Abstract
In Health Resort Medicine, both balneotherapy and thalassotherapy, salt waters and their peloids, or mud products are mainly used to treat rheumatic and skin disorders. These therapeutic agents act jointly via numerous mechanical, thermal, and chemical mechanisms. In this review, we examine a new mechanism of action specific to saline waters. When topically administered, this water rich in sodium and chloride penetrates the skin where it is able to modify cellular osmotic pressure and stimulate nerve receptors in the skin via cell membrane ion channels known as “Piezo” proteins. We describe several models of cutaneous adsorption/desorption and penetration of dissolved ions in mineral waters through the skin (osmosis and cell volume mechanisms in keratinocytes) and examine the role of these resources in stimulating cutaneous nerve receptors. The actions of salt mineral waters are mediated by a mechanism conditioned by the concentration and quality of their salts involving cellular osmosis-mediated activation/inhibition of cell apoptotic or necrotic processes. In turn, this osmotic mechanism modulates the recently described mechanosensitive piezoelectric channels.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Abbreviations
- AVD:
-
Apoptotic volume decrease
- C-TEAB:
-
C-tetraethylammonium bromide
- HaCaT:
-
Adult human keratinocyte cell line
- HSC:
-
Human stratum corneum
- KCl:
-
Potassium chloride
- Kow :
-
Octanol/water partition coefficient
- MS:
-
Mechanosensitive
- MT:
-
Mechanotransduction
- NaCl:
-
Sodium chloride
- NHEs:
-
Na+-H+-exchangers
- NMF:
-
Natural moisturizing factor
- NVI:
-
Necrotic volume increase
- Pow :
-
Participation coefficient
- QSPR:
-
Quantitative structure permeability relationships
- RVD:
-
Regulatory volume decrease
- RVI:
-
Regulatory volume increase
- TEA:
-
Triethanolamine
- TEWL:
-
Transepidermal water loss
- UVR:
-
Ultraviolet radiation
References
Abraham MH, Martins F (2004) Human skin permeation and partition: general linear free-energy relationship analyses. J Pharm Sci 93:1508–1523. https://doi.org/10.1002/jps.20070
Abu-Shakra M, Mayer A, Friger M, Harari M (2014) Dead Sea mud packs for chronic low back pain. Isr Med Assoc J 16:574–577
Agishi Y, Miyaji M, Shimizu T (2010) Impact of salt in balneo- and thalassotherapy in Japan. In: proceedings of the international conference; international congress. Spa therapy with saline waters in health resorts. Österr Z Phys Med Rehabil 20:60–61
Agre P, Kozono D (2003) Aquaporin water channels: molecular mechanisms for human diseases. FEBS Lett 555:72–78. https://doi.org/10.1016/S0014-5793(03)01083-4
Ahern CA, Payandeh J, Bosmans F, Chanda B (2016) The hitchhiker's guide to the voltage-gated sodium channel galaxy. J Gen Physiol 147:1–24. https://doi.org/10.1085/jgp.201511492
Alexander RT, Grinstein S (2006) Na+/H+ exchangers and the regulation of volume. Acta Physiol (Oxf) 187:159–167. https://doi.org/10.1111/j.1748-1716.2006.01558.x
Alvarez-Román R, Merino G, Kalia YN, Naik A, Guy RH (2003) Skin permeability enhancement by low frequency sonophoresis: lipid extraction and transport pathways. J Pharm Sci 92:1138–1146. https://doi.org/10.1002/jps.10370
Anderson BD, Higuchi WI, Raykar PV (1988) Heterogeneity effects on permeability-partition coefficient relationships in human stratum corneum. Pharm Res 5:566–573
Bae C, Sachs F, Gottlieb PA (2015) Protonation of the human PIEZO1 ion cannel stabilizes inactivation. J Biol Chem 290:5167–5173. https://doi.org/10.1074/jbc.M114.604033
Bagriantsev SN, Gracheva EO, Gallagher PG (2014) Piezo proteins: regulators of mechanosensation and other cellular processes. J Biol Chem 289:31673–31681. https://doi.org/10.1074/jbc.R114.612697
Bálint GP, Buchanan WW, Adám A, Ratkó I, Poór L, Bálint PV, Somos E, Tefner I, Bender T (2007) The effect of the thermal mineral water of Nagybaracska on patients with knee joint osteoarthritis-a double blind study. Clin Rheumatol 26:890–894. https://doi.org/10.1007/s10067-006-0420-1
Bazzichi L, Da Valle Y, Rossi A, Giacomelli C, Sernissi F, Giannaccini G, Betti L, Ciregia F, Giusti L, Scarpellini P, Dell'Osso L, Marazziti D, Bombardieri S, Lucacchini A (2013) A multidisciplinary approach to study the effects of balneotherapy and mud-bath therapy treatments on fibromyalgia. Clin Exp Rheumatol 31:S111–S120
Bellometti S, Galzigna L (1999) Function of the hypothalamic adrenal axis in patients with fibromyalgia syndrome undergoing mud-pack treatment. Int J Clin Pharmacol Res 19:27–33
Bellometti S, Giannini S, Sartori L, Crepaldi G (1997a) Cytokine levels in osteoarthrosis patients undergoing mud bath therapy. Int J Clin Pharmacol Res 17:149–153
Bellometti S, Cecchettin M, Galzigna L (1997b) Mud pack therapy in osteoarthrosis. Changes in serum levels of chondrocyte markers. Clin Chim Acta 268:101–106. https://doi.org/10.1016/S0009-8981(97)00171-X
Bellometti S, Poletto M, Gregotti C, Richelmi P, Bertè F (2000) Mud bath therapy influences nitric oxide, myeloperoxidase and glutathione peroxidase serum levels in arthritic patients. Int J Clin Pharmacol Res 20:69–80
Bellometti S, Galzigna L, Richelmi P, Gregotti C, Bertè F (2002) Both serum receptors of tumor necrosis factor are influenced by mud pack treatment in osteoarthrotic patients. Int J Tissue React 24:57–64
Bellometti S, Gallotti C, Pacileo G, Rota A, Tenconi MT (2007) Evaluation of outcomes in SPA-treated osteoarthrosic patients. J Prev Med Hyg 48:1–4. https://doi.org/10.15167/2421-4248/jpmh2007.48.1.81
Bender T, Karagülle Z, Bálint GP, Gutenbrunner C, Bálint PV, Sukenik S (2005) Hydrotherapy, balneotherapy, and spa treatment in pain management. Rheumatol Int 25:220–224. https://doi.org/10.1007/s00296-004-0487-4
Bender T, Bálint G, Prohászka Z, Géher P, Tefner IK (2014) Evidence-based hydro- and balneotherapy in Hungary-a systematic review and meta-analysis. Int J Biometeorol 58:311–323. https://doi.org/10.1007/s00484-013-0667-6
Bobet J (1999) Il était une fois… la thalassothérapie. Atlantica, Biarritz
