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Infrared irradiation differentially alters collagen metabolism in lightly and darkly pigmented human skin in vivo
G Model DESC 2975 No. of Pages 3
Journal of Dermatological Science xxx (2015) xxx–xxx
Contents lists available at ScienceDirect
Journal of Dermatological Science journal homepage: www.jdsjournal.com
Letter to the Editor Infrared irradiation differentially alters collagen metabolism in lightly and darkly pigmented human skin in vivo
Excessive exposure to solar UV irradiation causes photoaging, which involves fragmentation of the dermal extracellular matrix (ECM) [1]. The ECM consists mostly of type I and type III collagen fibrils, which are synthesized as procollagen precursors [1,2]. Acute exposure of human skin to erythematous doses of solar UV irradiation, reduces synthesis of procollagens and increases expression of ECM-degrading matrix metalloproteinases (MMPs) [1]. Thus, UV irradiation impairs the structure and function of dermal collagen fibrils. UV irradiation accounts for approximately 7% of the electromagnetic irradiation reaching the earth’s surface, while infrared (IR) irradiation comprises approximately 54% [3]. In addition to natural sun exposure, humans can be exposed to IR irradiation from therapeutic or cosmetic devices [4,5]. IR irradiation is classified as IR-A (760–1400 nm), IR-B (1400– 3000 nm), and IR-C (3000 nm to 1 mm) [6]. IR-A accounts for approximately 30% of total solar energy and penetrates skin the deepest, reaching the subcuticular level [3]. Recent studies indicate that IR irradiation may elicit clinical and biological effects on human skin [3,7]. We investigated the effects of solar versus artificial IR irradiation and pigmentation on changes induced by IR irradiation in human skin. The study was approved by the Institutional Review Board of the University Michigan and conducted according to the Declaration of Helsinki principles. All subjects provided written, informed consent. Subjects had Fitzpatrick skin type I or II (light) or type IV or V (dark). For all subjects, adjacent non-irradiated buttock skin served as control. Skin samples (4 or 6 mm punch biopsies) were taken 24 h (h = hours) after irradiation. Biomarkers were compared using repeated measures analysis of variance. Specific time point comparisons were made using Dunnett’s test. Statistical significance was achieved if p 0.05 for a two-tailed hypothesis. Logarithmic transformation was performed for some data sets to achieve normality. Data were analyzed using statistical software (SAS Institute, Inc., Cary, NC). Initially, we examined the effects of water-filtered IR-A irradiation that simulates natural sun exposure. Buttock skin of lightly pigmented subjects (n = 22; 12 male, 10 female; ages 22– 64) was exposed to a water-filtered IR-A irradiation source (Hydrosun Medizintechnik, Mullheim, Germany) at a dose of 544 J/cm2, placed 20 cm from skin The temperature ranged from
Abbreviations: MMP, matrix metalloproteinase; IR, infrared; UV, ultraviolet.
39 to 42 C and exposure time was 30, 60, or 80 min (min = minutes). Following irradiation, there were no significant changes in gene expression of type I or III procollagen or MMP1 or -3 at any time point. Next, we examined whether water-filtered IR-A irradiation enhanced UV irradiation-induced changes in procollagen or MMP expression. Additional lightly pigmented subjects (n = 6) were exposed to water-filtered IR-A at 42 C for 30 min, UV-B irradiation alone (2 MED), and a combination of both, on separate buttock sites. For these subjects, skin samples were obtained at 24, 48, 72, and 96 h post-irradiation. Exposure to UV-B irradiation alone suppressed type I and III procollagen and induced MMP-1 and -3 expression 24 h post-irradiation. These alterations persisted for 48 h and subsided over another 48 h. Addition of IR-A irradiation to UV-B exposure did not alter procollagen or MMP expression, at any time point, compared with UV-B irradiation alone. Next we investigated the effects of unfiltered IR-A irradiation on lightly and darkly pigmented human skin. Buttock skin of subjects (n = 78; 62 light, 16 dark; 63 male,15 female; ages 23– 61), was also exposed to an unfiltered IR-A irradiation (0.43 W/ cm2 at a distance of 20 cm from skin), measured using a Nova II L40 (150) A-SH-V2 detector (Ophir-Spiricon Inc., Logan, UT). The lamp was placed 14 cm from subjects’ skin to achieve equivalent irradiation energy to the water-filtered source. Output of the lamp was controlled by a feedback controller