Lower Limb Perfusion Asymmetries in Humans at Rest and Following Activity—A Collective View
Abstract
:1. Introduction
2. Methods
2.1. Participants
2.2. Experiment
- Phase I, corresponding to the baseline measurements; Phase II, corresponding to the application of the specific challenger in each protocol, chosen to modify perfusion; and Phase III, corresponding to recovery. Each phase had a duration of 5 to 10 min.
- Passive—The application of superficial massage to the leg with participants in a supine position. A trained therapist applied an effleurage procedure (a variant of the so-called “Swedish Massage”) to participants lying on a padded exam table. These protocols involved 56 participants (mean age {SD} 32.64 {16.64}; 50% female). Details on these protocols are shown in Table 1 and results have been published elsewhere [31,33,34,35].
- Active—Quasi-static and dynamic movement in an upright position. With participants (n = 83, mean age {SD} 28.01 {9.10}; 50.6% female) beginning standing in the upright position, the impact of quasi-static (plantar flexion, squat, and hemi-squat) or dynamic movement (step-in-place and walking) on perfusion was analyzed. Further notes on these protocols are shown in Table 1 and complete results published elsewhere [37,38,39].
2.3. Variables of Interest
2.4. Statistical Analysis
3. Results and Discussion
4. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Acknowledgments
Conflicts of Interest
References
- Bouley, J.F. Claudication Intermittent des Membres Posterieurs, determinee par L’obliteration des Arteres Femorales. Recl. Méd. Vét. 1831, 8, 517–527. [Google Scholar]
- Hensen, H. Beitrage zur Physiologie und pathologie des Blutdrucks (Contributions to the physiology and pathology of blood pressure). Dtsch. Arch. Med. 1900, 67, 436. [Google Scholar]
- Cheatle, T.R.; Coleridge-Smith, P.D.; Scurr, J.H. The investigation of peripheral vascular disease—A historical perspective. Vasc. Med. Rev. 1991, 2, 101–109. [Google Scholar] [CrossRef]
- Zusmanovich, F.N.; Elizarova, S.N. Dinamika perfuzionnogo davleniia v nizhnikh konechnostiakh v pokoe i posle fizicheskoĭ nagruzki (Perfusion pressure dynamics in lower extremities at rest and after exercise). Fiziol. Cheloveka 2002, 28, 133–136. [Google Scholar] [PubMed]
- Seder, J.S.; Botvinick, E.H.; Rahimtoola, S.H.; Goldstone, J.; Price, D.C. Detecting and localizing peripheral arterial disease: Assessment of 201Tl scintigraphy. Am. J. Roentgenol. 1981, 137, 373–380. [Google Scholar] [CrossRef] [Green Version]
- Collins, R.; Burch, J.; Cranny, G.; Aguiar-Ibáñez, R.; Craig, D.; Wright, K.; Berry, E.; Gough, M.; Kleijnen, J.; Westwood, M. Duplex ultrasonography, magnetic resonance angiography, and computed tomography angiography for diagnosis and assessment of symptomatic, lower limb peripheral arterial disease: Systematic review. BMJ 2007, 334, 1257. [Google Scholar] [CrossRef] [Green Version]
- Rodgers, J.L.; Jones, J.; Bolleddu, S.I.; Vanthenapalli, S.; Rodgers, L.E.; Shah, K.; Karia, K.; Panguluri, S.K. Cardiovascular Risks Associated with Gender and Aging. J. Cardiovasc. Dev. Dis. 2019, 6, 19. [Google Scholar] [CrossRef] [Green Version]
