Article pubs.acs.org/est
Sunscreens as a Source of Hydrogen Peroxide Production in Coastal Waters David Sánchez-Quiles*,† and Antonio Tovar-Sánchez†,‡ †
Department of Global Change Research, Mediterranean Institute for Advanced Studies (IMEDEA), Spanish National Research Council (CSIC)−University of the Balearic Islands (UIB), Miguel Marqués 21, 07190 Esporles, Balearic Islands, Spain ‡ Department of Ecology and Coastal Management, Andalusian Institute for Marine Science (ICMAN), Spanish National Research Council (CSIC), Campus Universitario Río San Pedro, 11510 Puerto Real, Cádiz, Spain ABSTRACT: Sunscreens have been shown to give the most effective protection for human skin from ultraviolet (UV) radiation. Chemicals from sunscreens (i.e., UV filters) accumulate in the sea and have toxic effects on marine organisms. In this report, we demonstrate that photoexcitation of inorganic UV filters (i.e., TiO2 and ZnO nanoparticles) under solar radiation produces significant amounts of hydrogen peroxide (H2O2), a strong oxidizing agent that generates high levels of stress on marine phytoplankton. Our results indicate that the inorganic oxide nanoparticle content in 1 g of commercial sunscreen produces rates of H2O2 in seawater of up to 463 nM/h, directly affecting the growth of phytoplankton. Conservative estimates for a Mediterranean beach reveal that tourism activities during a summer day may release on the order of 4 kg of TiO2 nanoparticles to the water and produce an increment in the concentration of H2O2 of 270 nM/day. Our results, together with the data provided by tourism records in the Mediterranean, point to TiO2 nanoparticles as the major oxidizing agent entering coastal waters, with direct ecological consequences on the ecosystem.
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INTRODUCTION
labeled according to the European Union (EU) CLP regulation (classification, labeling, and packaging; EC 1272/2008).16 Because of the physical−chemical properties (i.e., high particle reactivity, very low solubility, and binding to organic compounds), nano-TiO2 tends to become concentrated on the surface microlayer (SML) of the water column.14 In the SML of the seawater column, many processes take place (i.e., atmospheric inputs, solar energy flux, water transpiration, etc.) and where organic and inorganic components are enriched compared to the rest of the water column.17 With more than 202 million international tourist arrivals in 2013, the Mediterranean is the world’s leading destination for both international and domestic tourism.18 According to the World Tourism Organization, the Mediterranean expects to reach 264 million tourists in 2030, representing an average increase of some 3 million visitors a year.19 In fact, this prediction could be even higher because new data from the Spanish Ministry of Industry, Energy, and Tourism indicate that Spain broke the barrier of 60 million international visitors, with 60.6 million arrivals during this year.20 However, despite the increased awareness of the economic and environmental significance of tourism, scientific research on the environmental
Hydrogen peroxide (H2O2) is a common agent with a potential chemical and biological reactivity that can cause oxidative stress on marine organisms.1 Traditionally, the main sources of H2O2 in the marine environment involve the absorption of ultraviolet (UV) radiation from dissolved organic matter, atmospheric inputs via dry and wet deposition, and biological production by algae, with a maximum of the H2O2 concentration around 102 nM in coastal, estuarine, and offshore superficial waters.2 Nanotechnology is one of the fastest growing industries in the world, with multiple social applications.3 The most produced nanoparticles worldwide are titanium dioxide (nano-TiO2). Nano-TiO2 is widely used in many industrial applications, such as self-cleaning surface coatings, lightemitting diodes, solar cells, water treatment, and especially sunscreens and coatings for UV protection.4,5 It is well-known that nano-TiO2 can lead to the formation of reactive oxygen species (ROS) by photocatalytic reactions under UV radiation.6−9 To prevent photoreactivity and the consequent reactive effect on the human skin, nano-TiO2 particles in sunscreens are coated with silica or alumina. Nonetheless, this coating layer is quickly dissolved in aqueous media,10,11 enabling the production of ROS.12,13 It has recently been demonstrated that nano-TiO2 from sunscreens are released in coastal seawater directly from beachgoers and could be accumulating in sediments.14,15 Because of its chemical composition, it has been suggested that sunscreens should be © XXXX American Chemical Society
Received: April 28, 2014 Revised: July 9, 2014 Accepted: July 28, 2014
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risks associated with the use of sunscreen in a coastal area is very scarce. Here, we demonstrate from laboratory and field experiments that nanoparticles from sunscreens produce H2O2 in seawater and that it causes a toxic effect on marine phytoplankton. We studied the in situ concentration and distribution of Ti and H2O2 in the water column of a populated beach of Majorca Island (Spain) during a summer day.