Bodde HE, van den Brink I, Koerten HK, de Haan FHN (1991) Visualization of in vitro percutaneous penetration of mercuric chloride; transport through intercellular space versus cellular uptake through desmosomes. J Control Release 15:227–236. https://doi.org/10.1016/0168-3659(91)90114-S
Bonsignori F (2011) La Talassoterapia. Cure e benessere alle terme marine e al mare. ETS, Pisa
Bouwstra JA, Ponec M (2006) The skin barrier in healthy and diseased state. Biochim Biophys Acta 1758:2080–2095. https://doi.org/10.1016/j.bbamem.2006.06.021
Bouwstra JA, Dubbelaar FE, Gooris GS, Ponec M (2000) The lipid organisation in the skin barrier. Acta Derm Venereol Suppl (Stockh) 208:23–30. https://doi.org/10.1080/000155500750042826
Brockow T, Schiener R, Franke A, Resch KL, Peter RU (2007a) A pragmatic randomized controlled trial on the effectiveness of low concentrated saline spa water baths followed by ultraviolet B (UVB) compared to UVB only in moderate to severe psoriasis. J Eur Acad Dermatol Venereol 21:1027–1037. https://doi.org/10.1111/j.1468-3083.2007.02152.x
Brockow T, Schiener R, Franke A, Resch KL, Peter RU (2007b) A pragmatic randomized controlled trial on the effectiveness of highly concentrated saline spa wáter baths followed by UVB compared to UVB only in moderate to severe psoriasis. J Altern Complement Med 13:725–732. https://doi.org/10.1089/acm.2007.7099
Brouard M, Casado M, Djelidi S, Barrandon Y, Farman N (1999) Epithelial sodium channel in human epidermal keratinocytes: expression of its subunits and relation to sodium transport and differentiation. J Cell Sci 112(Pt 19):3343–3352
Burg MB, Kwon ED, Kültz D (1997) Regulation of gene expression by hypertonicity. Annu Rev Physiol 59:437–455. https://doi.org/10.1146/annurev.physiol.59.1.437
Cahalan SM, Lukacs V, Ranade SS, Chien S, Bandell M, Patapoutian A (2015) Piezo1 links mechanical forces to red blood cell volume. eLife 4:e07370. https://doi.org/10.7554/eLife.07370
Capurso A, Solfrizzi V, Panza F, Mastroianni F, Torres F, Del Parigi A, Colacicco AM, Capurso C, Nicoletti G, Veneziani B, Cellamare S, Scalabrino A (1999) Increased bile acid excretion and reduction of serum cholesterol after crenotherapy with salt-rich mineral water. Aging (Milano) 11(4):273–276
Carbajo JM (2014) Evaluación de los cambios en la piel tras la aplicación de cosméticos elaborados a partir del sedimento de las aguas minero-medicinales Lanjarón-Capuchina mediante métodos de bioingenieria cutánea. PhD Thesis, Universidad Complutense Madrid
Carbajo JM, Fernández-Torán MA, Corvillo I, Aguilera L, Meijide R, Carretero MI, Maraver F (2014) Biophysical skin effects of extemporaneous peloids from “Hervideros de Cofrentes Spa” natural mineral water according to their maturity time. J Jpn Soc Balneol Climatol Phys Med 77:507–508. https://doi.org/10.11390/onki.77.507
Carretero MI, Pozo M, Martin-Rubi JA, Pozo E, Maraver F (2010) Mobility of elements in interaction between artificial sweat and peloids used in Spanish spa. Appl Clay Sci 48:506–515. https://doi.org/10.1016/j.clay.2010.02.016
Chalfie M (2009) Neurosensory mechanotransduction. Nat Rev Mol Cell Biol 10:44–52. https://doi.org/10.1038/nrm2595
Chamberlin ME, Strange K (1989) Anisosmotic cell volume regulation: a comparative view. Am J Phys 257(2 Pt 1):C159–C173. https://doi.org/10.1152/ajpcell.1989.257.2.C159
Chary-Valckenaere I, Loeuille D, Jay N, Kohler F, Tamisier JN, Roques CF, Boulange M, Gay G (2018) Spa therapy together with supervised self-mobilisation improves pain, function and quality of life in patients with chronic shoulder pain: a single-blind randomised controlled trial. Int J Biometeorol. https://doi.org/10.1007/s00484-018-1502-x
Chen Y, Shen Y, Guo X, Zhang C, Yang W, Ma M, Liu S, Zhang M, Wen LP (2006) Transdermal protein delivery by a coadministered peptide identified via phage display. Nat Biotechnol 24:455–460
Chen L, Lian G, Han L (2010) Modeling transdermal permeation. Part I. Predicting skin permeability of both hydrophobic and hydrophilic solutes. AICHE J:561136–561146. https://doi.org/10.1002/aic.12048
Chen L, Han L, Lian G (2013) Recent advances in predicting skin permeability of hydrophilic solutes. Adv Drug Deliv Rev 65:295–305. https://doi.org/10.1016/j.addr.2012.05.001
Chizmadzhev YA, Indenbom AV, Kuzmin PI, Galichenko SV, Weaver JC, Potts RO (1998) Electrical properties of skin at moderate voltages: contribution of appendageal macropores. Biophys J 74(2 Pt 1):843–856. https://doi.org/10.1016/S0006-3495(98)74008-1
Ciprian L, Lo Nigro A, Rizzo M, Gava A, Ramonda R, Punzi L, Cozzi F (2013) The effects of combined spa therapy and rehabilitation on patients with ankylosing spondylitis being treated with TNF inhibitors. Rheumatol Int 33:241–245. https://doi.org/10.1007/s00296-011-2147-9
Clowes HM, Scott RC, Heylings JR (1994) Skin absorption: flow-through or static diffusion cells. Toxicol in Vitro 8:827–830. https://doi.org/10.1016/0887-2333(94)90078-7
Codish S, Abu-Shakra M, Flusser D, Friger M, Sukenik S (2005) Mud compress therapy for the hands of patients with rheumatoid arthritis. Rheumatol Int 25:49–54. https://doi.org/10.1007/s00296-003-0402-4
Constant F, Collin JF, Guillemin F, Boulangé M (1995) Effectiveness of spa therapy in chronic low back pain: a randomized clinical trial. J Rheumatol 22:1315–1320
Coste B, Mathur J, Schmidt M, Earley TJ, Ranade S, Petrus MJ, Dubin AE, Patapoutian A (2010) Piezo1 and Piezo2 are essential components of distinct mechanically activated cation channels. Science 330:55–60. https://doi.org/10.1126/science.1193270
Coste B, Xiao B, Santos JS, Syeda R, Grandl J, Spencer KS, Kim SE, Schmidt M, Mathur J, Dubin AE, Montal M, Patapoutian A (2012) Piezo proteins are pore-forming subunits of mechanically activated channels. Nature 483:176–181. https://doi.org/10.1038/nature10812
Cozzi F, Podswiadek M, Cardinale G, Oliviero F, Dani L, Sfriso P, Punzi L (2007) Mud-bath treatment in spondylitis associated with inflammatory bowel disease—a pilot randomised clinical trial. Joint Bone Spine 74:436–439. https://doi.org/10.1016/j.jbspin.2006.12.003