that maintained a set skin surface temperature (measured with Fluke thermocouple thermometer 51/52 II, Everrett, WA). Exposure of buttock skin of lightly pigmented subjects at 41 C for 60 min suppressed gene expression of type I and III procollagen by approximately 50% (p < 0.05, Fig. 1a), whereas no significant changes occurred for MMP-1 or -3 gene expression (data not shown). At higher temperatures (43 C for 60 min, upper limit before mild pain, erythema, and/or blistering developed), gene expression of type I and III procollagen was suppressed by approximately 60% (p < 0.05, Fig. 1b), while expression of MMP-1 and -3 was induced by 80- and 60-fold, respectively (p < 0.05, Fig. 1c). Interestingly, IR-A irradiation of darkly pigmented, using the same conditions, did not alter expression of procollagen or MMP (data not shown). Finally, we investigated the effects of increased exposure of lightly and darkly pigmented human skin to IR-A irradiation. Increasing exposure of lightly pigmented skin from 60 to 90 min at 43 C did not further suppress type I or III procollagen expression (p < 0.05, Fig. 2a), but did lead to increased MMP-1 and -3 induction (p < 0.05, Fig. 2a). Increasing exposure of darkly pigmented skin to 90 min at 43 C resulted in alterations not observed at 60 min. Type I and III procollagen were suppressed approximately 50% (p < 0.05, Fig. 2b), and MMP-1 and -3 were induced by 500- and 45-fold,
http://dx.doi.org/10.1016/j.jdermsci.2016.03.010 0923-1811/ ã 2016 Published by Elsevier Ireland Ltd on behalf of Japanese Society for Investigative Dermatology.
Please cite this article in press as: N. Elbuluk, et al., Infrared irradiation differentially alters collagen metabolism in lightly and darkly pigmented human skin in vivo, J Dermatol Sci (2016), http://dx.doi.org/10.1016/j.jdermsci.2016.03.010
G Model DESC 2975 No. of Pages 3
2
Letter to the Editor / Journal of Dermatological Science xxx (2015) xxx–xxx
Fig. 1. Suppression of procollagens and MMPs in lightly pigmented human skin following exposure to unfiltered infrared irradiation mimicking artificial sources. (a) Buttock skin of healthy Caucasian subjects was exposed to a single dose of unfiltered IR-A irradiation for 60 min at 41 C. Skin samples were obtained 24 h later, and real-time quantitative polymerase chain reaction was performed to determine gene expression of type I and type III procollagen (n = 6). Data are shown as mean fold change, compared with non-irradiated buttock skin. Error bars indicate SEM. *p <0.05. (b) Suppression of procollagens in lightly pigmented human skin following increased intensity of exposure to unfiltered infrared irradiation mimicking artificial sources. Buttock skin of healthy Caucasian subjects (n = 16) was exposed to a single dose of unfiltered IR-A irradiation for 60 min at an increased temperature of 43 C. Skin samples were obtained 24 h later, and real-time quantitative polymerase chain reaction was performed to determine gene expression of type I and type III procollagen. Data are shown as mean fold change, compared with non-irradiated buttock skin. Error bars indicate SEM. *p< 0.05. (c) Suppression of MMPs in lightly pigmented human skin following increased intensity of exposure to unfiltered infrared irradiation mimicking artificial sources. Same methods use in part B were used to determine gene expression of and matrix metalloproteinases (MMP)-1 and -3.
respectively (p < 0.05, Fig. 2B). No statistically significant difference was found in procollagen or MMP expression between lightly and darkly pigmented skin. The above data indicate that limited exposure (60 min) to full spectrum IR-A irradiation that raises skin surface temperature to 43 C can promote and mimic some effects of UV exposure, including inhibition of collagen production and stimulation of MMPs. Interestingly, melanin appears to provide some protection against the effects of IR irradiation, since longer exposure time was required to elicit changes in darkly pigmented skin. This study
supports data from prior studies showing that infrared irradiation can affect collagen production, however to our knowledge, this study is the first to rigorously examine the protective role of melanin against IR irradiation [5,6,8]. These data support the concept that UV irradiation is the primary cause of photoaging-related changes in the dermal ECM. However, the data do not rule out the possibility that exposure to solar-simulated IR irradiation of higher temperature or longer duration may elicit changes in procollagen or MMP expression.
