The “Wear and Tear” of the Organism in Temporomandibular Disorders: A Pilot Study Investigating the Effects of Allostatic Load on Heart Rate Variability and Inhibitory Control
Abstract
:1. Introduction
2. Materials and Methods
2.1. Participants
2.2. Measures
2.2.1. Pain Intensity
2.2.2. Heart Rate Variability
2.2.3. Cognitive Measures
Stroop Task
Go/No-Go Task
2.3. Procedure
2.4. Data Analysis
3. Results
3.1. Descriptive Statistics
n = 29 | TMD (n = 14) | Control (n = 15) | t | p | ||
---|---|---|---|---|---|---|
n | M (SD) | n | M (SD) | |||
Sex (F/M) | 11/3 | 12/3 | ||||
Age | 42 (13.82) | 41.53 (12.42) | ||||
HRV measures 1 | ||||||
SDNN | 3.39 (0.351) | 3.59 (0.405) | −1.309 | 0.102 | ||
RMSSD | 2.99 (0.412) | 3.36 (0.500) | −2.055 | 0.026 * | ||
HF | 4.80 (0.944) | 5.75 (0.929) | −2.743 | 0.005 ** | ||
Cognitive performance 2 | ||||||
Stroop Effect | 75.498 (74.462) | 72.261 (34.413) | 0.152 | 0.880 | ||
Go/No-Go—False Alarms | 2.64 (4.534) | 3.54 (2.989) | −0.601 | 0.553 | ||
Pain Intensity | ||||||
NRS | 2.44 (3.16) |
3.2. t-Test for Independent Samples: HRV Measurements
3.3. t-Test for Independent Samples: Inhibition Measurements
3.4. Correlations between Age and HRV Indices
3.5. Regression Model
4. Discussion
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Greene, C.S.; Obrez, A. Treating temporomandibular disorders with permanent mandibular repositioning: Is it medically necessary? Oral Surg. Oral Med. Oral Pathol. Oral Radiol. 2015, 119, 489–498. [Google Scholar] [CrossRef] [PubMed]
- Okeson, J.P.; de Leeuw, R. Differential Diagnosis of Temporomandibular Disorders and Other Orofacial Pain Disorders. Dent. Clin. N. Am. 2011, 55, 105–120. [Google Scholar] [CrossRef] [PubMed]
- Durham, J.; Newton-John, T.R.O.; Zakrzewska, J.M. Temporomandibular disorders. BMJ 2015, 350, h1154. [Google Scholar] [CrossRef] [PubMed]
- Lin, C.-S. Brain Signature of Chronic Orofacial Pain: A Systematic Review and Meta-Analysis on Neuroimaging Research of Trigeminal Neuropathic Pain and Temporomandibular Joint Disorders. PLoS ONE 2014, 9, e94300. [Google Scholar] [CrossRef] [PubMed]
- McEwen, B.S.; Wingfield, J.C. What’s in a name? Integrating homeostasis, allostasis and stress. Horm. Behav. 2010, 57, 105. [Google Scholar] [CrossRef] [PubMed]
- McEwen, B.S. The neurobiology of stress: From serendipity to clinical relevance. Brain Res. 2000, 886, 172–189. [Google Scholar] [CrossRef]
- Simons, L.E.; Elman, I.; Borsook, D. Psychological processing in chronic pain: A neural systems approach. Neurosci. Biobehav. Rev. 2014, 39, 61–78. [Google Scholar] [CrossRef] [PubMed]
- Juster, R.-P.; Lupien, S.J. Chronic stress and allostatic load. In Handbook of Clinical Gender Medicine; Karger Publishers: Berlin, Germany, 2012; pp. 70–81. [Google Scholar]
- Juster, R.-P.; McEwen, B.S.; Lupien, S.J. Allostatic load biomarkers of chronic stress and impact on health and cognition. Neurosci. Biobehav. Rev. 2010, 35, 2–16. [Google Scholar] [CrossRef] [PubMed]
- Forte, G.; Troisi, G.; Pazzaglia, M.; De Pascalis, V.; Casagrande, M. Heart Rate Variability and Pain: A Systematic Review. Brain Sci. 2022, 12, 153. [Google Scholar] [CrossRef] [PubMed]
- Laborde, S.; Mosley, E.; Thayer, J.F. Heart Rate Variability and Cardiac Vagal Tone in Psychophysiological Research—Recommendations for Experiment Planning, Data Analysis, and Data Reporting. Front. Psychol. 2017, 8, 213. [Google Scholar] [CrossRef] [PubMed]
- Laborde, S.; Mosley, E.; Mertgen, A. Vagal Tank Theory: The Three Rs of Cardiac Vagal Control Functioning—Resting, Reactivity, and Recovery. Front. Neurosci. 2018, 12, 458. [Google Scholar] [CrossRef] [PubMed]