Cozzi F, Raffeiner B, Beltrame V, Ciprian L, Coran A, Botsios C, Perissinotto E, Grisan E, Ramonda R, Oliviero F, Stramare R, Punzi L (2015) Effects of mud-bath therapy in psoriatic arthritis patients treated with TNF inhibitors. Clinical evaluation and assessment of synovial inflammation by contrast-enhanced ultrasound (CEUS). Joint Bone Spine 82:104–108. https://doi.org/10.1016/j.jbspin.2014.11.002
Czarnowicki T, Harari M, Ruzicka T, Ingber A (2011) Dead Sea climatotherapy for vitiligo: a retrospective study of 436 patients. J Eur Acad Dermatol Venereol 25:959–963. https://doi.org/10.1111/j.1468-3083.2010.03903.x
Davies PF (1995) Flow-mediated endothelial mechanotransduction. Physiol Rev 75:519–560. https://doi.org/10.1152/physrev.1995.75.3.519
de Andrade SC, de Carvalho RF, Soares AS, de Abreu Freitas RP, de Medeiros Guerra LM, Vilar MJ (2008) Thalassotherapy for fibromyalgia: a randomized controlled trial comparing aquatic exercises in sea water and water pool. Rheumatol Int 29:147–152. https://doi.org/10.1007/s00296-008-0644-2
De Palma A, Cheleschi S, Pascarelli NA, Tenti S, Galeazzi M, Fioravanti A (2017) Do MicroRNAs have a key epigenetic role in osteoarthritis and in mechanotransduction? Clin Exp Rheumatol 35:518–526
Değim Z, Celebi N, Sayan H, Babül A, Erdoğan D, Take G (2002) An investigation on skin wound healing in mice with a taurine-chitosan gel formulation. Amino Acids 22:187–198. https://doi.org/10.1007/s007260200007
Dönmez A, Karagülle MZ, Tercan N, Dinler M, Işsever H, Karagülle M, Turan M (2005) SPA therapy in fibromyalgia: a randomised controlled clinic study. Rheumatol Int 26:168–172. https://doi.org/10.1007/s00296-005-0623-9
Dubin AE, Schmidt M, Mathur J, Petrus MJ, Xiao B, Coste B, Patapoutian A (2012) Inflammatory signals enhance piezo2-mediated mechanosensitive currents. Cell Rep 2:511–517. https://doi.org/10.1016/j.celrep.2012.07.014
Duparc-Ricoux S, Monnet P, Fabry R (2004) Thalassotherapy: complementary or competitor of the hydro-mineral cure? Press Therm Clim 141:71–77
Eisenhoffer GT, Loftus PD, Yoshigi M, Otsuna H, Chien CB, Morcos PA, Rosenblatt J (2012) Crowding induces live cell extrusion to maintain homeostatic cell numbers in epithelia. Nature 484:546–549. https://doi.org/10.1038/nature10999
Elias PM, Brown BE, Fritsch P, Goerke J, Gray GM, White RJ (1979) Localization and composition of lipids in neonatal mouse stratum granulosum and stratum corneum. J Invest Dermatol 73:339–348. https://doi.org/10.1111/1523-1747.ep12550377
Elkayam O, Wigler I, Tishler M, Rosenblum I, Caspi D, Segal R, Fishel B, Yaron M (1991) Effect of spa therapy in Tiberias on patients with rheumatoid arthritis and osteoarthritis. J Rheumatol 18:1799–1803
Elsing C, Gosch I, Hennings JC, Hübner CA, Herrmann T (2007) Mechanisms of hypotonic inhibition of the sodium, proton exchanger type 1 (NHE1) in a biliary epithelial cell line (Mz-Cha-1). Acta Physiol (Oxf) 190:199–208. https://doi.org/10.1111/j.1748-1716.2007.01682.x
Eyckmans J, Boudou T, Yu X, Chen CS (2011) A hitchhiker's guide to mechanobiology. Dev Cell 21:35–47. https://doi.org/10.1016/j.devcel.2011.06.015
Faucherre A, Kissa K, Nargeot J, Mangoni ME, Jopling C (2014) Piezo1 plays a role in erythrocyte volume homeostasis. Haematologica 99:70–75. https://doi.org/10.3324/haematol.2013.086090
Fazaa A, Souabni L, Ben Abdelghani K, Kassab S, Chekili S, Zouari B, Hajri R, Laatar A, Zakraoui L (2014) Comparison of the clinical effectiveness of thermal cure and rehabilitation in knee osteoarthritis. A randomized therapeutic trial. Ann Phys Rehabil Med 57(9–10):561–569. https://doi.org/10.1016/j.rehab.2014.09.007
Felix SH (1999) Thalassotherapy in paediatrics. Press Therm Clim 136:249–250
Fioravanti A, Perpignano G, Tirri G, Cardinale G, Gianniti C, Lanza CE, Loi A, Tirri E, Sfriso P, Cozzi F (2007) Effects of mud-bath treatment on fibromialgia patients: a randomized clinical trial. Rheumatol Int 27:1157–1161. https://doi.org/10.1007/s00296-007-0358-x
Fioravanti A, Cantarini L, Guidelli GM, Galeazzi M (2011) Mechanisms of action of spa therapies in rheumatic diseases: what scientific evidence is there? Rheumatol Int 31:1–8. https://doi.org/10.1007/s00296-010-1628-6
Fioravanti A, Karagülle M, Bender T, Karagülle MZ (2017) Balneotherapy in osteoarthritis: facts, fiction and gaps in knowledge. Eur J Integr Med 9:148–150. https://doi.org/10.1016/j.eujim.2017.01.001
Flusser D, Abu-Shakra M, Friger M, Codish S, Sukenik S (2002) Therapy with mud compresses for knee osteoarthritis: comparison of natural mud preparations with mineral-depleted mud. J Clin Rheumatol 8:197–203. https://doi.org/10.1097/01.RHU.0000022542.38402.A9
Friberg SE, Osborne DW (1985) Small angle x-ray diffraction patterns of stratum corneum and a model structure for its lipids. J Disp Sci Techn 6:485–495
Gambichler T, Demetriou C, Terras S, Bechara FG, Skrygan M (2011) The impact of salt water soaks on biophysical and molecular parameters in psoriatic epidermis equivalents. Dermatology 223:230–238. https://doi.org/10.1159/000332983
Geng J, Zhao Q, Zhang T, Xiao B (2017) In touch with the mechanosensitive piezo channels: structure, ion permeation, and mechanotransduction. Curr Top Membr 79:159–195. https://doi.org/10.1016/bs.ctm.2016.11.006
Gomes C, Carretero MI, Pozo M, Maraver F, Cantista P, Armijo F, Legido JL, Teixeira F, Rautureau M, Delgado R (2013) Peloids and pelotherapy: historical evolution, classification and glossary. Appl Clay Sci 75–76:28–38. https://doi.org/10.1016/j.clay.2013.02.008
Gottlieb PA, Sachs F (2012) Piezo1: properties of a cation selective mechanical channel. Channels (Austin) 6:214–219. https://doi.org/10.4161/chan.21050
Gottlieb PA, Bae C, Sachs F (2012) Gating the mechanical channel Piezo1: a comparison between whole-cell and patch recording. Channels (Austin) 6:282–289. https://doi.org/10.4161/chan.21064
Grozeva A, Stoicheva M (2015) Thalassotherapy in diabetic polyneuropathy: a study in Pomorie, Bulgaria. J Jpn Soc Balneol Climatol Phys Med 78:271–275. https://doi.org/10.11390/onki.78.271
Gu Y, Gu C (2014) Physiological and pathological functions of mechanosensitive ion channels. Mol Neurobiol 50:339–347. https://doi.org/10.1007/s12035-014-8654-4