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MATERIALS AND METHODS Chemical Analysis. H2O2 was determined following the methodology previously described by Price et al.21,22 Briefly, a flow injection system with chemiluminescence detection (Felume System Waterville Analytical, Waterville, ME) was used to monitor the oxidation of luminol at pH 10.8 in the presence of H2O2 using cobalt(II) as the catalyst. All samples were filtered through a 0.22 μm polypropylene cartridge filter and analyzed immediately after collection. The concentration of the stock H2O2 solution was determined spectrophotometrically using the molar absorptivity of 38.1 ± 1.4 M−1 cm−1 at 240 nm.23 The chlorophyll a (Chl a) concentration was determinate fluorimetrically following the method described by HolmHansen et al.24 TiO2 was determined according to Sánchez-Quiles et al., where a multisyringe flow injection analysis coupled with a liquid waveguide capillary cell (MSFIA−LWCC) was used for the spectrophotometric determination of TiO2 after prior digestion with potassium peroxodisulfate.25 Metals in commercial sunscreens were previously reported.14 All sampling and analytical operations were performed following trace metal clean techniques.26 All chemical analysis was performed in triplicate. Kinetic Experiment. A total of 1 g of a commercial sunscreen (sunscreen A; see Table 1) was diluted in 1 L of
Figure 1. Map of sampling locations.
During the experiment, the UV radiation was monitored using an UV radiometer (PCE-UV34). Field Sampling. Coastal seawater samples were collected from Palmira beach (Peguera, Majorca Island; Figure 1) during August 7−8, 2013. Palmira beach is a semi-enclosed crenulated beach (300 m) situated between a headland and a groin. Depths of up to 5 m are reached in the offshore side of an embayment, which has an approximate volume of 1.2 × 105 m3 and water residence time of 3 days.14,27 Samples of the water column were collected in triplicate at various times during 24 h. Water (5 cm depth) was collected using a pneumatic boat that was anchored at 1.5 m depth in the bathing area of the beach. Water samples at 1 m depth and at the bottom (i.e., 1.5 m depth) were collected manually by a scuba diver. The surface microlayer was collected using the glass plate (GP) sampler. This procedure has been found to be one of the most reliable methods for collecting trace metals and consists of a rectangular GP with a handle attached, which is immersed and retrieved vertically through the water surface. The film adhering to the glass surface is wiped off into a sample bottle using Teflon wiper blades.17 Before sampling, glasses were acid-cleaned overnight and then rinsed thoroughly with ultrapure water (Milli-Q water). To check for procedural contamination, we collected SML blanks on board the pneumatic boat by rinsing the GP with ultrapure water and collecting 500 mL using the GP system. We estimated a surface microlayer thickness of 26 μm, calculated using the formula by Wurl28 (we used a GP with 975 cm2 surface area, and about 100 dips were required to collect 500 mL of water). UV radiation was directly measured in the field, and H2O2 concentrations were analyzed after collection in a field laboratory installed on the beach.