- Eid, M.A.; Mehta, K.S.; Goodney, P.P. Epidemiology of peripheral artery disease. Semin. Vasc. Surg. 2021, 34, 38–46. [Google Scholar] [CrossRef]
- Wood, N.B.; Zhao, S.Z.; Zambanini, A.; Jackson, M.; Gedroyc, W.; Thom, S.A.; Hughes, A.D.; Xu, X.Y. Curvature and tortuosity of the superficial femoral artery: A possible risk factor for peripheral arterial disease. J. Appl. Physiol. 2006, 101, 1412–1418. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Eisen, L.A.; Minami, T.; Sekiguchi, H.; Berger, J.S.; Mayo, P.; Narasimhan, M. Ultrasound demonstration of asymmetry between the left and right femoral and radial arteries. Chest 2006, 130, 201S. [Google Scholar] [CrossRef]
- Marcinkevics, Z.; Lukstina, Z.; Rubins, U.; Grabovskis, A.; Aivars, J.I. Bilateral difference of superficial and deep femoral artery haemodynamic and anatomical parameters. Artery Res. 2013, 7, 201–210. [Google Scholar] [CrossRef]
- Mei, C.C.; Zhang, J.; Jing, H.X. Fluid mechanics of Windkessel effect. Med. Biol. Eng. Comput. 2018, 56, 1357–1366. [Google Scholar] [CrossRef] [PubMed]
- Climie, R.E.; Gallo, A.; Picone, D.S.; Di Lascio, N.; van Sloten, T.T.; Guala, A.; Mayer, C.C.; Hametner, B.; Bruno, R.M. Measuring the Interaction Between the Macro- and Micro-Vasculature. Front. Cardiovasc. Med. 2019, 6, 169. [Google Scholar] [CrossRef] [Green Version]
- Cracowski, J.L.; Roustit, M. Human Skin Microcirculation. Compr. Physiol. 2020, 10, 1105–1154. [Google Scholar] [CrossRef] [PubMed]
- Siegel, M.E.; Siemsen, J.K. A new noninvasive approach to peripheral vascular disease: Thallium-201 leg scans. Am. J. Roentgenol. 1978, 131, 827–830. [Google Scholar] [CrossRef] [Green Version]
- Bishop, C.; Read, P.; Chavda, S.; Turner, A. Asymmetries of the Lower Limb: The Calculation Conundrum in Strength Training and Conditioning. Strength Cond. J. 2016, 38, 27–32. [Google Scholar] [CrossRef] [Green Version]
- Vaisman, A.; Guiloff, R.; Rojas, J.; Delgado, I.; Figueroa, D.; Calvo, R. Lower Limb Symmetry: Comparison of Muscular Power Between Dominant and Nondominant Legs in Healthy Young Adults Associated with Single-Leg-Dominant Sports. Orthop. J. Sports Med. 2017, 5, 2325967117744240. [Google Scholar] [CrossRef] [PubMed]
- Van Melick, N.; Meddeler, B.M.; Hoogeboom, T.J.; Nijhuis-van der Sanden, M.W.G.; van Cingel, R.E.H. How to determine leg dominance: The agreement between self-reported and observed performance in healthy adults. PLoS ONE 2017, 12, e0189876. [Google Scholar]
- Bellenfant, K.B.; Robbins, G.L.; Rogers, R.R.; Kopec, T.J.; Ballmann, C.G. Effects of Dominant and Nondominant Limb Immobilization on Muscle Activation and Physical Demand during Ambulation with Axillary Crutches. J. Funct. Morphol. Kinesiol. 2021, 6, 16. [Google Scholar] [CrossRef]
- Lanshammar, K.; Ribom, E.L. Differences in muscle strength in dominant and non-dominant leg in females aged 20–39 years—A population-based study. Phys. Ther. Sport 2011, 12, 76–79. [Google Scholar] [CrossRef] [PubMed]
- Maloney, S.J. The Relationship between Asymmetry and Athletic Performance: A Critical Review. J. Strength Cond. Res. 2019, 33, 2579–2593. [Google Scholar] [CrossRef] [PubMed]