Gudipaty SA, Lindblom J, Loftus PD, Redd MJ, Edes K, Davey CF, Krishnegowda V, Rosenblatt J (2017) Mechanical stretch triggers rapid epithelial cell division through Piezo1. Nature 543:118–121. https://doi.org/10.1038/nature21407
Guidelli GM, Tenti S, De Nobili E, Fioravanti A (2012) Fibromyalgia syndrome and spa therapy: myth or reality? Clin Med Insights Arthritis Musculoskelet Disord 5:19–26. https://doi.org/10.4137/CMAMD.S8797
Gutenbrunner C, Bender T, Cantista P, Karagülle Z (2010) A proposal for a worldwide definition of health resort medicine, balneology, medical hydrology and climatology. Int J Biometeorol 54:495–507. https://doi.org/10.1007/s00484-010-0321-5
Halevy S, Sukenik S (1998) Different modalities of spa therapy for skin diseases at the Dead Sea area. Arch Dermatol 134:1416–1420. https://doi.org/10.1001/archderm.134.11.1416
Halevy S, Giryes H, Friger M, Grossman N, Karpas Z, Sarov B, Sukenik S (2001) The role of trace elements in psoriatic patients undergoing balneotherapy with Dead Sea bath salt. Isr Med Assoc J 3:828–832
Hallows KR, Knauf PA (1994) Principles of cell volume regulation. In: Strange K (ed) Cellular and molecular physiology of cell volume regulation. CRC Press, Boca Raton, pp 3–29
Hansen S, Henning A, Naegel A, Heisig M, Wittum G, Neumann D, Kostka KH, Zbytovska J, Lehr CM, Schaefer UF (2008) In-silico model of skin penetration based on experimentally determined input parameters. Part I: experimental determination of partition and diffusion coefficients. Eur J Pharm Biopharm 68:352–367. https://doi.org/10.1016/j.ejpb.2007.05.012
Hanzel A, Horvát K, Molics B, Berényi K, Németh B, Szendi K, Varga C (2018) Clinical improvement of patients with osteoarthritis using thermal mineral water at Szigetvár spa-results of a randomised double-blind controlled study. Int J Biometeorol 62:253–259. https://doi.org/10.1007/s00484-017-1446-6
Hao J, Delmas P (2010) Multiple desensitization mechanisms of mechanotransducer channels shape firing of mechanosensory neurons. J Neurosci 30:13384–13395. https://doi.org/10.1523/JNEUROSCI.2926-10.2010
Hathout RM, Mansour S, Mortada ND, Geneidi AS, Guy RH (2010) Uptake of microemulsion components into the stratum corneum and their molecular effects on skin barrier function. Mol Pharm 7:1266–1273. https://doi.org/10.1021/mp100068s
Häussinger D (1996) The role of cellular hydration in the regulation of cell function. Biochem J 313:697–710. https://doi.org/10.1042/bj3130697
Hoffmann EK, Dunham PB (1995) Membrane mechanisms and intracellular signalling in cell volume regulation. Int Rev Cytol 161:173–262. https://doi.org/10.1016/S0074-7696(08)62498-5
Hoffmann EK, Lambert IH, Pedersen SF (2009) Physiology of cell volume regulation in vertebrates. Physiol Rev 89:193–277. https://doi.org/10.1152/physrev.00037.2007
Ikeda R, Cha M, Ling J, Jia Z, Coyle D, Gu JG (2014) Merkel cells transduce and encode tactile stimuli to drive Aβ-afferent impulses. Cell 157:664–675. https://doi.org/10.1016/j.cell.2014.02.026
Jacobi U, Tassopoulos T, Surber C, Lademann J (2006) Cutaneous distribution and localization of dyes affected by vehicles all with different lipophilicity. Arch Dermatol Res 297:303–310. https://doi.org/10.1007/s00403-005-0621-5
Jakab M, Fürst J, Gschwentner M, Bottà G et al (2002) Mechanisms sensing and modulating signals arising from cell swelling. Cell Physiol Biochem 12:235–258. https://doi.org/10.1159/000067895
Jia Z, Ikeda R, Ling J, Viatchenko-Karpinski V, Gu JG (2016) Regulation of Piezo2 mechanotransduction by static plasma membrane tension in primary afferent neurons. J Biol Chem 291:9087–9104. https://doi.org/10.1074/jbc.M115.692384
Kalia YN, Naik A, Garrison J, Guy RH (2004) Iontophoretic drug delivery. Adv Drug Deliv Rev 56:619–658. https://doi.org/10.1016/j.addr.2003.10.026
Karagülle MZ, Karagülle M (2004) Balneotherapy and spa therapy of rheumatic diseases in Turkey: a systematic review. Forsch Komplementarmed Klass Naturheilkd 11:33–41. https://doi.org/10.1159/000077194
Karagülle M, Karagülle MZ (2015) Effectiveness of balneotherapy and spa therapy for the treatment of chronic low back pain: a review on latest evidence. Clin Rheumatol 34:207–214. https://doi.org/10.1007/s10067-014-2845-2
Karagülle M, Karagülle MZ, Karagülle O, Dönmez A, Turan M (2007) A 10-day course of SPA therapy is beneficial for people with severe knee osteoarthritis. A 24-weekrandomised, controlled pilot study. Clin Rheumatol 26:2063–2071. https://doi.org/10.1007/s10067-007-0618-x
Karagülle M, Kardeş S, Karagülle O, Dişçi R, Avcı A, Durak İ, Karagülle MZ (2017a) Effect of spa therapy with saline balneotherapy on oxidant/antioxidant status in patients with rheumatoid arthritis: a single-blind randomized controlled trial. Int J Biometeorol 61:169–180. https://doi.org/10.1007/s00484-016-1201-4
Karagülle M, Kardeş S, Karagülle MZ (2017b) Real-life effectiveness of spa therapy in rheumatic and musculoskeletal diseases: a retrospective study of 819 patients. Int J Biometeorol 61:1945–1956. https://doi.org/10.1007/s00484-017-1384-3
Karagülle M, Kardeş S, Dişçi R, Karagülle MZ (2018a) Spa therapy adjunct to pharmacotherapy is beneficial in rheumatoid arthritis: a crossover randomized controlled trial. Int J Biometeorol 62:195–205. https://doi.org/10.1007/s00484-017-1441-y
Karagülle M, Kardeş S, Karagülle MZ (2018b) Long-term efficacy of spa therapy in patients with rheumatoid arthritis. Rheumatol Int 38:353–362. https://doi.org/10.1007/s00296-017-3926-8
Kardeş S, Karagülle M, Geçmen İ, Adıgüzel T, Yücesoy H, Karagülle MZ (2018) Outpatient balneological treatment of osteoarthritis in older persons: a retrospective study. Z Gerontol Geriatr. https://doi.org/10.1007/s00391-018-1370-3
Kasting GB, Barai ND, Wang TF, Nitsche JM (2003) Mobility of water in human stratum corneum. J Pharm Sci 92:2326–2340. https://doi.org/10.1002/jps.10483
Katz U, Shoenfeld Y, Zakin V, Sherer Y, Sukenik S (2012) Scientific evidence of the therapeutic effects of dead sea treatments: a systematic review. Semin Arthritis Rheum 42:186–200. https://doi.org/10.1016/j.semarthrit.2012.02.006