- Forte, G.; Favieri, F.; Casagrande, M. Heart Rate Variability and Cognitive Function: A Systematic Review. Front. Neurosci. 2019, 13, 710. [Google Scholar] [CrossRef] [PubMed]
- Magnon, V.; Vallet, G.T.; Benson, A.; Mermillod, M.; Chausse, P.; Lacroix, A.; Bouillon-Minois, J.-B.; Dutheil, F. Does heart rate variability predict better executive functioning? A systematic review and meta-analysis. Cortex 2022, 155, 218–236. [Google Scholar] [CrossRef] [PubMed]
- Siennicka, A.; Quintana, D.; Fedurek, P.; Wijata, A.; Paleczny, B.; Ponikowska, B.; Danel, D. Resting heart rate variability, attention and attention maintenance in young adults. Int. J. Psychophysiol. 2019, 143, 126–131. [Google Scholar] [CrossRef] [PubMed]
- Zeng, J.; Meng, J.; Wang, C.; Leng, W.; Zhong, X.; Gong, A.; Bo, S.; Jiang, C. High vagally mediated resting-state heart rate variability is associated with superior working memory function. Front. Neurosci. 2023, 17, 1119405. [Google Scholar] [CrossRef] [PubMed]
- Thayer, J.F.; Hansen, A.L.; Saus-Rose, E.; Johnsen, B.H. Heart Rate Variability, Prefrontal Neural Function, and Cognitive Performance: The Neurovisceral Integration Perspective on Self-regulation, Adaptation, and Health. Ann. Behav. Med. 2009, 37, 141–153. [Google Scholar] [CrossRef] [PubMed]
- Thayer, J. Brain and vagus nerve stimulation: A neurovisceral integration perspective. Brain Stimul. 2021, 14, 1750. [Google Scholar] [CrossRef]
- Forte, G.; Favieri, F.; Leemhuis, E.; De Martino, M.L.; Giannini, A.M.; De Gennaro, L.; Casagrande, M.; Pazzaglia, M. Ear your heart: Transcutaneous auricular vagus nerve stimulation on heart rate variability in healthy young participants. PeerJ 2022, 10, e14447. [Google Scholar] [CrossRef] [PubMed]
- Koenig, J.; Jarczok, M.; Ellis, R.; Hillecke, T.; Thayer, J. Heart rate variability and experimentally induced pain in healthy adults: A systematic review. Eur. J. Pain 2014, 18, 301–314. [Google Scholar] [CrossRef] [PubMed]
- Thayer, J.F.; Lane, R.D. A model of neurovisceral integration in emotion regulation and dysregulation. J. Affect. Disord. 2000, 61, 201–216. [Google Scholar] [CrossRef] [PubMed]
- Cohen, H.; Neumann, L.; Shore, M.; Amir, M.; Cassuto, Y.; Buskila, D. Autonomic dysfunction in patients with fibromyalgia: Application of power spectral analysis of heart rate variability. Semin. Arthritis Rheum. 2000, 29, 217–227. [Google Scholar] [CrossRef] [PubMed]
- Drury, R.L.; Simonetti, S.A. Heart Rate Variability in Dental Science. Front. Med. 2019, 6, 13. [Google Scholar] [CrossRef] [PubMed]
- Cutrim, R.C.; Santos-de-Araújo, A.D.; Pontes-Silva, A.; Protazio, J.B.; Anselmo-e-Silva, C.I.; Costa, C.P.; Goncalves, M.C.; de Oliveira, B.M.J.; de Almeida, L.V.; Filho, E.M.M.; et al. Short-term heart rate variability at rest in individuals with tem-poromandibular disorder: A comparative analysis. Clin. Oral Investig. 2023, 27, 6559–6566. [Google Scholar] [CrossRef] [PubMed]
- D’Amico, D.; Amestoy, M.E.; Fiocco, A.J. The association between allostatic load and cognitive function: A systematic and me-ta-analytic review. Psychoneuroendocrinology 2020, 121, 104849. [Google Scholar] [CrossRef]
- Diamond, A. Executive Functions. Annu. Rev. Psychol. 2013, 64, 135–168. [Google Scholar] [CrossRef] [PubMed]
- Tiego, J.; Tiego, J.; Testa, R.; Testa, R.; Bellgrove, M.A.; Bellgrove, M.A.; Pantelis, C.; Pantelis, C.; Whittle, S.; Whittle, S. A Hierarchical Model of Inhibitory Control. Front. Psychol. 2018, 9, 1339. [Google Scholar] [CrossRef] [PubMed]
- Forte, G.; Troisi, G.; Favieri, F.; Casagrande, M. Inhibition changes across the lifespan: Experimental evidence from the Stroop task. BMC Psychol. 2024, 12, 336. [Google Scholar] [CrossRef] [PubMed]