- Hoffman, J.R.; Ratamess, N.A.; Klatt, M.; Faigenbaum, A.D.; Kang, J. Do Bilateral Power Deficits Influence Direction-Specific Movement Patterns? Res. Sports Med. 2007, 15, 125–132. [Google Scholar] [CrossRef]
- Bell, D.R.; Sanfilippo, J.L.; Binkley, N.; Heiderscheit, B.C. Lean mass asymmetry influences force and power asymmetry during jumping in collegiate athletes. J. Strength Cond. Res. 2014, 28, 884–891. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Heil, J.; Loffing, F.; Büsch, D. The Influence of Exercise-Induced Fatigue on Inter-Limb Asymmetries: A Systematic Review. Sports Med. Open 2020, 6, 39. [Google Scholar] [CrossRef] [PubMed]
- Kadoguchi, T.; Horiuchi, M.; Kinugawa, S.; Okita, K. Heterogeneity in the vasodilatory function of individual extremities. Vascular 2020, 28, 87–95. [Google Scholar] [CrossRef] [PubMed]
- Jungmann, P.M.; Pfirrmann, C.; Federau, C. Characterization of lower limb muscle activation patterns during walking and running with Intravoxel Incoherent Motion (IVIM) MR perfusion imaging. Magn. Reson. Imaging 2019, 63, 12–20. [Google Scholar] [CrossRef] [PubMed]
- Peter, M.; Durding, B.M. Footedness of left- and right-handers. Am. J. Psychol. 1979, 92, 133–142. [Google Scholar] [CrossRef] [PubMed]
- Srivaratharajah, K.; Abramson, B.L. Women and Peripheral Arterial Disease: A Review of Sex Differences in Epidemiology, Clinical Manifestations, and Outcomes. Can. J. Cardiol. 2018, 34, 356–361. [Google Scholar] [CrossRef]
- Huxley, V.H.; Kemp, S.S. Sex-Specific Characteristics of the Microcirculation. Adv. Exp. Med. Biol. 2018, 1065, 307–328. [Google Scholar] [CrossRef]
- Ansdell, P.; Thomas, K.; Hicks, K.M.; Hunter, S.K.; Howatson, G.; Goodall, S. Physiological sex differences affect the integrative response to exercise: Acute and chronic implications. Exp. Physiol. 2020, 105, 2007–2021. [Google Scholar] [CrossRef]
- Gregório, J.; Silva., H.; Rocha, C.; Rodrigues, L.M. Perfusion is sex related but response to massage evokes the same hemodynamic adaptation in both sexes—Results from an exploratory factor analysis. Proceed Physioma 2019—1st Int Meeting Portuguese Physiological Society. Biomed. Biopharm. Res. 2019, 16, 31–32. [Google Scholar] [CrossRef]
- Bassareo, P.P.; Crisafulli, A. Gender Differences in Hemodynamic Regulation and Cardiovascular Adaptations to Dynamic Exercise. Curr. Cardiol. Rev. 2020, 16, 65–72. [Google Scholar] [CrossRef]
- Rocha, C.; Macedo, A.; Nuno, S.; Silva, H.; Ferreira, H.; Rodrigues, L.M. Exploring the perfusion modifications occurring with massage in the human lower limbs by non-contact polarized spectroscopy. Biomed. Biopharm. Res. 2018, 15, 196–204. [Google Scholar] [CrossRef]
- Rocha, C.; Silva, H.; Ferreira, H.; Rodrigues, L.M. Comparing the effects of human hind limb massage by analysis of Laser Doppler flowmetry and Photoplethysmography signal components using the wavelet transform. Biomed. Biopharm. Res. 2018, 15, 70–81. [Google Scholar] [CrossRef]
- Rodrigues, L.M.; Rocha, C.; Ferreira, H.Á.; Silva, H.N. Lower limb massage in humans increases local perfusion and impacts systemic hemodynamics. J. Appl. Physiol. 2020, 128, 1217–1226. [Google Scholar] [CrossRef] [PubMed]