Kazandjieva J, Grozdev I, Darlenski R, Tsankov N (2008) Climatotherapy of psoriasis. Clin Dermatol 26(5):477–485
Kesiktas N, Karakas S, Gun K, Gun N, Murat S, Uludag M (2012) Balneotherapy for chronic low back pain: a randomized, controlled study. Rheumatol Int 32(10):3193–3199
Kim JH, Lee J, Lee HB, Shin JH, Kim EK (2010) Water-retentive and anti-inflammatory properties of organic and inorganic substances from Korean sea mud. Nat Prod Commun 5:395–398
Kleinewietfeld M, Manzel A, Titze J, Kvakan H, Yosef N, Linker RA, Muller DN, Hafler DA (2013) Sodium chloride drives autoimmune disease by the induction of pathogenic TH17 cells. Nature 496(7446):518–522. https://doi.org/10.1038/nature11868
Kopel E, Levi A, Harari M, Ruzicka T, Ingber A (2013) Effect of the Dead Sea climatotherapy for psoriasis on quality of life. Isr Med Assoc J 15:99–102
Koser DE, Thompson AJ, Foster SK, Dwivedy A, Pillai EK, Sheridan GK, Svoboda H, Viana M, Costa LD, Guck J, Holt CE, Franze K (2016) Mechanosensing is critical for axon growth in the developing brain. Nat Neurosci 19:1592–1598. https://doi.org/10.1038/nn.4394
Kulisch A, Bender T, Németh A, Szekeres L (2009) Effect of thermal water and adjunctive electrotherapy on chronic low back pain: a double-blind, randomized, follow-up study. J Rehabil Med 41:73–79. https://doi.org/10.2340/16501977-0291
Kung C, Martinac B, Sukharev S (2010) Mechanosensitive channels in microbes. Annu Rev Microbiol 64:313–329. https://doi.org/10.1146/annurev.micro.112408.134106
Kushner J, Kim D, So PT, Blankschtein D, Langer RS (2007) Dual-channel two-photon miscroscopy study of transdermal transport in skin treated with low-frequency ultrasound and a chemical enhancer. J Invest Dermatol 127:2832–2846. https://doi.org/10.1038/sj.jid.5700908
Lang F, Waldegger S (1997) Regulating cell volume. Am Sci 85:456–463
Lang F, Busch GL, Ritter M, Völkl H, Waldegger S, Gulbins E, Häussinger D (1998) Functional significance of cell volume regulatory mechanisms. Physiol Rev 78:247–306. https://doi.org/10.1152/physrev.1998.78.1.247
Léauté-Labrèze C, Saillour F, Chêne G, Cazenave C, Luxey-Bellocq ML, Sanciaume C, Toussaint JF, Taïeb A (2001) Saline spa water or combined water and UV-B for psoriasis vs conventional UV-B: lessons from the Salies de Béarn randomized study. Arch Dermatol 137:1035–1039
Lee W, Leddy HA, Chen Y, Lee SH, Zelenski NA, McNulty AL, Wu J, Beicker KN, Coles J, Zauscher S, Grandl J, Sachs F, Guilak F, Liedtke WB (2014) Synergy between Piezo1 and Piezo2 channels confers high-strain mechanosensitivity to articular cartilage. Proc Natl Acad Sci U S A 111:E5114–E5122. https://doi.org/10.1073/pnas.1414298111
Levin CY, Maibach HI (2001) Do cool water or physiologic saline compresses enhance resolution of experimentally-induced irritant contact dermatitis? Contact Dermatitis 45:146–150. https://doi.org/10.1034/j.1600-0536.2001.045003146.x
Lewis AH, Cui AF, McDonald MF, Grandl J (2017) Transduction of repetitive mechanical stimuli by Piezo1 and Piezo2 ion channels. Cell Rep 19:2572–2585. https://doi.org/10.1016/j.celrep.2017.05.079
Li J, Hou B, Tumova S, Muraki K, Bruns A, Ludlow MJ, Sedo A, Hyman AJ, McKeown L, Young RS, Yuldasheva NY, Majeed Y, Wilson LA, Rode B, Bailey MA, Kim HR, Fu Z, Carter DAL, Bilton J, Imrie H, Ajuh P, Dear TN, Cubbon RM, Kearney MT, Prasad KR, Evans PC, Ainscough JFX, Beech DJ (2014) Piezo1 integration of vascular architecture with physiological force. Nature 515:279–282. https://doi.org/10.1038/nature13701
Lian G, Chen L, Han L (2008) An evaluation of mathematical models for predicting skin permeability. J Pharm Sci 97:584–598. https://doi.org/10.1002/jps.21074
Lucchetta MC, Monaco G, Valenzi VI, Russo MV, Campanella J, Nocchi S, Mennuni G, Fraioli A (2007) The historical-scientific foundations of thalassotherapy: state of the art. Clin Ter 158:533–541
MacLeod RJ (1994) How an epithelial cell swells is a determinant of the signaling pathways that activate RVD. In: Strange K (ed) Cellular and molecular physiology of cell volume regulation. CRC Press, Boca Raton, pp 191–200
Mahboob N, Sousan K, Shirzad A, Amir G, Mohammad V, Reza M, Mansour VA, Hadi V (2009) The efficacy of a topical gel prepared using Lake Urmia mud in patients with knee osteoarthritis. J Altern Complement Med 15:1239–1242. https://doi.org/10.1089/acm.2009.0304
Maksimovic S, Nakatani M, Baba Y, Nelson AM, Marshall KL, Wellnitz SA, Firozi P, Woo SH, Ranade S, Patapoutian A, Lumpkin EA (2014) Epidermal Merkel cells are mechanosensory cells that tune mammalian touch receptors. Nature 509:617–621. https://doi.org/10.1038/nature13250
Maraver F, Armijo F (2010) Vademecum II de aguas mineromedicinales españolas. Complutense, Madrid
Maraver F, Michan A, Morer C, Aguilera L (2011) Is thalassotherapy simply a type of climatotherapy? Int J Biometeorol 55:107–108. https://doi.org/10.1007/s00484-010-0382-5
Maraver F, Fernández-Torán MA, Corvillo I, Morer C, Vázquez I, Aguilera L, Armijo F (2015) Pelotherapy, a review. Med Naturista 9:38–46
Maroto R, Raso A, Wood TG, Kurosky A, Martinac B, Hamill OP (2005) TRPC1 forms the stretch-activated cation channel in vertebrate cells. Nat Cell Biol 7:179–185. https://doi.org/10.1038/ncb1218
Martins JR, Penton D, Peyronnet R, Arhatte M, Moro C, Picard N, Kurt B, Patel A, Honoré E, Demolombe S (2016) Piezo1-dependent regulation of urinary osmolarity. Pflugers Arch 468:1197–1206. https://doi.org/10.1007/s00424-016-1811-z
Matz H, Orion E, Wolf R (2003) Balneotherapy in dermatology. Dermatol Ther 16:132–140. https://doi.org/10.1046/j.1529-8019.2003.01622.x
McHugh BJ, Murdoch A, Haslett C, Sethi T (2012) Loss of the integrin-activating transmembrane protein Fam38A (Piezo1) promotes a switch to a reduced integrin-dependent mode of cell migration. PLoS One 7:e40346. https://doi.org/10.1371/journal.pone.0040346
Michaels AS, Chandrasekaran SK, Shaw JE (1975) Drug permeation through human skin: theory and in-vitro experimental measurement. AICHE J 21:985–996. https://doi.org/10.1002/aic.690210522