- Bjekić, J.; Živanović, M.; Purić, D.; Oosterman, J.M.; Filipović, S.R. Pain and executive functions: A unique relationship between Stroop task and experimentally induced pain. Psychol. Res. 2018, 82, 580–589. [Google Scholar] [CrossRef] [PubMed]
- Forte, G.; Troisi, G.; Favieri, F.; De Pascalis, V.; Langher, V.; Casagrande, M. Inhibition and Heart Rate Variability in Experimentally Induced Pain. J. Pain Res. 2023, 16, 3239–3249. [Google Scholar] [CrossRef] [PubMed]
- Friedman, N.P.; Miyake, A. The Relations Among Inhibition and Interference Control Functions: A Latent-Variable Analysis. J. Exp. Psychol. Gen. 2004, 133, 101–135. [Google Scholar] [CrossRef] [PubMed]
- Marouf, R.; Caron, S.; Lussier, M.; Bherer, L.; Piché, M.; Rainville, P. Reduced pain inhibition is associated with reduced cognitive inhibition in healthy aging. Pain 2014, 155, 494–502. [Google Scholar] [CrossRef] [PubMed]
- Oosterman, J.M.; Dijkerman, H.C.; Kessels, R.P.C.; Scherder, E.J.A. A unique association between cognitive inhibition and pain sensitivity in healthy participants. Eur. J. Pain 2010, 14, 1046–1050. [Google Scholar] [CrossRef] [PubMed]
- Berryman, C.; Stanton, T.R.; Bowering, K.J.; Tabor, A.; McFarlane, A.; Moseley, G.L. Do people with chronic pain have impaired executive function? A meta-analytical review. Clin. Psychol. Rev. 2014, 34, 563–579. [Google Scholar] [CrossRef] [PubMed]
- Nes, L.S.; Carlson, C.R.; Crofford, L.J.; de Leeuw, R.; Segerstrom, S.C. Self-regulatory deficits in fibromyalgia and temporomandibular disorders. Pain 2010, 151, 37–44. [Google Scholar] [CrossRef] [PubMed]
- Weissman-Fogel, I.; Moayedi, M.; Tenenbaum, H.C.; Goldberg, M.B.; Freeman, B.V.; Davis, K.D. Abnormal cortical activity in patients with temporomandibular disorder evoked by cognitive and emotional tasks. Pain 2011, 152, 384–396. [Google Scholar] [CrossRef] [PubMed]
- Hollins, M.; Bryen, C.P.; Taylor, D. Effects of chronic pain history on perceptual and cognitive inhibition. Exp. Brain Res. 2020, 238, 321–332. [Google Scholar] [CrossRef] [PubMed]
- Viechtbauer, W.; Smits, L.; Kotz, D.; Budé, L.; Spigt, M.; Serroyen, J.; Crutzen, R. A simple formula for the calculation of sample size in pilot studies. J. Clin. Epidemiol. 2015, 68, 1375–1379. [Google Scholar] [CrossRef] [PubMed]
- Tarvainen, M.P.; Niskanen, J.-P.; Lipponen, J.A.; Ranta-Aho, P.O.; Karjalainen, P.A. Kubios HRV–Heart rate variability analysis software. Comput. Methods Progr. Biomed. 2014, 113, 210–220. [Google Scholar] [CrossRef] [PubMed]
- Pham, T.; Lau, Z.J.; Chen, S.H.A.; Makowski, D. Heart Rate Variability in Psychology: A Review of HRV Indices and an Analysis Tutorial. Sensors 2021, 21, 3998. [Google Scholar] [CrossRef] [PubMed]
- Shaffer, F.; Ginsberg, J.P. An Overview of Heart Rate Variability Metrics and Norms. Front. Public Health 2017, 5, 258. [Google Scholar] [CrossRef] [PubMed]
- Stroop, J.R. Studies of interference in serial verbal reactions. J. Exp. Psychol. 1935, 18, 643–662. [Google Scholar] [CrossRef]
- Yukishita, T.; Lee, K.; Kim, S.; Yumoto, Y.; Kobayashi, A.; Shirasawa, T.; Kobayashi, H. Age and sex-dependent alterations in heart rate variability profiling the characteristics of men and women in their 30s. Anti-Aging Med. 2010, 7, 94–99. [Google Scholar] [CrossRef]
- Chandra, P.; Sands, R.L.; Gillespie, B.W.; Levin, N.W.; Kotanko, P.; Kiser, M.; Finkelstein, F.; Hinderliter, A.; Pop-Busui, R.; Rajagopalan, S.; et al. Predictors of heart rate variability and its prognostic significance in chronic kidney disease. Nephrol. Dial. Transplant. 2012, 27, 700–709. [Google Scholar] [CrossRef] [PubMed]
