Novel techniques to enhance wound healing
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Published:
Apr 12, 2019
Keywords:
electrical stimulation low intensity laser therapy shockwave therapy ultrasound therapy wound healing
Main Article Content
Abstract
Wound healing is a complex, dynamic and multifaceted biological process. Wound repair is mainly similar at all anatomical sites and can be divided into four major phases including hemostatic phase, inflammatory phase, proliferative phase and remodeling phase. Interrupted or failure during healing process can lead to chronic wound healing. Chronic wound healing is the most common complication in veterinary practice. This condition leads to painful, uncomfortable and later consequently died, as well as leads time consuming and cost of treatment. Currently, physical therapy modalities in the wound healing process have been developed and widely used for adjunctive therapy in veterinary medicine, including electrical stimulation, shockwave therapy, ultrasound therapy and low intensity laser therapy to enhance wound healing. The biological effects of electrical stimulation are result of exogenous electrical signals and are amplifying the biological signal into target tissue. The mechanism of shockwave therapy and ultrasound therapy are the consequence of cavitation phenomenon, activated cellular activity, and increase tissue perfusion. Meanwhile, mean mechanism of low intensity laser therapy is known to supply direct biostimulative light energy to target cells, and to initiate cellular processes. These modalities deliver physical energy to produce therapeutic biological effect, especially inflammatory phase and proliferative phase. Importantly, the biological effects produced by these modalities are including supported the proper environment for healing process, increasing phagocytosis by macrophages, leukocyte adhesion, growth factor production, angiogenesis, collagen synthesis, fibroblast synthesis and granulation tissue formation. In additions, physical energy may affect into the remodeling stage by increasing wound breaking strength.
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Review articles
References
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Bjordal, J.M., Johnson, M.I., Iversen, V., Aimbire, F., Lopes-Martins, R.A. 2006. Low-level laser therapy in acute pain: a systematic review of possible mechanisms of action and clinical effects in randomized placebo-controlled trials. Photomed Laser Surg. 24 (2), 158-168.
Broughton, G., 2nd, Janis, J.E., Attinger, C.E. 2006. Wound healing: an overview. Plast Reconstr Surg. 117(7 Suppl), DOI: 10.1097/1001.prs.0000222562.0000260260.f0000222569.
Chaussy, C., Schmiedt, E., Jocham, D., Brendel, W., Forssmann, B., Walther, V. 2002. First clinical experience with extracorporeally induced destruction of kidney stones by shock waves. 1981. J Urol. 167 (2), 844-847.
Chester, D., Brown, A.C. 2017. The role of biophysical properties of provisional matrix proteins in wound repair. Matrix Biology. 60-61, 124-140.
Demir, H., Balay, H., Kirnap, M. 2004. A comparative study of the effects of electrical stimulation and laser treatment on experimental wound healing in rats. J Rehabil Res Dev. 41 (2), 147-154.
Diegelmann, R.F., Evans, M.C. 2004. Wound healing: an overview of acute, fibrotic and delayed healing. Front Biosci. 9, 283-289.
Ebrahimi, T., Moslemi, N., Rokn, A., Heidari, M., Nokhbatolfoghahaie, H., Fekrazad, R. 2012. The influence of low-intensity laser therapy on bone healing. J Dent (Tehran). 9 (4), 238-248.
Ennis, W.J., Lee, C., Gellada, K., Corbiere, T.F., Koh, T.J. 2016. Advanced technologies to improve wound healing: electrical stimulation, vibration therapy, and ultrasound-what is the evidence? Plast Reconstr Surg. 138 (3 Suppl), 94S-104S.
Enoch, S., Leaper, D.J. 2005. Basic science of wound healing. surgery. 23 (2), 37-42.
Evans, D.H., Abrahamse, H. 2008. Efficacy of three different laser wavelengths for in vitro wound healing. Photodermatol Photoimmunol Photomed. 24 (4), 199-210.
Fantinati, M.S., Mendonca, D.E., Fantinati, A.M., Santos, B.F., Reis, J.C., Afonso, C.L., Vinaud, M.C., Lino Rde, S.J. 2016. Low intensity ultrasound therapy induces angiogenesis and persistent inflammation in the chronic phase of the healing process of third degree burn wounds experimentally induced in diabetic and non-diabetic rats. Acta Cir Bras. 31 (7), 463-471.