Miller MA, Yu F, Kim KI, Kasting GB (2017) Uptake and desorption of hydrophilic compounds from human stratum corneum. J Control Release 261:307–317. https://doi.org/10.1016/j.jconrel.2017.06.015
Miraglia Del Giudice M, Decimo F, Maiello N, Leonardi S, Parisi G, Golluccio M, Capasso M, Balestrieri U, Rocco A, Perrone L, Ciprandi G (2011) Effectiveness of ischia thermal water nasal aerosol in children with seasonal allergic rhinitis: a randomized and controlled study. Int J Immunopathol Pharmacol 24(4):1103–1109. https://doi.org/10.1177/039463201102400431
Mitragotri S (2003) Modeling skin permeability to hydrophilic and hydrophobic solutes based on four permeation pathways. J Control Release 86:69–92. https://doi.org/10.1016/S0168-3659(02)00321-8
Mitragotri S, Blankschtein D, Langer R (1996) Transdermal drug delivery using low-frequency sonophoresis. Pharm Res 13:411–420
Mitragotri S, Anissimov YG, Bunge AL, Frasch HF, Guy RH, Hadgraft J, Kasting GB, Lane ME, Roberts MS (2011) Mathematical models of skin permeability: an overview. Int J Pharm 418:115–129. https://doi.org/10.1016/j.ijpharm.2011.02.023
Mohd Nani SZ, Majid FA, Jaafar AB, Mahdzir A, Musa MN (2016) Potential health benefits of deep sea water: a review. Evid Based Complement Alternat Med 2016:6520475–6520418. https://doi.org/10.1155/2016/6520475
Morer C (2016a) Talasoterapia y enfermedad neurológica. PhD Thesis, Universidad Complutense Madrid
Morer C (2016b) Talasoterapia. Bol Soc Esp Hidrol Med 31:119–146. https://doi.org/10.23853/bsehm.2017.0209
Morer C, Boestad C, Zuluaga P, Alvarez-Badillo A, Maraver F (2017a) Effects of an intensive thalassotherapy and aquatic therapy program in stroke patients. A pilot study. Rev Neurol 65:249–256
Morer C, Roques CF, Françon A, Forestier R, Maraver F (2017b) The role of mineral elements and other chemical compounds used in balneology: data from double-blind randomized clinical trials. Int J Biometeorol 61:2159–2173. https://doi.org/10.1007/s00484-017-1421-2
Moufarrij S, Deghayli L, Raffoul W, Hirt-Burri N, Michetti M, de Buys RA, Norberg M, Applegate LA (2014) How important is hydrotherapy? Effects of dynamic action of hot spring water as a rehabilitative treatment for burn patients in Switzerland. Ann Burns Fire Disasters 27:184–191
Müller S, Quast T, Schröder A, Hucke S, Klotz L, Jantsch J, Gerzer R, Hemmersbach R, Kolanus W (2013) Salt-dependent chemotaxis of macrophages. PLoS One 8(9):e73439. https://doi.org/10.1371/journal.pone.0073439
Murthy SE, Dubin AE, Patapoutian A (2017) Piezos thrive under pressure: mechanically activated ion channels in health and disease. Nat Rev Mol Cell Biol 18:771–783. https://doi.org/10.1038/nrm.2017.92
Naegel A, Hansen S, Neumann D, Lehr CM, Schaefer UF, Wittum G, Heisig M (2008) In-silico model of skin penetration based on experimentally determined input parameters. Part II: mathematical modelling of in-vitro diffusion experiments. Identification of critical input parameters. Eur J Pharm Biopharm 68:368–379. https://doi.org/10.1016/j.ejpb.2007.05.018
Nakagawa N, Sakai S, Matsumoto M, Yamada K, Nagano M, Yuki T, Sumida Y, Uchiwa H (2004) Relationship between NMF (lactate and potassium) content and the physical properties of the stratum corneum in healthy subjects. J Invest Dermatol 122:755–763. https://doi.org/10.1111/j.0022-202X.2004.22317.x
Nasermoaddeli A, Kagamimori S (2005) Balneotherapy in medicine: a review. Environ Health Prev Med 10(4):171–179
Nastos VE (2010) Saline mud therapy for headache secondary to cervical osteoarthritis. In: proceedings of the international conference; international congress. Spa therapy with saline waters in health resorts. Österr Z Phys Med Rehabil 20:56
Nicoletti G, Corbella M, Jaber O, Marone P, Scevola D, Faga A (2015) Non-pathogenic microflora of a spring water with regenerative properties. Biomed Rep 3:758–762. https://doi.org/10.3892/br.2015.507
Nilius B (2010) Pressing and squeezing with Piezos. EMBO Rep 11:902–903. https://doi.org/10.1038/embor.2010.181
Nissen JB, Avrach WW, Hansen ES, Stengaard-Pedersen K, Kragballe K (1998) Increased levels of enkephalin following natural sunlight (combined with salt water bathing at the Dead Sea) and ultraviolet A irradiation. Br J Dermatol 139:1012–1019. https://doi.org/10.1046/j.1365-2133.1998.02557.x
Nitsche JM, Wang TF, Kasting GB (2006) A two-phase analysis of solute partitioning into the stratum corneum. J Pharm Sci 95:649–666. https://doi.org/10.1002/jps.20549
Nonomura K, Woo SH, Chang RB, Gillich A, Qiu Z, Francisco AG, Ranade SS, Liberles SD, Patapoutian A (2017) Piezo2 senses airway stretch and mediates lung inflation-induced apnoea. Nature 541:176–181. https://doi.org/10.1038/nature20793
Norlén L (2007) Nanostructure of the stratum corneum extracellular lipid matrix as observed by cryo-electron microscopy of vitreous skin sections. Int J Cosmet Sci 29:335–352. https://doi.org/10.1111/j.1468-2494.2007.00395.x
Okada Y, Maeno E, Shimizu T, Dezaki K, Wang J, Morishima S (2001) Receptor-mediated control of regulatory volume decrease (RVD) and apoptotic volume decrease (AVD). J Physiol 532:3–16. https://doi.org/10.1111/j.1469-7793.2001.0003g.x
O'Neill WC (1999) Physiological significance of volume-regulatory transporters. Am J Phys 276(5 Pt 1):C995–C1011. https://doi.org/10.1152/ajpcell.1999.276.5.C995
Orlov SN, Hamet P (2015) Salt and gene expression: evidence for [Na+]i/[K+]i-mediated signaling pathways. Pflugers Arch 467:489–498. https://doi.org/10.1007/s00424-014-1650-8
Özkuk K, Gürdal H, Karagülle M, Barut Y, Eröksüz R, Karagülle MZ (2017) Balneological outpatient treatment for patients with knee osteoarthritis; an effective non-drug therapy option in daily routine? Int J Biometeorol 61:719–728. https://doi.org/10.1007/s00484-016-1250-8
Ozkurt S, Dönmez A, Zeki Karagülle M, Uzunoğlu E, Turan M, Erdoğan N (2012) Balneotherapy in fibromyalgia: a single blind randomized controlled clinical study. Rheumatol Int 32(7):1949–1954. https://doi.org/10.1007/s00296-011-1888-9
Pappas A (2009) Epidermal surface lipids. Dermato-endocrinology 1:72–76