Table 1. Mean Concentration (±SD) of Metal Oxides within Commercial Sunscreens (mg g−1 of Sunscreen)
a
sunscreen
aspect
SPF
TiO2
ZnO
A B C
solar milk cream solar spray
50 30 30
77.6 ± 3.0 nd nd
nda 90.5 ± 0.1 nd
nd = not detected.
filtered seawater from a pristine coastal area and stirred in the lab for 55 h under UV radiation (Osram Germicidal Puritec HNS 30WG13; radiated wavelength of 200−280 nm). Aliquots of 5 mL were sampled at different times up to 55 h and filtered through a 0.22 μm polypropylene cartridge filter prior to H2O2 analysis. Incubation Experiment. Teflon bags filled with 2 L of untreated seawater collected in a pristine area of Ses Salines Cape (Majorca Island; Figure 1) were used for phytoplankton incubations. Triplicate treatments were inoculated with 125 mg L−1 [that is the half maximal effective concentration (EC50) measured for acute toxicity in marine diatoms]14 of three commercial sunscreens with different composition and protection factors (Table 1) and incubated for 24 h under natural solar radiation in a 1000 L open tank with temperature control to guarantee the environmental seawater temperature conditions. During the experiment, H 2 O 2 and Chl a concentrations were analyzed every 6 h in all treatments.
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RESULTS AND DISCUSSION Production of H2O2 from Commercial Sunscreen. Kinetic experiments demonstrate that, under controlled UV ambient radiation, a commercial sunscreen (i.e., 1 g L−1 of sunscreen A; Table 1) may produce up to 10 202 ± 606 nM of H2O2 in seawater in 22 h, which is equivalent to 447 times the initial levels in coastal water (22.8 ± 2.6 nM) (Figure 2). The net hydrogen peroxide production rate (NHPPR), calculated as the difference between the highest (after 22 h) and initial H2O2 concentrations during the experiment, was 462.7 nM h−1 for the sunscreen and 10.1 nM h−1 for the control, leading to a B
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797.7 and 424.8 nmol/mg of nanoparticles from sunscreen containing TiO2 and ZnO in its formulation, respectively) (panels B and C of Figure 3). Even though sunscreen without metal oxides in its formulation (i.e., sunscreen C in Table 1) can generate H2O2, this showed up to 59 and 31 times lower ROS production than those commercial sunscreens with nanoTiO2 and nano-ZnO, respectively (Figure 3D). Although these two metal oxides are likely to be mainly responsible for H2O2 production,12,13 as shown in panels B and C of Figure 3, we are aware that other elements included in the formulation of sunscreen (i.e., benzophenone-3, octocrylene, octilmethoxycinnamate, p-aminobenzoic acid, and 2-phenylbenzimidazole-5sulfonic acid) may also contribute to ROS production29−31 (Figure 3D). Our results show that a concentration of H2O2 above 1.7 μM (measured during the maximum solar radiation) causes toxicity in the phytoplankton population, as reflected by a dramatic decrease of Chl a in the incubation treatments (i.e., from 0.36 ± 0.07 mg m−3 at 9:00 h to 0.07 ± 0.02 mg m−3 at 15:00 h; Figure 3D). H2O2 Coastal Concentration. We investigated the H2O2 and Ti4+ concentrations and distributions in the water column at Palmira beach (Majorca Island; Figure 1) during a 24 h diurnal cycle (Figure 4). The highest concentrations of H2O2 and Ti4+ were measured at noon in the SML (278.0 ± 11.6 and 833.7 ± 50.1 nM of H2O2 and Ti4+, respectively) and in the bottom water (1.5 m; 264.7 ± 13.3 and 689.3 ± 104.3 nM of H2O2 and Ti4+, respectively; Figure 5). As previously stated,14,15 TiO2 is mostly accumulated in the SML and in the sediments, and consequently, the production of H2O2 is the highest in these compartments, even in the bottom water (1.5 m depth), where UV radiation is much lower than in the SML (2.8 and 0.6 mW cm−2, respectively) but enough to produce the photocatalytic reaction.