Feitosa, M.C., Carvalho, A.F., Feitosa, V.C., Coelho, I.M., Oliveira, R.A., Arisawa, E.A. 2015. Effects of the low-level laser therapy (LLLT) in the process of healing diabetic foot ulcers. Acta Cir Bras. 30 (12), 852-857.
Guo, S., Dipietro, L.A. 2010. Factors affecting wound healing. J Dent Res. 89 (3), 219-229.
Gupta, A., Keshri, G.K., Yadav, A., Gola, S., Chauhan, S., Salhan, A.K., Bala Singh, S. 2015. Superpulsed (Ga-As, 904 nm) low-level laser therapy (LLLT) attenuates inflammatory response and enhances healing of burn wounds. J Biophotonics. 8 (6), 489-501.
Hayashi, D., Kawakami, K., Ito, K., Ishii, K., Tanno, H., Imai, Y., Kanno, E., Maruyama, R., Shimokawa, H., Tachi, M. 2012. Low-energy extracorporeal shock wave therapy enhances skin wound healing in diabetic mice: a critical role of endothelial nitric oxide synthase. Wound Repair Regen. 20 (6), 887-895.
Hoffman, M., Monroe, D.M. 2012. Low intensity laser therapy speeds wound healing in hemophilia by enhancing platelet procoagulant activity. Wound Repair Regen. 20 (5), 770-777.
Janis, J.E., Harrison, B. 2016. Wound healing: part I. basic science. Plast Reconstr Surg. 138 (3 Suppl), 10.1097/PRS.0000000000002773.
Karu, T. 1989. Photobiology of low-power laser effects. Health Phys. 56 (5), 691-704.
Kavros, S.J., Liedl, D.A., Boon, A.J., Miller, J.L., Hobbs, J.A., Andrews, K.L. 2008. Expedited wound healing with noncontact, low-frequency ultrasound therapy in chronic wounds: a retrospective analysis. Adv Skin Wound Care. 21 (9), 416-423.
Khan, I., Arany, P. 2015. Biophysical approaches for oral wound healing: emphasis on photobiomodulation. Adv Wound Care (New Rochelle). 4 (12), 724-737.
Kisch, T., Sorg, H., Forstmeier, V., Mailaender, P., Kraemer, R. 2015. Fractionated repetitive extracorporeal shock wave therapy: a new standard in shock wave therapy? Biomed Res Int. 2015, 10.1155/2015/454981.
Kloth, L.C. 2014. Electrical stimulation technologies for wound healing. Adv Wound Care (New Rochelle). 3 (2), 81-90.
Krukowska, J., Wrona, J., Sienkiewicz, M., Czernicki, J. 2016. A comparative analysis of analgesic efficacy of ultrasound and shock wave therapy in the treatment of patients with inflammation of the attachment of the plantar fascia in the course of calcaneal spurs. Arch Orthop Trauma Surg. 136 (9), 1289-1296.
Kuo, Y.R., Wang, C.T., Wang, F.S., Chiang, Y.C., Wang, C.J. 2009. Extracorporeal shock-wave therapy enhanced wound healing via increasing topical blood perfusion and tissue regeneration in a rat model of STZ-induced diabetes. Wound Repair Regen. 17 (4), 522-530.
Maan, Z.N., Januszyk, M., Rennert, R.C., Duscher, D., Rodrigues, M., Fujiwara, T., Ho, N., Whitmore, A., Hu, M.S., Longaker, M.T., Gurtner, G.C. 2014. Noncontact, low-frequency ultrasound therapy enhances neovascularization and wound healing in diabetic mice. Plast Reconstr Surg. 134 (3), DOI: 10.1097/PRS.0000000000000467.
Marinho, R.R., Matos, R.M., Santos, J.S., Ribeiro, M.A., Smaniotto, S., Barreto, E.O., Ribeiro, R.A., Lima, R.C., Jr., Albuquerque, R.L., Jr., Thomazzi, S.M. 2013. Potentiated anti-inflammatory effect of combined 780 nm and 660 nm low level laser therapy on the experimental laryngitis. J Photochem Photobiol B. 121, DOI: 10.1016/j.jphotobiol.2013.02.012.
McClure, S., Dorfmuller, C. 2003. Extracorporeal shock wave therapy: theory and equipment. Clinical Techniques in Equine Practice. 2 (4), 348-357.