- Silva, H.; Ferreira, H.Á.; da Silva, H.P.; Monteiro Rodrigues, L. The Venoarteriolar Reflex Significantly Reduces Contralateral Perfusion as Part of the Lower Limb Circulatory Homeostasis in vivo. Front. Physiol. 2018, 9, e1123. [Google Scholar] [CrossRef] [Green Version]
- Florindo, M.; Silva, H.; Rodrigues, L.M. Impact of the isometric contraction of the calf on the local microcirculation. Biomed. Biopharm. Res. 2017, 14, 179–186. [Google Scholar] [CrossRef]
- Nuno, S.; Florindo, M.; Silva, H.; Rodrigues, L.M. Studying the impact of different body positioning, squatting, and unipodal flexion on perfusion in the lower limb—An exploratory approach complemented with optical spectroscopy (TiVi). Biomed. Biopharm. Res. 2020, 17, 187–196. [Google Scholar] [CrossRef]
- Florindo, M.; Nuno, S.L.; Rodrigues, L.M. Lower limb dynamic activity significantly reduces foot skin perfusion- exploring data with different optical sensors in age-grouped healthy adults. Skin Pharmacol. Physiol. 2021. [Google Scholar] [CrossRef]
- Rodrigues, L.M.; Silva, H.; Ferreira, H.; Renault, M.-A.; Gadeau, A.-P. Observations on the perfusion recovery of regenerative angiogenesis in an ischemic limb model under hyperoxia. Physiol. Rep. 2018, 6, e13736. [Google Scholar] [CrossRef]
- Aboyans, V.; Criqui, M.H.; Abraham, P.; Allison, M.A.; Creager, M.A.; Diehm, C.; Fowkes, F.G.; Hiatt, W.R.; Jönsson, B.; Lacroix, P.; et al. American Heart Association Council on Peripheral Vascular Disease, Council on Epidemiology and Prevention, Council on Clinical Cardiology, Council on Cardiovascular Radiology and Intervention, and Council on Cardiovascular Surgery and Anesthesia. Measurement and interpretation of the ankle-brachial index: A scientific statement from the American Heart Association. Circulation 2012, 126, 2890–2909. [Google Scholar] [CrossRef] [Green Version]
- Czell, D.; Schreier, R.; Rupp, I.R.; Eberhard, S.; Colombo, G.; Dietz, V. Influence of passive leg movements on blood circulation on the tilt table in healthy adults. JNER 2004, 1, 4. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- World Medical Association. World Medical Association Declaration of Helsinki: Ethical principles for medical research involving human subjects. JAMA 2013, 310, 2191–2194. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Van Gelder, L.M.A.; Angelini, L.; Buckley, E.E.; Mazzà, C. A Proposal for a Linear Calculation of Gait Asymmetry. Symmetry 2021, 13, 1560. [Google Scholar] [CrossRef]
- Abiri, B.; Vafa, M. Dietary Restriction, Cardiovascular aging and age-related cardiovascular diseases: A review of the evidence. In Reviews on Biomarker Studies in Aging and Anti-Aging Research. Advances in Experimental Medicine and Biology; Guest, P., Ed.; Springer: Cham, Switzerland, 2019; Volume 1178. [Google Scholar] [CrossRef]
- Xu, X.; Wang, B.; Ren, C.; Hu, J.; Greenberg, D.A.; Chen, T.; Xie, L.; Jin, K. Age-related Impairment of Vascular Structure and Functions. Aging Dis. 2017, 8, 590–610. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Shinozaki, N. Effect of body position on skin perfusion pressure in patients with severe peripheral arterial disease. Circ. J. 2012, 76, 2863–2866. [Google Scholar] [CrossRef] [Green Version]