- Montaquila, J.M.; Trachik, B.J.; Bedwell, J.S. Heart rate variability and vagal tone in schizophrenia: A review. J. Psychiatr. Res. 2015, 69, 57–66. [Google Scholar] [CrossRef] [PubMed]
- Thayer, J.F.; Yamamoto, S.S.; Brosschot, J.F. The relationship of autonomic imbalance, heart rate variability and cardiovascular disease risk factors. Int. J. Cardiol. 2010, 141, 122–131. [Google Scholar] [CrossRef] [PubMed]
- Chinthakanan, S.; Laosuwan, K.; Boonyawong, P.; Kumfu, S.; Chattipakorn, N.; Chattipakorn, S.C. Reduced heart rate variability and increased saliva cortisol in patients with TMD. Arch. Oral Biol. 2018, 90, 125–129. [Google Scholar] [CrossRef] [PubMed]
- Guidi, J.; Lucente, M.; Sonino, N.; Fava, G.A. Allostatic Load and Its Impact on Health: A Systematic Review. Psychother. Psychosom. 2021, 90, 11–27. [Google Scholar] [CrossRef]
- Glass, J.M.; Williams, D.A.; Fernandez-Sanchez, M.-L.; Kairys, A.; Barjola, P.; Heitzeg, M.M.; Clauw, D.J.; Schmidt-Wilcke, T. Executive Function in Chronic Pain Patients and Healthy Controls: Different Cortical Activation During Response Inhibition in Fibromyalgia. J. Pain 2011, 12, 1219–1229. [Google Scholar] [CrossRef] [PubMed]
- McEwen, B.S. Protective and damaging effects of stress mediators: Central role of the brain. Dialog. Clin. Neurosci. 2006, 8, 367–381. [Google Scholar] [CrossRef] [PubMed]
- Forte, G.; Casagrande, M. Effects of Blood Pressure on Cognitive Performance in Aging: A Systematic Review. Brain Sci. 2020, 10, 919. [Google Scholar] [CrossRef] [PubMed]
Group | SDNN | RMSSD | HF | ||
---|---|---|---|---|---|
Age | TMD | Pearson’s r p-value | −0.71 ** 0.002 | −0.57 * 0.021 | −0.54 * 0.033 |
Control | Pearson’s r p-value | −0.36 0.19 | −0.30 0.27 | −0.38 0.16 |
Predictor | F | η2 p | β | p | |
---|---|---|---|---|---|
Stroop Effect | RMSSD | 16.04 | 0.61 | 1.11 | <0.01 |
Pain Intensity | 11.15 | 0.53 | 0.43 | <0.01 | |
RMSSD × Pain Intensity | 1.60 | 0.14 | −0.30 | 0.24 | |
R2 | 0.84 | ||||
F | 17.6 | ||||
p | >0.001 | ||||
False Alarms | RMSSD | 0.52 | 0.05 | 0.47 | 0.48 |
Pain Intensity | 0.81 | 0.08 | −0.27 | 0.39 | |
RMSSD × Pain Intensity | 0.43 | 0.04 | −0.36 | 0.53 | |
R2 | 14 | ||||
F | 0.56 | ||||
p | 0.65 |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2024 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Troisi, G.; Di Giacomo, P.; Forte, G.; Langher, V.; Casagrande, M.; Di Paolo, C. The “Wear and Tear” of the Organism in Temporomandibular Disorders: A Pilot Study Investigating the Effects of Allostatic Load on Heart Rate Variability and Inhibitory Control. J. Pers. Med. 2024, 14, 787. https://doi.org/10.3390/jpm14080787
Troisi G, Di Giacomo P, Forte G, Langher V, Casagrande M, Di Paolo C. The “Wear and Tear” of the Organism in Temporomandibular Disorders: A Pilot Study Investigating the Effects of Allostatic Load on Heart Rate Variability and Inhibitory Control. Journal of Personalized Medicine. 2024; 14(8):787. https://doi.org/10.3390/jpm14080787
Chicago/Turabian StyleTroisi, Giovanna, Paola Di Giacomo, Giuseppe Forte, Viviana Langher, Maria Casagrande, and Carlo Di Paolo. 2024. "The “Wear and Tear” of the Organism in Temporomandibular Disorders: A Pilot Study Investigating the Effects of Allostatic Load on Heart Rate Variability and Inhibitory Control" Journal of Personalized Medicine 14, no. 8: 787. https://doi.org/10.3390/jpm14080787
APA StyleTroisi, G., Di Giacomo, P., Forte, G., Langher, V., Casagrande, M., & Di Paolo, C. (2024). The “Wear and Tear” of the Organism in Temporomandibular Disorders: A Pilot Study Investigating the Effects of Allostatic Load on Heart Rate Variability and Inhibitory Control. Journal of Personalized Medicine, 14(8), 787. https://doi.org/10.3390/jpm14080787