Mester, E., Mester, A.F., Mester, A. 1985. The biomedical effects of laser application. Lasers Surg Med. 5 (1), 31-39.
Mittermayr, R., Antonic, V., Hartinger, J., Kaufmann, H., Redl, H., Teot, L., Stojadinovic, A., Schaden, W. 2012. Extracorporeal shock wave therapy (ESWT) for wound healing: technology, mechanisms, and clinical efficacy. Wound Repair Regen. 20 (4), 456-465.
Mizutani, K., Aoki, A., Coluzzi, D., Yukna, R., Wang, C.Y., Pavlic, V., Izumi, Y. 2016. Lasers in minimally invasive periodontal and peri-implant therapy. Periodontol 2000. 71 (1), 185-212.
Omar, M.T., Alghadir, A., Al-Wahhabi, K.K., Al-Askar, A.B. 2014. Efficacy of shock wave therapy on chronic diabetic foot ulcer: a single-blinded randomized controlled clinical trial. Diabetes Res Clin Pract. 106 (3), 548-554.
Reinke, J.M., Sorg, H. 2012. Wound repair and regeneration. Eur Surg Res. 49 (1), 35-43.
Rosinczuk, J., Taradaj, J., Dymarek, R., Sopel, M. 2016. Mechanoregulation of wound healing and skin homeostasis. Biomed Res Int. 2016. DOI: 10.1155/2016/3943481.
Sadava, E.E., Krpata, D.M., Gao, Y., Rosen, M.J., Novitsky, Y.W. 2014. Wound healing process and mediators: Implications for modulations for hernia repair and mesh integration. J Biomed Mater Res A. 102 (1), 295-302.
Schaden, W., Thiele, R., Kolpl, C., Pusch, M., Nissan, A., Attinger, C.E., Maniscalco-Theberge, M.E., Peoples, G.E., Elster, E.A., Stojadinovic, A. 2007. Shock wave therapy for acute and chronic soft tissue wounds: a feasibility study. J Surg Res. 143 (1), 1-12.
Schreml, S., Szeimies, R.M., Prantl, L., Karrer, S., Landthaler, M., Babilas, P. 2010. Oxygen in acute and chronic wound healing. Br J Dermatol. 163 (2), 257-268.
Shalaby, T.I., Nasra, M. K., Mohamed, M. M., Eldine, R.S. 2013. Effect of visible laser therapy on wound healing dynamics in diabetic induced mice. Romanian J.Biophys. 23, 1-14.
Singer, A.J., Clark, R.A. 1999. Cutaneous wound healing. N Engl J Med. 341 (10), 738-746.
Sinno, H., Prakash, S. 2013. Complements and the wound healing cascade: an updated review. Plast Surg Int. 2013, DOI: 10.1155/2013/146764.
Speed, C.A. 2001. Therapeutic ultrasound in soft tissue lesions. Rheumatology (Oxford). 40(12), 1331-1336.
Talebi, G., Torkaman, G., Firoozabadi, M., Shariat, S. 2008. Effect of anodal and cathodal microamperage direct current electrical stimulation on injury potential and wound size in guinea pigs. J Rehabil Res Dev. 45 (1), 153-159.
Thakral, G., Lafontaine, J., Najafi, B., Talal, T.K., Kim, P., Lavery, L.A. 2013. Electrical stimulation to accelerate wound healing. Diabet Foot Ankle. 4, DOI: 10.3402/dfa.v4i0.22081.
Ud-Din, S., Sebastian, A., Giddings, P., Colthurst, J., Whiteside, S., Morris, J., Nuccitelli, R., Pullar, C., Baguneid, M., Bayat, A. 2015. Angiogenesis is induced and wound size is reduced by electrical stimulation in an acute wound healing model in human skin. PLoS One. 10 (4), DOI: 10.1371/journal.pone.0124502.
Yang, G., Luo, C., Yan, X., Cheng, L., Chai, Y. 2011. Extracorporeal shock wave treatment improves incisional wound healing in diabetic rats. Tohoku J Exp Med. 225 (4), 285-292.