Please cite this article in press as: N. Elbuluk, et al., Infrared irradiation differentially alters collagen metabolism in lightly and darkly pigmented human skin in vivo, J Dermatol Sci (2016), http://dx.doi.org/10.1016/j.jdermsci.2016.03.010
G Model DESC 2975 No. of Pages 3
Letter to the Editor / Journal of Dermatological Science xxx (2015) xxx–xxx
3
Fig. 2. Suppression of procollagens and induction of MMPs in lightly pigmented and darkly pigmented human skin following increased intensity and duration of exposure to unfiltered infrared irradiation mimicking artificial sources. Buttock skin of (a) healthy Caucasian subjects (n = 12) and (b) African American subjects (n = 6) was exposed to a single dose of unfiltered IR-A irradiation for a longer duration (90 min) at an increased temperature of 43 C. Skin samples were obtained 24 h later, and real-time quantitative polymerase chain reaction was performed to determine gene expression of type I and type III procollagen, and matrix metalloproteinases (MMP)-1 and 3. Data are shown as mean fold change, compared with non-irradiated buttock skin. Error bars indicate SEM. *p < 0.05. When comparing the results between African American and Caucasian subjects, there was no statistical difference in the degree of suppression of type I and III procollagen or the induction of MMP-1 and MMP-3.
Conflict of interest The authors have no conflict of interest to declare. Acknowledgements The authors thank Suzan Rehbine, LPN, for assistance in procuring tissue samples; Laura VanGoor, BFA, for graphic illustrations; and Ted Hamilton, MS, for statistical analysis. The project was supported, in part, by Grant Number UL1RR024986 from the National Center for Research Resources. References [1] G.J. Fisher, Z.Q. Wang, S.C. Datta, J. Varani, S. Kang, J.J. Voorhees, Pathophysiology of premature skin aging induced by ultraviolet light, N. Engl. J. Med. 337 (1997) 1419–1428. [2] L.T. Smith, K.A. Holbrook, J.A. Madri, Collagen types I, III, and V in human embryonic and fetal skin, Am. J. Anat. 175 (1986) 507–521. [3] J.T.C. Krutmann, I. Kochevar, Fundamentals of cutaneous photobiology and photoimmunology, in: K.G.L. Wolfe, S. Katz, B. Gilchrest, A. Paller, D. Leffell (Eds.), Fitzpatrick’s Dermatology in General Medicine, McGraw Hill, New York, 2008. [4] K.D. Desmet, D.A. Paz, J.J. Corry, J.T. Eells, M.T. Wong-Riley, M.M. Henry, et al., Clinical and experimental applications of NIR-LED photobiomodulation, Photomed. Laser Surg. 24 (2006) 121–128. [5] P.S.S. Schroeder, A. Monta, Premature skin aging by infrared radition, tobacco smoke, and ozone, in: B.K.J. Gilchrest (Ed.), Skin Aging, Heidelberg, Springer, 2006, pp. 45–53. [6] S.M. Schieke, P. Schroeder, J. Krutmann, Cutaneous effects of infrared radiation: from clinical observations to molecular response mechanisms, Photodermatol. Photoimmunol. Photomed. 19 (2003) 228–234. [7] J.H. Chung, J.Y. Seo, H.R. Choi, M.K. Lee, C.S. Youn, G. Rhie, et al., Modulation of skin collagen metabolism in aged and photoaged human skin in vivo, J. Invest. Dermatol. 117 (2001) 1218–1224.
[8] S. Schieke, H. Stege, V. Kurten, S. Grether-Beck, H. Sies, J. Krutmann, Infrared-A radiation-induced matrix metalloproteinase 1 expression is mediated through extracellular signal-regulated kinase 1/2 activation in human dermal fibroblasts, J. Invest. Dermatol. 119 (2002) 1323–1329.
