.0181417. PMID: 28727753; PMCID: PMC5519093.Crossref

  • [44]

    Schistad E, Stubhaug A, Furberg AS, Engdahl BL, Nielsen CS. C-reactive protein and cold-pressor tolerance in the general population: the Tromso Study. Pain 2017;158:1280–8, http://dx.doi.org/10.1097/j.pain.0000000000000912. PMID: 28420008.CrossrefPubMed

  • [45]

    Amengual-Cladera E, Llado L, Gianotti M, Proenza AM. Sex differences in the effect of high-fat diet feeding on rat white adipose tissue mitochondrial function and insulin sensitivity. Metabolism 2012;61:1108–17, http://dx.doi.org/10.1016/j.metabol.2011.12.016. PMID: 22401878.CrossrefPubMed

  • [46]

    Junior F, Cardoso JR, Christofaro DG, Codogno JS, de Moraes AC, Fernandes RA. The relationship between visceral fat thickness and bone mineral density in sedentary obese children and adolescents. BMC Pediatr 2013;13:37, http://dx.doi.org/10.1186/1471-2431-13-37. PMID: 23510224; PMCID: 3606829.PubMed

  • [47]

    Hardy R, Cooper MS. Bone loss in inflammatory disorders. J Endocrinol 2009;201:309–20, http://dx.doi.org/10.1677/JOE-08-0568. PMID: 19443863.CrossrefPubMed

  • [48]

    Agrawal S, Gollapudi S, Su H, Gupta S. Leptin activates human B cells to secrete TNF-alpha, 1L-6, and 1L-10 via JAK2/STAT3 and p38MAPK/ERK1/2 signaling pathway. J Clin Immunol 2011;31:472–8, http://dx.doi.org/10.1007/s10875-010-9507-1. PMID: 21243519; PMCID: 3132280.Crossref

  • [49]

    Woolf CJ, Allchorne A, Safieh-Garabedian B, Poole S. Cytokines, nerve growth factor and inflammatory hyperalgesia: the contribution of tumour necrosis factor alpha. Br J Pharmacol 1997;121:417–24, http://dx.doi.org/10.1038/sj.bjp.0701148. PMID: 9179382; PMCID: 1564704.PubMedCrossref

  • [50]

    Richter F, Natura G, Loser S, Schmidt K, Viisanen H, Schaible HG. Tumor necrosis factor causes persistent sensitization of joint nociceptors to mechanical stimuli in rats. Arthritis Rheum 2010;62:3806–14, http://dx.doi.org/10.1002/art.27715. PMID: 20722011.CrossrefPubMed

  • [51]

    Stoll G, Jung S, Jander S, van der Meide P, Hartung HP. Tumor necrosis factoralpha in immune-mediated demyelination and Wallerian degeneration of the rat peripheral nervous system. J Neuroimmunol 1993;45:175–82. PMID: 8331160.CrossrefGoogle Scholar

  • [52]

    Thaler JP, Yi CX, Schur EA, Guyenet SJ, Hwang BH, Dietrich MO, Zhao X, Sarruf DA, Lzgur V, Maravilla KR, Nguyen HT, Fischer JD, Matsen ME, Wisse BE, Morton GJ, Horvath TL, Baskin DG, Tschop MH, Schwartz MW. Obesity is associated with hypothalamic injury in rodents and humans. J Clin 1nvestig 2012;122:153–62, http://dx.doi.org/10.1172/JC159660. PMID: 22201683; PMCID: 3248304.Crossref

  • [53]

    Tran DQ, Tse EK, Kim MH, Belsham DD. Diet-induced cellular neuroinflammation in the hypothalamus: Mechanistic insights from investigation of neurons and microglia. Mol Cell Endocrinol 2016;438:18–26, http://dx.doi.org/10.1016/j.mce.2016.05.015. PMID: 27208620.CrossrefPubMed

  • [54]