Figure 2. Kinetic experiment of H2O2 production in seawater: (●) control and (○) treatment of 1 g L−1 of sunscreen A (see Table 1) (n = 3).
kinetic production of H2O2 in samples contained in sunscreens of 46 times faster than controls. Although the concentration of sunscreen used in the experiment is probably higher than its usual concentration found in the marine environment, our results clearly demonstrate that sunscreens lead to H2O2 production in seawater. As previously suggested,11 inorganic nanoparticle oxides (i.e., nano-TiO 2 ) included in the formulation of commercial sunscreens are photocalatytic under UV radiation, even though these nanoparticles are coated to avoid photoreactivity on human skin. A field sunscreen incubation experiment carried out under solar radiation in a diurnal cycle showed a maximum production of H2O2 during the highest UV radiation (up to
Figure 3. Incubation experiment: (A) control without sunscreen, (B) 0.125 g L−1 of sunscreen A, (C) 0.125 g L−1 of sunscreen B, and (D) 0.125 g L−1 of sunscreen C. The solid line represents Chl a (n = 3, except control at 15:00 h, where n = 1), and the dashed line represents UV radiation. Bars represent the H2O2 concentration (n = 3). C
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Figure 5. Field sampling at Palmira beach. Solid and dashed lines represent the UV radiation at 23:30 and 12:00, respectively. Black and white circles represent the Ti concentration at 23:30 and 12:00, respectively. Black and white bars represent the H2O2 concentration at 23:30 and 12:00, respectively. The dark sample of the bottom was collected at 8:00.
that in the subsurface water (from 5 cm to 1 m), were 2.0 and 1.9 for H2O2 and 1.6 and 1.3 for Ti4+, respectively. According to Clark et al., concentrations of H2O2 between 200 and 300 nM do not cause cell lysis but do contribute to oxidative stress.2 The concentrations measured in this study are higher than data reported in oligotrophic surface waters of the Mediterranean Sea (91 ± 21 nM)22 and higher than the maximum concentration reported by Clark et al. in bathing waters of the southern California coast (182 ± 14 nM).35 Therefore, tourist beaches in the Mediterranean, such as Palmira beach, may have significant concentrations of H2O2, with a direct effect on the marine coastal phytoplankton. The NHPPR estimated after 4 h of solar irradiation (from 8:00 to 12:00) was 50.5, 28.9, 13.9, and 51.8 nM h−1 in the SML, 5 cm, 1 m, and bottom, respectively. SML and bottom, where TiO2 is accumulated, presented the highest NHPPR. Although the same order of magnitude, these ratios are higher than NHPPR previously reported from marine bathing waters of California (15.6 ± 3.5 nM h−1)35 and consistent with rates from estuarine and coastal waters with a high content of dissolved organic matter from rivers (from 17 to 56 nM h−1).2 Because riverine inputs are non-existent in the Balearic Islands and organic matter concentrations in these coastal waters are very low,36 the H2O2 production from organic matter is expected to be low. Estimation of H2O2 Production from Sunscreen in a Touristic Beach. A simple calculation seems to validate the magnitude and importance of H2O2 production from sunscreen in coastal waters. Provided that the reported content of nanoTiO2 in commercial sunscreens is 46 mg/g of cream15 and assuming that the typical application by an adult is approximately 36 g/application (which is half the recommended usage per adult)37 and that 25% of sunscreen applied could washed off the skin into the water,38 we estimate a summer daily release of nano-TiO2 of approximately 4 kg at Palmira beach (where the number of beachgoers per summer day is of approximately 10 00014). Combining the H2O2 production from sunscreen obtained from our experiments (i.e., 797.7 nmol/mg of TiO2 nanoparticles) and the volume of water of the bathing zone in Palmira beach (i.e., 1.2 × 107 L, assuming an area of 1.6 × 104 m2 and 1.5 m depth), we estimate an increase of NHPPR of H2O2 of 270 nM day−1. A recent Spanish Ministry report indicates that tourism in Spain is increasing rapidly, with a new tourism record in 2013
Figure 4. (A) UV radiation, (B) H2O2 concentration, and (C) Ti4+ concentration in the water column of Palmira beach: (▲) SML, (△) 5 cm, (●) 1 m, and (○) bottom.