Nada Elbuluk* Ronald O. Perelman Department of Dermatology, NYU Langone Medical Center, New York, NY, USA Frank Wang, Bao Anh Patrick Tran Craig Hammerberg John J. Voorhees Department of Dermatology, University of Michigan School of Medicine, Ann Arbor, MI, USA, USA Sewon Kang Department of Dermatology, Johns Hopkins Hospital, Baltimore, MD, USA, USA Gary J. Fisher Department of Dermatology, University of Michigan School of Medicine, Ann Arbor, MI, USA, USA * Corresponding author. E-mail address: [email protected] (N. Elbuluk). Received 11 September 2015 Received in revised form 14 March 2016 Accepted 17 March 2016
Please cite this article in press as: N. Elbuluk, et al., Infrared irradiation differentially alters collagen metabolism in lightly and darkly pigmented human skin in vivo, J Dermatol Sci (2016), http://dx.doi.org/10.1016/j.jdermsci.2016.03.010
Journal of Dermatological Science xxx (2015) xxx–xxx
Contents lists available at ScienceDirect
Journal of Dermatological Science journal homepage: www.jdsjournal.com
Letter to the Editor Infrared irradiation differentially alters collagen metabolism in lightly and darkly pigmented human skin in vivo
Excessive exposure to solar UV irradiation causes photoaging, which involves fragmentation of the dermal extracellular matrix (ECM) [1]. The ECM consists mostly of type I and type III collagen fibrils, which are synthesized as procollagen precursors [1,2]. Acute exposure of human skin to erythematous doses of solar UV irradiation, reduces synthesis of procollagens and increases expression of ECM-degrading matrix metalloproteinases (MMPs) [1]. Thus, UV irradiation impairs the structure and function of dermal collagen fibrils. UV irradiation accounts for approximately 7% of the electromagnetic irradiation reaching the earth’s surface, while infrared (IR) irradiation comprises approximately 54% [3]. In addition to natural sun exposure, humans can be exposed to IR irradiation from therapeutic or cosmetic devices [4,5]. IR irradiation is classified as IR-A (760–1400 nm), IR-B (1400– 3000 nm), and IR-C (3000 nm to 1 mm) [6]. IR-A accounts for approximately 30% of total solar energy and penetrates skin the deepest, reaching the subcuticular level [3]. Recent studies indicate that IR irradiation may elicit clinical and biological effects on human skin [3,7]. We investigated the effects of solar versus artificial IR irradiation and pigmentation on changes induced by IR irradiation in human skin. The study was approved by the Institutional Review Board of the University Michigan and conducted according to the Declaration of Helsinki principles. All subjects provided written, informed consent. Subjects had Fitzpatrick skin type I or II (light) or type IV or V (dark). For all subjects, adjacent non-irradiated buttock skin served as control. Skin samples (4 or 6 mm punch biopsies) were taken 24 h (h = hours) after irradiation. Biomarkers were compared using repeated measures analysis of variance. Specific time point comparisons were made using Dunnett’s test. Statistical significance was achieved if p 0.05 for a two-tailed hypothesis. Logarithmic transformation was performed for some data sets to achieve normality. Data were analyzed using statistical software (SAS Institute, Inc., Cary, NC). Initially, we examined the effects of water-filtered IR-A irradiation that simulates natural sun exposure. Buttock skin of lightly pigmented subjects (n = 22; 12 male, 10 female; ages 22– 64) was exposed to a water-filtered IR-A irradiation source (Hydrosun Medizintechnik, Mullheim, Germany) at a dose of 544 J/cm2, placed 20 cm from skin The temperature ranged from
Abbreviations: MMP, matrix metalloproteinase; IR, infrared; UV, ultraviolet.
39 to 42 C and exposure time was 30, 60, or 80 min (min = minutes). Following irradiation, there were no significant changes in gene expression of type I or III procollagen or MMP1 or -3 at any time point. Next, we examined whether water-filtered IR-A irradiation enhanced UV irradiation-induced changes in procollagen or MMP expression. Additional lightly pigmented subjects (n = 6) were exposed to water-filtered IR-A at 42 C for 30 min, UV-B irradiation alone (2 MED), and a combination of both, on separate buttock sites. For these subjects, skin samples were obtained at 24, 48, 72, and 96 h post-irradiation. Exposure to UV-B irradiation alone suppressed type I and III procollagen and induced MMP-1 and -3 expression 24 h post-irradiation. These alterations persisted for 48 h and subsided over another 48 h. Addition of IR-A irradiation to UV-B exposure did not alter procollagen or MMP expression, at any time point, compared with UV-B irradiation alone. Next we investigated the effects of unfiltered IR-A irradiation on lightly and darkly pigmented human skin. Buttock skin of subjects (n = 78; 62 light, 16 dark; 63 male,15 female; ages 23– 61), was also exposed to an unfiltered