Zecha, J.A., Raber-Durlacher, J.E., Nair, R.G., Epstein, J.B., Sonis, S.T., Elad, S., Hamblin, M.R., Barasch, A., Migliorati, C.A., Milstein, D.M., Genot, M.T., Lansaat, L., van der Brink, R., Arnabat-Dominguez, J., van der Molen, L., Jacobi, I., van Diessen, J., de Lange, J., Smeele, L.E., Schubert, M.M., Bensadoun, R.J. 2016. Low level laser therapy/photobiomodulation in the management of side effects of chemoradiation therapy in head and neck cancer: part 1: mechanisms of action, dosimetric, and safety considerations. Support Care Cancer. 24 (6), 2781-2792.
Zins, S.R., Amare, M.F., Tadaki, D.K., Elster, E.A., Davis, T.A. 2010. Comparative analysis of angiogenic gene expression in normal and impaired wound healing in diabetic mice: effects of extracorporeal shock wave therapy. Angiogenesis. 13 (4), 293-304.
Bjordal, J.M., Johnson, M.I., Iversen, V., Aimbire, F., Lopes-Martins, R.A. 2006. Low-level laser therapy in acute pain: a systematic review of possible mechanisms of action and clinical effects in randomized placebo-controlled trials. Photomed Laser Surg. 24 (2), 158-168.
Broughton, G., 2nd, Janis, J.E., Attinger, C.E. 2006. Wound healing: an overview. Plast Reconstr Surg. 117(7 Suppl), DOI: 10.1097/1001.prs.0000222562.0000260260.f0000222569.
Chaussy, C., Schmiedt, E., Jocham, D., Brendel, W., Forssmann, B., Walther, V. 2002. First clinical experience with extracorporeally induced destruction of kidney stones by shock waves. 1981. J Urol. 167 (2), 844-847.
Chester, D., Brown, A.C. 2017. The role of biophysical properties of provisional matrix proteins in wound repair. Matrix Biology. 60-61, 124-140.
Demir, H., Balay, H., Kirnap, M. 2004. A comparative study of the effects of electrical stimulation and laser treatment on experimental wound healing in rats. J Rehabil Res Dev. 41 (2), 147-154.
Diegelmann, R.F., Evans, M.C. 2004. Wound healing: an overview of acute, fibrotic and delayed healing. Front Biosci. 9, 283-289.
Ebrahimi, T., Moslemi, N., Rokn, A., Heidari, M., Nokhbatolfoghahaie, H., Fekrazad, R. 2012. The influence of low-intensity laser therapy on bone healing. J Dent (Tehran). 9 (4), 238-248.
Ennis, W.J., Lee, C., Gellada, K., Corbiere, T.F., Koh, T.J. 2016. Advanced technologies to improve wound healing: electrical stimulation, vibration therapy, and ultrasound-what is the evidence? Plast Reconstr Surg. 138 (3 Suppl), 94S-104S.
Enoch, S., Leaper, D.J. 2005. Basic science of wound healing. surgery. 23 (2), 37-42.
Evans, D.H., Abrahamse, H. 2008. Efficacy of three different laser wavelengths for in vitro wound healing. Photodermatol Photoimmunol Photomed. 24 (4), 199-210.
Fantinati, M.S., Mendonca, D.E., Fantinati, A.M., Santos, B.F., Reis, J.C., Afonso, C.L., Vinaud, M.C., Lino Rde, S.J. 2016. Low intensity ultrasound therapy induces angiogenesis and persistent inflammation in the chronic phase of the healing process of third degree burn wounds experimentally induced in diabetic and non-diabetic rats. Acta Cir Bras. 31 (7), 463-471.
Feitosa, M.C., Carvalho, A.F., Feitosa, V.C., Coelho, I.M., Oliveira, R.A., Arisawa, E.A. 2015. Effects of the low-level laser therapy (LLLT) in the process of healing diabetic foot ulcers. Acta Cir Bras. 30 (12), 852-857.
Guo, S., Dipietro, L.A. 2010. Factors affecting wound healing. J Dent Res. 89 (3), 219-229.
Gupta, A., Keshri, G.K., Yadav, A., Gola, S., Chauhan, S., Salhan, A.K., Bala Singh, S. 2015. Superpulsed (Ga-As, 904 nm) low-level laser therapy (LLLT) attenuates inflammatory response and enhances healing of burn wounds. J Biophotonics. 8 (6), 489-501.