- Kawasaki, T.; Uemura, T.; Matsuo, K.; Masumoto, K.; Harada, Y.; Chuman, T.; Murata, T. The effect of different positions on lower limbs skin perfusion pressure. Indian J. Plast. Surg. 2013, 46, 508–512. [Google Scholar] [CrossRef]
- Egorova, N.; Vouyouka, A.G.; Quin, J.; Guillerme, S.; Moskowitz, A.; Marin, M.; Faries, P.L. Analysis of gender-related differences in lower extremity peripheral arterial disease. J. Vasc. Surg. 2010, 51, 372–379. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Peters, S.A.E.; Muntner, P.; Woodward, M. Sex Differences in the Prevalence of, and Trends in, Cardiovascular Risk Factors, Treatment, and Control in the United States, 2001 to 2016. Circulation 2019, 139, 1025–1035. [Google Scholar] [CrossRef] [PubMed]
- Manevska, N.; Gjorceva, D.P.; Ahmeti, I.; Todorovska, L.; Stojanoski, S.; Kocovska, M.Z. Tissue-Muscle Perfusion Scintigraphy of the Lower Limbs in a Patient with Type 2 Diabetes Mellitus and Peripheral Arterial Disease. Mol. Imaging Radionucl. Ther. 2016, 25, 42–46. [Google Scholar] [CrossRef]
- De Ritter, R.; de Jong, M.; Vos, R.C.; van der Kallen, C.; Sep, S.; Woodward, M.; Stehouwer, C.; Bots, M.L.; Peters, S. Sex differences in the risk of vascular disease associated with diabetes. Biol. Sex Differ. 2020, 11, 1. [Google Scholar] [CrossRef] [PubMed] [Green Version]
References | Participant Profile | Reference Measuring Technology | Measurement Sites | Protocol Duration (Three Phases) | Challenge (Ph2) |
---|---|---|---|---|---|
Gregorio et al. [31] | Healthy, young, both sexes | LDF | 2nd toe, plantar, both feet | Ph1—10 min Ph2—5 min Ph3—10 min | Massage |
Rocha et al. [33] | Healthy, aged, both sexes | LDF | 2nd toe, plantar, both feet | Ph1—10 min Ph2—5 min Ph3—10 min | Massage |
Rocha et al. [34] | Healthy, young, both sexes | LDF | 2nd toe, plantar, both feet | Ph1—10 min Ph2—5 min Ph3—10 min | Massage |
Rodrigues et al. [35] | Healthy, young, both sexes | LDF | 2nd toe, plantar, both feet | Ph1—10 min Ph2—5 min Ph3—10 min | Massage |
Florindo et al. [37] | Healthy, aged, both sexes | LDF | Dorsal, 1st metatarsal, both feet | Ph1—10 min Ph2—1 min Ph3—5 min | Plantar flexion |
Nuno et al. [38] | Healthy, young, both sexes | LDF | Dorsal, 2nd–3rd toe root, both feet | Ph1—10 min Ph2—5 min Ph3—10 min | Hemi-squat; squat |
Florindo et al. [39] | Healthy, young and aged, both sexes | LDF | Dorsal, 1st metatarsal, both feet | Ph1—10 min Ph2—5 min Ph3—10 min | Walking |
MEN | Massage | Plantar Flexion | Step-in-Place | Hemi-Squat | Squat | Walking | p |
---|---|---|---|---|---|---|---|
N (%) | 28 (40.6) | 9 (13.0) | 12 (17.4) | 4 (5.8) | 4 (5.8) | 12 (17.4) | - |
Median Age, years (min—max) | 20.5 (18.0–66.0) | 30.0 (21.0–55.0) | 22.5 (18.0–32.0) | 31.5 (20.0–32.0) | 31.5 (20.0–32.0) | 31.5 (19.0–58.0) | 0.563 |
Mean Weight, kg (SD) | 76.1 (10.0) | 75.9 (15.3) | 77.1 (6.3) | 68.0 (6.7) | 68.0 (6.7) | 75.5 (6.6) | 0.398 |