IR-A irradiation (0.43 W/ cm2 at a distance of 20 cm from skin), measured using a Nova II L40 (150) A-SH-V2 detector (Ophir-Spiricon Inc., Logan, UT). The lamp was placed 14 cm from subjects’ skin to achieve equivalent irradiation energy to the water-filtered source. Output of the lamp was controlled by a feedback controller that maintained a set skin surface temperature (measured with Fluke thermocouple thermometer 51/52 II, Everrett, WA). Exposure of buttock skin of lightly pigmented subjects at 41 C for 60 min suppressed gene expression of type I and III procollagen by approximately 50% (p < 0.05, Fig. 1a), whereas no significant changes occurred for MMP-1 or -3 gene expression (data not shown). At higher temperatures (43 C for 60 min, upper limit before mild pain, erythema, and/or blistering developed), gene expression of type I and III procollagen was suppressed by approximately 60% (p < 0.05, Fig. 1b), while expression of MMP-1 and -3 was induced by 80- and 60-fold, respectively (p < 0.05, Fig. 1c). Interestingly, IR-A irradiation of darkly pigmented, using the same conditions, did not alter expression of procollagen or MMP (data not shown). Finally, we investigated the effects of increased exposure of lightly and darkly pigmented human skin to IR-A irradiation. Increasing exposure of lightly pigmented skin from 60 to 90 min at 43 C did not further suppress type I or III procollagen expression (p < 0.05, Fig. 2a), but did lead to increased MMP-1 and -3 induction (p < 0.05, Fig. 2a). Increasing exposure of darkly pigmented skin to 90 min at 43 C resulted in alterations not observed at 60 min. Type I and III procollagen were suppressed approximately 50% (p < 0.05, Fig. 2b), and MMP-1 and -3 were induced by 500- and 45-fold,
http://dx.doi.org/10.1016/j.jdermsci.2016.03.010 0923-1811/ ã 2016 Published by Elsevier Ireland Ltd on behalf of Japanese Society for Investigative Dermatology.
Please cite this article in press as: N. Elbuluk, et al., Infrared irradiation differentially alters collagen metabolism in lightly and darkly pigmented human skin in vivo, J Dermatol Sci (2016), http://dx.doi.org/10.1016/j.jdermsci.2016.03.010
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Letter to the Editor / Journal of Dermatological Science xxx (2015) xxx–xxx
Fig. 1. Suppression of procollagens and MMPs in lightly pigmented human skin following exposure to unfiltered infrared irradiation mimicking artificial sources. (a) Buttock skin of healthy Caucasian subjects was exposed to a single dose of unfiltered IR-A irradiation for 60 min at 41 C. Skin samples were obtained 24 h later, and real-time quantitative polymerase chain reaction was performed to determine gene expression of type I and type III procollagen (n = 6). Data are shown as mean fold change, compared with non-irradiated buttock skin. Error bars indicate SEM. *p <0.05. (b) Suppression of procollagens in lightly pigmented human skin following increased intensity of exposure to unfiltered infrared irradiation mimicking artificial sources. Buttock skin of healthy Caucasian subjects (n = 16) was exposed to a single dose of unfiltered IR-A irradiation for 60 min at an increased temperature of 43 C. Skin samples were obtained 24 h later, and real-time quantitative polymerase chain reaction was performed to determine gene expression of type I and type III procollagen. Data are shown as mean fold change, compared with non-irradiated buttock skin. Error bars indicate SEM. *p< 0.05. (c) Suppression of MMPs in lightly pigmented human skin following increased intensity of exposure to unfiltered infrared irradiation mimicking artificial sources. Same methods use in part B were used to determine gene expression of and matrix metalloproteinases (MMP)-1 and -3.
respectively (p < 0.05, Fig. 2B). No statistically significant difference was found in procollagen or MMP expression between lightly and darkly pigmented skin. The above data indicate that limited exposure (60 min) to full spectrum IR-A irradiation that raises skin surface temperature to 43 C can promote and mimic some effects of UV exposure, including inhibition of collagen production and stimulation of MMPs. Interestingly, melanin appears to provide some protection against the effects of IR irradiation, since longer exposure time was required to elicit changes in darkly pigmented skin. This study
supports data from prior studies showing that infrared irradiation can affect collagen production, however to our knowledge, this study is the first to rigorously examine the protective role of melanin against IR irradiation [5,6,8]. These data support the concept that UV irradiation is the primary cause of photoaging-related changes in the dermal ECM. However, the data do not rule out the possibility that exposure to solar-simulated IR irradiation of higher temperature or longer duration may elicit changes in procollagen or MMP expression.