Hayashi, D., Kawakami, K., Ito, K., Ishii, K., Tanno, H., Imai, Y., Kanno, E., Maruyama, R., Shimokawa, H., Tachi, M. 2012. Low-energy extracorporeal shock wave therapy enhances skin wound healing in diabetic mice: a critical role of endothelial nitric oxide synthase. Wound Repair Regen. 20 (6), 887-895.
Hoffman, M., Monroe, D.M. 2012. Low intensity laser therapy speeds wound healing in hemophilia by enhancing platelet procoagulant activity. Wound Repair Regen. 20 (5), 770-777.
Janis, J.E., Harrison, B. 2016. Wound healing: part I. basic science. Plast Reconstr Surg. 138 (3 Suppl), 10.1097/PRS.0000000000002773.
Karu, T. 1989. Photobiology of low-power laser effects. Health Phys. 56 (5), 691-704.
Kavros, S.J., Liedl, D.A., Boon, A.J., Miller, J.L., Hobbs, J.A., Andrews, K.L. 2008. Expedited wound healing with noncontact, low-frequency ultrasound therapy in chronic wounds: a retrospective analysis. Adv Skin Wound Care. 21 (9), 416-423.
Khan, I., Arany, P. 2015. Biophysical approaches for oral wound healing: emphasis on photobiomodulation. Adv Wound Care (New Rochelle). 4 (12), 724-737.
Kisch, T., Sorg, H., Forstmeier, V., Mailaender, P., Kraemer, R. 2015. Fractionated repetitive extracorporeal shock wave therapy: a new standard in shock wave therapy? Biomed Res Int. 2015, 10.1155/2015/454981.
Kloth, L.C. 2014. Electrical stimulation technologies for wound healing. Adv Wound Care (New Rochelle). 3 (2), 81-90.
Krukowska, J., Wrona, J., Sienkiewicz, M., Czernicki, J. 2016. A comparative analysis of analgesic efficacy of ultrasound and shock wave therapy in the treatment of patients with inflammation of the attachment of the plantar fascia in the course of calcaneal spurs. Arch Orthop Trauma Surg. 136 (9), 1289-1296.
Kuo, Y.R., Wang, C.T., Wang, F.S., Chiang, Y.C., Wang, C.J. 2009. Extracorporeal shock-wave therapy enhanced wound healing via increasing topical blood perfusion and tissue regeneration in a rat model of STZ-induced diabetes. Wound Repair Regen. 17 (4), 522-530.
Maan, Z.N., Januszyk, M., Rennert, R.C., Duscher, D., Rodrigues, M., Fujiwara, T., Ho, N., Whitmore, A., Hu, M.S., Longaker, M.T., Gurtner, G.C. 2014. Noncontact, low-frequency ultrasound therapy enhances neovascularization and wound healing in diabetic mice. Plast Reconstr Surg. 134 (3), DOI: 10.1097/PRS.0000000000000467.
Marinho, R.R., Matos, R.M., Santos, J.S., Ribeiro, M.A., Smaniotto, S., Barreto, E.O., Ribeiro, R.A., Lima, R.C., Jr., Albuquerque, R.L., Jr., Thomazzi, S.M. 2013. Potentiated anti-inflammatory effect of combined 780 nm and 660 nm low level laser therapy on the experimental laryngitis. J Photochem Photobiol B. 121, DOI: 10.1016/j.jphotobiol.2013.02.012.
McClure, S., Dorfmuller, C. 2003. Extracorporeal shock wave therapy: theory and equipment. Clinical Techniques in Equine Practice. 2 (4), 348-357.
Mester, E., Mester, A.F., Mester, A. 1985. The biomedical effects of laser application. Lasers Surg Med. 5 (1), 31-39.
Mittermayr, R., Antonic, V., Hartinger, J., Kaufmann, H., Redl, H., Teot, L., Stojadinovic, A., Schaden, W. 2012. Extracorporeal shock wave therapy (ESWT) for wound healing: technology, mechanisms, and clinical efficacy. Wound Repair Regen. 20 (4), 456-465.
Mizutani, K., Aoki, A., Coluzzi, D., Yukna, R., Wang, C.Y., Pavlic, V., Izumi, Y. 2016. Lasers in minimally invasive periodontal and peri-implant therapy. Periodontol 2000. 71 (1), 185-212.