Pathak MM, Nourse JL, Tran T, Hwe J, Arulmoli J, Le DT, Bernardis E, Flanagan LA, Tombola F (2014) Stretch-activated ion channel Piezo1 directs lineage choice in human neural stem cells. Proc Natl Acad Sci U S A 111:16148–16153. https://doi.org/10.1073/pnas.1409802111
Polefka TG, Bianchini RJ, Shapiro S (2012) Interaction of mineral salts with the skin: a literature survey. Int J Cosmet Sci 34:416–423. https://doi.org/10.1111/j.1468-2494.2012.00731.x
Potts RO, Francoeur ML (1991) The influence of stratum corneum morphology on wáter permeability. J Invest Dermatol 96:495–499. https://doi.org/10.1016/0022-202X(91)90455-Y
Potts RO, Guy RH (1992) Predicting skin permeability. Pharm Res 9:663–669. https://doi.org/10.1023/A:1015810312465
Proksch E, Nissen HP, Bremgartner M, Urquhart C (2005) Bathing in a magnesium-rich Dead Sea salt solution improves skin barrier function, enhances skin hydration, and reduces inflammation in atopic dry skin. Int J Dermatol 44:151–157. https://doi.org/10.1111/j.1365-4632.2005.02079.x
Ranade SS, Woo SH, Dubin AE, Moshourab RA, Wetzel C, Petrus M, Mathur J, Bégay V, Coste B, Mainquist J, Wilson AJ, Francisco AG, Reddy K, Qiu Z, Wood JN, Lewin GR, Patapoutian A (2014) Piezo2 is the major transducer of mechanical forces for touch sensation in mice. Nature 516:121–125. https://doi.org/10.1038/nature13980
Ranade SS, Syeda R, Patapoutian A (2015) Mechanically activated ion channels. Neuron 87:1162–1179. https://doi.org/10.1016/j.neuron.2015.08.032
Rawlings AV, Harding CR (2004) Moisturization and skin barrier function. Dermatol Ther 17(Suppl 1):43–48. https://doi.org/10.1111/j.1396-0296.2004.04S1005.x
Retailleau K, Duprat F, Arhatte M, Ranade SS, Peyronnet R, Martins JR, Jodar M, Moro C, Offermanns S, Feng Y, Demolombe S, Patel A, Honoré E (2015) Piezo1 in smooth muscle cells is involved in hypertension-dependent arterial remodeling. Cell Rep 13:1161–1171. https://doi.org/10.1016/j.celrep.2015.09.072
Rogozian BN, Efimenko NV, Kaĭsinova AS, Babiakin AF (2011) Thalassotherapy for the patients suffering osteoarthrosis. The medical technology. Vopr Kurortol Fizioter Lech Fiz Kult 88:51–54. https://doi.org/10.17116/kurort2011651-54
Rosette C, Karin M (1996) Ultraviolet light and osmotic stress: activation of the JNK cascade through multiple growth factor and cytokine receptors. Science 274:1194–1197. https://doi.org/10.1126/science.274.5290.1194
Sasaki Y, Sathi GA, Yamamoto O (2017) Wound healing effect of bioactive ion released from Mg-smectite. Mater Sci Eng C Mater Biol Appl 77:52–57. https://doi.org/10.1016/j.msec.2017.03.236
Schiener R, Brockow T, Franke A, Salzer B, Peter RU, Resch KL (2007) Bath PUVA and saltwater baths followed by UV-B phototherapy as treatments for psoriasis: a randomized controlled trial. Arch Dermatol 143:586–596. https://doi.org/10.1001/archderm.143.5.586
Schuh A (2009) Die Evidenz der Klima- und Thalassotherapie. Ein Review. Schweiz Z Ganzheitsmed 21:96–104. https://doi.org/10.1159/000287219
Servin-Vences MR, Moroni M, Lewin GR, Poole K (2017) Direct measurement of TRPV4 and PIEZO1 activity reveals multiple mechanotransduction pathways in chondrocytes. elife 6:e21074. https://doi.org/10.7554/eLife.21074
Simon F, Varela D, Eguiguren AL, Díaz LF, Sala F, Stutzin A (2004) Hydroxyl radical activation of a Ca(2+)-sensitive nonselective cation channel involved in epithelial cell necrosis. Am J Physiol Cell Physiol 287:C963–C970. https://doi.org/10.1152/ajpcell.00041.2004
Southwell D, Barry BW, Woodford R (1984) Variations in permeability of human skin within and between specimens. Int J Pharm 18:299–309. https://doi.org/10.1016/0378-5173(84)90145-5
Spilioti E, Vargiami M, Letsiou S, Gardikis K, Sygouni V, Koutsoukos P, Chinou I, Kassi E, Moutsatsou P (2017) Biological properties of mud extracts derived from various spa resorts. Environ Geochem Health 39(4):821–833. https://doi.org/10.1007/s10653-016-9852-y
Staffieri A, Miani C, Bergamin AM, Arcangeli P, Canzi P (1998) Effect of sulfur salt-bromine-iodine thermal waters on albumin and IgA concentrations in nasal secretions. Acta Otorhinolaryngol Ital 18(4):233–238
Strange K (2004) Cellular volume homeostasis. Adv Physiol Educ 28(1–4):155–159
Suchyna TM (2017) Piezo channels and GsMTx4: two milestones in our understanding of excitatory mechanosensitive channels and their role in pathology. Prog Biophys Mol Biol 130(Pt B):244–253. https://doi.org/10.1016/j.pbiomolbio.2017.07.011
Sukenik S, Neumann L, Buskila D, Kleiner-Baumgarten A, Zimlichman S, Horowitz J (1990) Dead Sea bath salts for the treatment of rheumatoid arthritis. Clin Exp Rheumatol 8:353–357
Sukenik S, Buskila D, Neumann L, Kleiner-Baumgarten A (1992) Mud pack therapy in rheumatoid arthritis. Clin Rheumatol 11:243–247. https://doi.org/10.1007/BF02207966
Sukenik S, Giryes H, Halevy S, Neumann L, Flusser D, Buskila D (1994) Treatment of psoriatic arthritis at the Dead Sea. J Rheumatol 21:1305–1309
Sukenik S, Neumann L, Flusser D, Kleiner-Baumgarten A, Buskila D (1995) Balneotherapy for rheumatoid arthritis at the Dead Sea. Isr J Med Sci 31:210–214
Sukenik S, Flusser D, Abu-Shakra M (1999) The role of spa therapy in various rheumatic diseases. Rheum Dis Clin N Am 25:883–897
Taimor G, Lorenz H, Hofstaetter B, Schlüter KD, Piper HM (1999) Induction of necrosis but not apoptosis after anoxia and reoxygenation in isolated adult cardiomyocytes of rat. Cardiovasc Res 41:147–156
Talreja P, Kleene NK, Pickens WL, Wang TF, Kasting GB (2001) Visualization of the lipid barrier and measurement of lipid path length in human stratum corneum. AAPS PharmSci 3:E13
Tang H, Blankschtein D, Langer R (2002) Prediction of steady-state skin permeabilities of polar and nonpolar permeants across excised pig skin based on measurements of transient diffusion: characterization of hydration effects on the skin porous pathway. J Pharm Sci 91:1891–1907. https://doi.org/10.1002/jps.10177
Tefner IK, Németh A, Lászlófi A, Kis T, Gyetvai G, Bender T (2012) The effect of spa therapy in chronic low back pain: a randomized controlled, single-blind, follow-up study. Rheumatol Int 32(10):3163–3169