Mean Height, meters (SD) | 1.8 (0.1) | 1.8 (0.1) | 1.8 (0.1) | 1.7 (0.0) | 1.7 (0.0) | 1.7 (0.1) | 0.211 |
Mean BMI, kg/m2 (SD) | 23.9 (2.9) | 24.6 (4.1) | 24.7 (1.2) | 22.8 (1.8) | 22.8 (1.8) | 25.0 (1.4) | 0.446 |
Mean SYS (SD) | 118.2 (11.8) | 116.0 (14.6) | 123.0 (13.6) | 124.0 (7.4) | 124.0 (7.4) | 124.2 (17.7) | 0.570 |
Mean DIA (SD) | 74.4 (9.2) | 75.1 (9.0) | 71.5 (8.2) | 67.0 (6.7) | 67.0 (6.7) | 71.4 (7.3) | 0.324 |
Median ABI (min—max) | 1.1 (1.0–1.3) | 1.2 (1.1–1.8) | 1.1 (1.0–1.2) | 1.0 (1.0–1.1) | 1.0 (1.0–1.1) | 1.1 (1.0–1.2) | 0.008 * |
WOMEN | |||||||
N (%) | 28 (40.0) | 9 (12.9) | 11 (15.7) | 4 (5.7) | 4 (5.7) | 14 (20.0) | - |
Median Age, years (min—max) | 23.0 (18.0–62.0) | 26.0 (21.0–59.0) | 23.0 (20.0–31.0) | 22.0 (21.0–22.0) | 22.0 (21.0–22.0) | 22.5 (19.0–44.0) | 0.463 |
Mean Weight, kg (SD) | 60.5 (9.1) | 72.9 (15.5) | 57.8 (8.7) | 61.3 (10.7) | 61.3 (10.7) | 60.7 (10.2) | 0.043 * |
Mean Height, meters (SD) | 1.6 (0.1) | 1.6 (0.1) | 1.6 (0.1) | 1.7 (0.1) | 1.7 (0.1) | 1.6 (0.1) | 0.597 |
Mean BMI, kg/m2 (SD) | 22.9 (3.3) | 27.7 (6.4) | 21.4 (2.8) | 21.8 (2.1) | 21.8 (2.1) | 22.8 (3.0) | 0.007 * |
Mean SYS (SD) | 113.0 (13.8) | 123.7 (11.0) | 115.9 (8.2) | 122.0 (7.6) | 122.0 (7.6) | 114.5 (14.4) | 0.218 |
Mean DIA (SD) | 74.1 (7.2) | 83.2 (8.5) | 72.1 (11.2) | 63.0 (7.9) | 63.0 (7.9) | 68.5 (6.6) | <0.001 * |
Median ABI (min—max) | 1.1 (1.0–1.3) | 1.2 ⸸ (1.0–1.4) | 1.1 (0.9–1.2) | 1.0 (1.0–1.0) | 1.0 (1.0–1.0) | 1.0 (0.9–1.2) | 0.001 * |
Perfusion at Baseline (4th Quartile) | Perfusion at Recovery (4th Quartile) | |||
---|---|---|---|---|
OR [95% CI] (p-Value) | aOR [95% CI] (p-Value) | OR [95% CI] (p-Value) | aOR [95% CI] (p-Value) | |
SEX | ||||
Men | 2.4 [1.1–5.4] (0.030) | 2.6 [1.1–6.3] (0.032) | 1.8 [0.8–3.8] (0.159) | 1.6 [0.7–3.8] (0.281) |
Women | 1 | 1 | 1 | 1 |
BMI, kg/m2 | ||||
less than 25 | 0.4 [0.2–0.8] (0.013) | 0.5 [0.2–1.3] (0.173) | 0.4 [0.2–0.8] (0.013) | 0.6 [0.2–1.4] (0.198) |
more than 25 | 1 | 1 | 1 | 1 |
AGE, years | ||||
less than 30 | 0.4 [0.2–0.8] (0.010) | 0.4 [0.2–1.0] (0.064) | 0.2 [0.1–0.5] (<0.001) | 0.3 [0.1–0.6] (0.003) |
more than 30 | 1 | 1 | 1 | 1 |
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2021 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
Rodrigues, L.M.; Rocha, C.G.; Florindo, M.E.; Gregório, J. Lower Limb Perfusion Asymmetries in Humans at Rest and Following Activity—A Collective View. Symmetry 2021, 13, 2348. https://doi.org/10.3390/sym13122348
Rodrigues LM, Rocha CG, Florindo ME, Gregório J. Lower Limb Perfusion Asymmetries in Humans at Rest and Following Activity—A Collective View. Symmetry. 2021; 13(12):2348. https://doi.org/10.3390/sym13122348
Chicago/Turabian StyleRodrigues, Luis Monteiro, Clemente Gomes Rocha, Margarida Esteves Florindo, and João Gregório. 2021. "Lower Limb Perfusion Asymmetries in Humans at Rest and Following Activity—A Collective View" Symmetry 13, no. 12: 2348. https://doi.org/10.3390/sym13122348
APA StyleRodrigues, L. M., Rocha, C. G., Florindo, M. E., & Gregório, J. (2021). Lower Limb Perfusion Asymmetries in Humans at Rest and Following Activity—A Collective View. Symmetry, 13(12), 2348. https://doi.org/10.3390/sym13122348