Omar, M.T., Alghadir, A., Al-Wahhabi, K.K., Al-Askar, A.B. 2014. Efficacy of shock wave therapy on chronic diabetic foot ulcer: a single-blinded randomized controlled clinical trial. Diabetes Res Clin Pract. 106 (3), 548-554.
Reinke, J.M., Sorg, H. 2012. Wound repair and regeneration. Eur Surg Res. 49 (1), 35-43.
Rosinczuk, J., Taradaj, J., Dymarek, R., Sopel, M. 2016. Mechanoregulation of wound healing and skin homeostasis. Biomed Res Int. 2016. DOI: 10.1155/2016/3943481.
Sadava, E.E., Krpata, D.M., Gao, Y., Rosen, M.J., Novitsky, Y.W. 2014. Wound healing process and mediators: Implications for modulations for hernia repair and mesh integration. J Biomed Mater Res A. 102 (1), 295-302.
Schaden, W., Thiele, R., Kolpl, C., Pusch, M., Nissan, A., Attinger, C.E., Maniscalco-Theberge, M.E., Peoples, G.E., Elster, E.A., Stojadinovic, A. 2007. Shock wave therapy for acute and chronic soft tissue wounds: a feasibility study. J Surg Res. 143 (1), 1-12.
Schreml, S., Szeimies, R.M., Prantl, L., Karrer, S., Landthaler, M., Babilas, P. 2010. Oxygen in acute and chronic wound healing. Br J Dermatol. 163 (2), 257-268.
Shalaby, T.I., Nasra, M. K., Mohamed, M. M., Eldine, R.S. 2013. Effect of visible laser therapy on wound healing dynamics in diabetic induced mice. Romanian J.Biophys. 23, 1-14.
Singer, A.J., Clark, R.A. 1999. Cutaneous wound healing. N Engl J Med. 341 (10), 738-746.
Sinno, H., Prakash, S. 2013. Complements and the wound healing cascade: an updated review. Plast Surg Int. 2013, DOI: 10.1155/2013/146764.
Speed, C.A. 2001. Therapeutic ultrasound in soft tissue lesions. Rheumatology (Oxford). 40(12), 1331-1336.
Talebi, G., Torkaman, G., Firoozabadi, M., Shariat, S. 2008. Effect of anodal and cathodal microamperage direct current electrical stimulation on injury potential and wound size in guinea pigs. J Rehabil Res Dev. 45 (1), 153-159.
Thakral, G., Lafontaine, J., Najafi, B., Talal, T.K., Kim, P., Lavery, L.A. 2013. Electrical stimulation to accelerate wound healing. Diabet Foot Ankle. 4, DOI: 10.3402/dfa.v4i0.22081.
Ud-Din, S., Sebastian, A., Giddings, P., Colthurst, J., Whiteside, S., Morris, J., Nuccitelli, R., Pullar, C., Baguneid, M., Bayat, A. 2015. Angiogenesis is induced and wound size is reduced by electrical stimulation in an acute wound healing model in human skin. PLoS One. 10 (4), DOI: 10.1371/journal.pone.0124502.
Yang, G., Luo, C., Yan, X., Cheng, L., Chai, Y. 2011. Extracorporeal shock wave treatment improves incisional wound healing in diabetic rats. Tohoku J Exp Med. 225 (4), 285-292.
Zecha, J.A., Raber-Durlacher, J.E., Nair, R.G., Epstein, J.B., Sonis, S.T., Elad, S., Hamblin, M.R., Barasch, A., Migliorati, C.A., Milstein, D.M., Genot, M.T., Lansaat, L., van der Brink, R., Arnabat-Dominguez, J., van der Molen, L., Jacobi, I., van Diessen, J., de Lange, J., Smeele, L.E., Schubert, M.M., Bensadoun, R.J. 2016. Low level laser therapy/photobiomodulation in the management of side effects of chemoradiation therapy in head and neck cancer: part 1: mechanisms of action, dosimetric, and safety considerations. Support Care Cancer. 24 (6), 2781-2792.
Zins, S.R., Amare, M.F., Tadaki, D.K., Elster, E.A., Davis, T.A. 2010. Comparative analysis of angiogenic gene expression in normal and impaired wound healing in diabetic mice: effects of extracorporeal shock wave therapy. Angiogenesis. 13 (4), 293-304.