Tenti S, Cheleschi S, Galeazzi M, Fioravanti A (2015) Spa therapy: can be a valid option for treating knee osteoarthritis? Int J Biometeorol 59:1133–1143. https://doi.org/10.1007/s00484-014-0913-6
Tezel A, Sens A, Mitragotri S (2003) Description of transdermal transport of hydrophilic solutes during low-frequency sonophoresis based on a modified porous pathway model. J Pharm Sci 92:381–393. https://doi.org/10.1002/jps.10299
Tsoureli-Nikita E, Menchini G, Ghersetich I, Hercogova J (2002) Alternative treatment of psoriasis with balneotherapy using Leopoldine spa water. J Eur Acad Dermatol Venereol 16:260–262
Tyler WJ (2012) The mechanobiology of brain function. Nat Rev Neurosci 13:867–878. https://doi.org/10.1038/nrn3383
van Kemenade PM, Houben MM, Huyghe JM, Douven LF (2004) Do osmotic forces play a role in the uptake of water by human skin? Skin Res Technol 10:109–112. https://doi.org/10.1111/j.1600-0846.2004.00059.x
Ventura SA, Kasting GB (2017) Dynamics of glycerine and water transport across human skin from binary mixtures. Int J Cosmet Sci 39:165–178. https://doi.org/10.1111/ics.12362
Verkman AS, Mitra AK (2000) Structure and function of aquaporin water channels. Am J Physiol Renal Physiol 278:F13–F28. https://doi.org/10.1152/ajprenal.2000.278.1.F13
Walsh CM, Bautista DM, Lumpkin EA (2015) Mammalian touch catches up. Curr Opin Neurobiol 34:133–139. https://doi.org/10.1016/j.conb.2015.05.003
Wang TF, Kasting GB, Nitsche JM (2007) A multiphase microscopic diffusion model for stratum corneum permeability. II. Estimation of physicochemical parameters, and application to a large permeability database. J Pharm Sci 96:3024–3051. https://doi.org/10.1002/jps.20883
Wehner F, Olsen H, Tinel H, Kinne-Saffran E, Kinne RK (2003) Cell volume regulation: osmolytes, osmolyte transport, and signal transduction. Rev Physiol Biochem Pharmacol 148:1–80. https://doi.org/10.1007/s10254-003-0009-x
Welch WJ, Brown CR (1996) Influence of molecular and chemical chaperones on protein folding. Cell Stress Chaperones 1:109–115
Wertz PW, Swartzendruber DC, Madison KC, Downing DT (1987) Composition and morphology of epidermal cyst lipids. J Invest Dermatol 89:419–425
Wiedow O, Streit V, Christophers E, Ständer M (1989) Liberation of human leukocyte elastase by hypertonic saline baths in psoriasis. Hautarzt 40:518–522
Wigler I, Elkayam O, Paran D, Yaron M (1995) Spa therapy for gonarthrosis: a prospective study. Rheumatol Int 15:65–68. https://doi.org/10.1007/BF00262710
Wiig H, Schröder A, Neuhofer W, Jantsch J, Kopp C, Karlsen TV, Boschmann M, Goss J, Bry M, Rakova N, Dahlmann A, Brenner S, Tenstad O, Nurmi H, Mervaala E, Wagner H, Beck FX, Müller DN, Kerjaschki D, Luft FC, Harrison DG, Alitalo K, Titze J (2013) Immune cells control skin lymphatic electrolyte homeostasis and blood pressure. J Clin Invest 123:2803–2815. https://doi.org/10.1172/JCI60113
Wiig H, Luft FC, Titze JM (2018) The interstitium conducts extrarenal storage of sodium and represents a third compartment essential for extracellular volume and blood pressure homeostasis. Acta Physiol (Oxf) 222:e13006. https://doi.org/10.1111/apha.13006
Woo SH, Ranade S, Weyer AD, Dubin AE, Baba Y, Qiu Z, Petrus M, Miyamoto T, Reddy K, Lumpkin EA, Stucky CL, Patapoutian A (2014) Piezo2 is required for Merkel-cell mechanotransduction. Nature 509(7502):622–626. https://doi.org/10.1038/nature13251
Woo SH, Lukacs V, de Nooij JC, Zaytseva D, Criddle CR, Francisco A, Jessell TM, Wilkinson KA, Patapoutian A (2015a) Piezo2 is the principal mechanotransduction channel for proprioception. Nat Neurosci 18:1756–1762. https://doi.org/10.1038/nn.4162
Woo SH, Lumpkin EA, Patapoutian A (2015b) Merkel cells and neurons keep in touch. Trends Cell Biol 25:74–81. https://doi.org/10.1016/j.tcb.2014.10.003
Wright AR, Rees SA (1998) Cardiac cell volume: crystal clear or murky waters? A comparison with other cell types. Pharmacol Ther 80:89–121. https://doi.org/10.1016/S0163-7258(98)00025-4
Wu J, Lewis AH, Grandl J (2017) Touch, tension, and transduction—the function and regulation of piezo ion channels. Trends Biochem Sci 42:57–71. https://doi.org/10.1016/j.tibs.2016.09.004
Xu XZ (2016) Demystifying mechanosensitive piezo ion channels. Neurosci Bull 32:307–309. https://doi.org/10.1007/s12264-016-0033-x
Yancey PH, Clark ME, Hand SC, Bowlus RD, Somero GN (1982) Living with water stress: evolution of osmolyte systems. Science 217:1214–1222. https://doi.org/10.1126/science.7112124
Yoshizawa Y, Tanojo H, Kim SJ, Maibach HI (2001) Sea water or its components alter experimental irritant dermatitis in man. Skin Res Technol 7:36–39. https://doi.org/10.1034/j.1600-0846.2001.007001036.x
Yoshizawa Y, Kitamura K, Kawana S, Maibach HI (2003) Water, salts and skin barrier of normal skin. Skin Res Technol 9:31–33. https://doi.org/10.1034/j.1600-0846.2003.00346.x
Zhang T, Chi S, Jiang F, Zhao Q, Xiao B (2017) A protein interaction mechanism for suppressing the mechanosensitive Piezo channels. Nat Commun 8:1797. https://doi.org/10.1038/s41467-017-01712-z
Zijlstra TR, van de Laar MA, Bernelot Moens HJ, Taal E, Zakraoui L, Rasker JJ (2005) Spa treatment for primary fibromyalgia syndrome: a combination of thalassotherapy, exercise and patient education improves symptoms and quality of life. Rheumatology (Oxford) 44:539–546. https://doi.org/10.1093/rheumatology/keh537
Zöller N, Valesky E, Hofmann M, Bereiter-Hahn J, Bernd A, Kaufmann R, Meissner M, Kippenberger S (2015) Impact of different spa waters on inflammation parameters in human keratinocyte HaCaT cells. Ann Dermatol 27:709–714. https://doi.org/10.5021/ad.2015.27.6.709
Funding
This study was funded by grant UCM-911757 awarded to the research group of the Universidad Complutense de Madrid (Medical Hydrology).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Rights and permissions
About this article
Cite this article
Carbajo, J.M., Maraver, F. Salt water and skin interactions: new lines of evidence. Int J Biometeorol 62, 1345–1360 (2018). https://doi.org/10.1007/s00484-018-1545-z
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00484-018-1545-z