Please cite this article in press as: N. Elbuluk, et al., Infrared irradiation differentially alters collagen metabolism in lightly and darkly pigmented human skin in vivo, J Dermatol Sci (2016), http://dx.doi.org/10.1016/j.jdermsci.2016.03.010
G Model DESC 2975 No. of Pages 3
Letter to the Editor / Journal of Dermatological Science xxx (2015) xxx–xxx
3
Fig. 2. Suppression of procollagens and induction of MMPs in lightly pigmented and darkly pigmented human skin following increased intensity and duration of exposure to unfiltered infrared irradiation mimicking artificial sources. Buttock skin of (a) healthy Caucasian subjects (n = 12) and (b) African American subjects (n = 6) was exposed to a single dose of unfiltered IR-A irradiation for a longer duration (90 min) at an increased temperature of 43 C. Skin samples were obtained 24 h later, and real-time quantitative polymerase chain reaction was performed to determine gene expression of type I and type III procollagen, and matrix metalloproteinases (MMP)-1 and 3. Data are shown as mean fold change, compared with non-irradiated buttock skin. Error bars indicate SEM. *p < 0.05. When comparing the results between African American and Caucasian subjects, there was no statistical difference in the degree of suppression of type I and III procollagen or the induction of MMP-1 and MMP-3.
Conflict of interest The authors have no conflict of interest to declare. Acknowledgements The authors thank Suzan Rehbine, LPN, for assistance in procuring tissue samples; Laura VanGoor, BFA, for graphic illustrations; and Ted Hamilton, MS, for statistical analysis. The project was supported, in part, by Grant Number UL1RR024986 from the National Center for Research Resources. References [1] G.J. Fisher, Z.Q. Wang, S.C. Datta, J. Varani, S. Kang, J.J. Voorhees, Pathophysiology of premature skin aging induced by ultraviolet light, N. Engl. J. Med. 337 (1997) 1419–1428. [2] L.T. Smith, K.A. Holbrook, J.A. Madri, Collagen types I, III, and V in human embryonic and fetal skin, Am. J. Anat. 175 (1986) 507–521. [3] J.T.C. Krutmann, I. Kochevar, Fundamentals of cutaneous photobiology and photoimmunology, in: K.G.L. Wolfe, S. Katz, B. Gilchrest, A. Paller, D. Leffell (Eds.), Fitzpatrick’s Dermatology in General Medicine, McGraw Hill, New York, 2008. [4] K.D. Desmet, D.A. Paz, J.J. Corry, J.T. Eells, M.T. Wong-Riley, M.M. Henry, et al., Clinical and experimental applications of NIR-LED photobiomodulation, Photomed. Laser Surg. 24 (2006) 121–128. [5] P.S.S. Schroeder, A. Monta, Premature skin aging by infrared radition, tobacco smoke, and ozone, in: B.K.J. Gilchrest (Ed.), Skin Aging, Heidelberg, Springer, 2006, pp. 45–53. [6] S.M. Schieke, P. Schroeder, J. Krutmann, Cutaneous effects of infrared radiation: from clinical observations to molecular response mechanisms, Photodermatol. Photoimmunol. Photomed. 19 (2003) 228–234. [7] J.H. Chung, J.Y. Seo, H.R. Choi, M.K. Lee, C.S. Youn, G. Rhie, et al., Modulation of skin collagen metabolism in aged and photoaged human skin in vivo, J. Invest. Dermatol. 117 (2001) 1218–1224.
[8] S. Schieke, H. Stege, V. Kurten, S. Grether-Beck, H. Sies, J. Krutmann, Infrared-A radiation-induced matrix metalloproteinase 1 expression is mediated through extracellular signal-regulated kinase 1/2 activation in human dermal fibroblasts, J. Invest. Dermatol. 119 (2002) 1323–1329.
Nada Elbuluk* Ronald O. Perelman Department of Dermatology, NYU Langone Medical Center, New York, NY, USA Frank Wang, Bao Anh Patrick Tran Craig Hammerberg John J. Voorhees Department of Dermatology, University of Michigan School of Medicine, Ann Arbor, MI, USA, USA Sewon Kang Department of Dermatology, Johns Hopkins Hospital, Baltimore, MD, USA, USA Gary J. Fisher Department of Dermatology, University of Michigan School of Medicine, Ann Arbor, MI, USA, USA * Corresponding author. E-mail address: [email protected] (N. Elbuluk). Received 11 September 2015 Received in revised form 14 March 2016 Accepted 17 March 2016
Please cite this article in press as: N. Elbuluk, et al., Infrared irradiation differentially alters collagen metabolism in lightly and darkly pigmented human skin in vivo, J Dermatol Sci (2016), http://dx.doi.org/10.1016/j.jdermsci.2016.03.010