    Valdearcos M, Robblee MM, Benjamin DL, Nomura DK, Xu AW, Koli-wad SK. Microglia dictate the impact of saturated fat consumption on hypothalamic inflammation and neuronal function. Cell Rep 2014;9:2124–38, http://dx.doi.org/10.1016/j.celrep.2014.11.018. PMID: 25497089.PubMedCrossref

  • [55]

    Taves S, Berta T, Liu DL, Gan S, Chen G, Kim YH, Van de Ven T, Laufer S, Ji RR. Spinal inhibition of p38 MAP kinase reduces inflammatory and neuropathic pain in male but not female mice: sex-dependent microglial signaling in the spinal cord. Brain Behav 1mmun 2015, http://dx.doi.org/10.1016/j.bbi.2015.10.006. PMID: 26472019.

  • [56]

    Ferrari LF, Gear RW, Levine JD. Attenuation of activity in an endogenous analgesia circuit by ongoing pain in the rat. J Neurosci 2010;30:13699–706, http://dx.doi.org/10.1523/JNEUROSC1.2867-10.2010. PMID:20943910; PMCID: 2970511.Crossref

  • [57]

    Kim JY, Tillu DV, Quinn TL, Mejia GL, Shy A, Asiedu MN, Murad E, Schumann AP, Totsch SK, Sorge RE, Mantyh PW, Dussor G, Price TJ. Spinal dopaminergic projections control the transition to pathological pain plasticity via a D1/D5-mediated mechanism. J Neurosci 2015;35:6307–17, http://dx.doi.org/10.1523/JNEUROSC1.3481-14.2015. PMID:25904784.Crossref

  • [58]

    Reichling DB, Levine JD. Critical role of nociceptor plasticity in chronic pain. Trends Neurosci 2009;32:611–8, http://dx.doi.org/10.1016/j.tins.2009.07.007. PMID:19781793;PMCID:2787756.CrossrefPubMed

About the article

1300 University Blvd, CH 415, Birmingham, AL 35294, USA


Received: 2017-04-24

Revised: 2017-08-23

Accepted: 2017-08-24

Published Online: 2017-10-01

Published in Print: 2017-10-01


Author contributions:RES and SKT designed the experiments, SKT tested the animals, SKT and TLQ performed the blood testing and specimen collection. RES, SKT and BAG designed the SAD with the assistance of Dr. Tina Herfel (Envigo). BAG oversaw the blood analysis. RMC and LM ran the immunohistochemistry, TLQimaged the slides, TLQ and LJS performed quantification. RES and SKT wrote the manuscript.

Funding sources:This study was supported by an Early Career Research Grant to RES from the International Association for the Study of Pain.

Ethical issues:None.

Conflict of interest:The authors report no real or perceived conflicts of interest.


Citation Information: Scandinavian Journal of Pain, Volume 17, Issue 1, Pages 316–324, ISSN (Online) 1877-8879, ISSN (Print) 1877-8860, DOI: https://doi.org/10.1016/j.sjpain.2017.08.009.

Export Citation

© 2017 Scandinavian Association for the Study of Pain.Get Permission

Citing Articles

Here you can find all Crossref-listed publications in which this article is cited. If you would like to receive automatic email messages as soon as this article is cited in other publications, simply activate the “Citation Alert” on the top of this page.

[1]
S.K. Totsch, R.Y. Meir, R.M. Orlandella, L.A. Norian, and R.E. Sorge
Physiology & Behavior, 2018
[2]
Trevor Kirby and Javier Ochoa-Repáraz
Medical Sciences, 2018, Volume 6, Number 3, Page 69
[3]
Zongbin Song, Wenrui Xie, Judith A. Strong, Temugin Berta, Yvonne M. Ulrich-Lai, Qulian Guo, and Jun-Ming Zhang
PAIN, 2018, Volume 159, Number 9, Page 1731
[4]
S.K. Totsch, R.Y. Meir, T.L. Quinn, S.A. Lopez, B.A. Gower, and R.E. Sorge
European Journal of Pain, 2018

Comments (0)

Please log in or register to comment.
Log in