We are aware that dissolved Fe(II)/Fe(III), occurring naturally in the seawater, can generate ROS via a photo-Fenton reaction (eqs 1 and 2)32 Fe(II) + H 2O2 → Fe(III) + OH− + OH*
(1)
Fe(III) + H 2O + hν → Fe(II) + H+ + OH*
(2)
However, the Fenton reaction achieves the optimal yields at micromolar concentrations of Fe.33 Because dissolved Fe concentrations in seawater of Majorca are lower than 15 nM,34 the contribution of the Fenton reaction to the ROS production in these waters is unlikely. Enrichment factors (EF) of H2O2 and Ti4+ in the SML and bottom, calculated as the ratio between the concentration in the SML or bottom over D
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containing titanium dioxide (an EPR study). J. Photochem. Photobiol., B 2005, 79, 121−134. (13) Lewicka, Z. A.; Yu, W. W.; Oliva, B. L.; Contreras, E. Q.; Colvin, V. L. Photochemical behavior of nanoscale TiO2 and ZnO sunscreen ingredients. J. Photochem. Photobiol. Chem. 2013, 263, 24−33. (14) Tovar-Sánchez, A.; Sánchez-Quiles, D.; Basterretxea, G.; Benedé, J. L.; Chisvert, A.; Salvador, A.; Moreno-Garrido, I.; Blasco, J. Sunscreen products as emerging pollutants to coastal waters. PLoS One 2013, 8, No. e65451. (15) Botta, C.; Labille, J.; Auffan, M.; Borschneck, D.; Miche, H.; Cabié, M.; Masion, A.; Rose, J.; Bottero, J.-Y. TiO2-based nanoparticles released in water from commercialized sunscreens in a life-cycle perspective: Structures and quantities. Environ. Pollut. 2011, 159, 1543−1550. (16) Sobek, A.; Bejgarn, S.; Rudén, C.; Molander, L.; Breitholtz, M. In the shadow of the Cosmetic DirectiveInconsistencies in EU environmental hazard classification requirements for UV-filters. Sci. Total Environ. 2013, 461−462, 706−711. (17) Stortini, A. M.; Cincinelli, A.; Degli Innocenti, N.; TovarSánchez, A.; Knulst, J. Surface microlayer. In Comprehensive Sampling and Sample Preparation; Pawliszyn, J., Ed.; Academic Press: Waltham, MA, 2012; Chapter 1.12, pp 223−246. (18) World Tourism Organization (UNWTO). UNWTO World Tourism Barometer; UNWTO: Madrid, Spain, 2014; http://mkt. unwto.org/en/barometer. (19) World Tourism Organization (UNWTO). Tourism Towards 2030/Global Overview; UNWTO: Madrid, Spain, 2011; http://www.eunwto.org/content/w45127/?p= 189899a5998f428f99f66ca0e17d2218. (20) Spanish Ministry of Industry, Energy, and Tourism. Frontur; Spanish Ministry of Industry, Energy, and Tourism: Madrid, Spain, 2014; http://www.iet.tourspain.es/es-es/estadisticas/frontur/paginas/ default.aspx. (21) Price, D.; Worsfold, P. J.; Fauzi, R.; Mantoura, C. Determination of hydrogen peroxide in sea water by flow-injection analysis with chemiluminescence detection. Anal. Chim. Acta 1994, 298, 121−128. (22) Price, D.; Mantoura, R. F. C.; Worsfold, P. J. Shipboard determination of hydrogen peroxide in the western Mediterranean sea using flow injection with chemiluminescence detection. Anal. Chim. Acta 1998, 371, 205−215. (23) Miller, W. L.; Kester, D. R. Hydrogen peroxide measurement in seawater by (p-hydroxyphenyl)acetic acid dimerization. Anal. Chem. 1988, 60, 2711−2715. (24) Holm-Hansen, O.; Lorenzen, C. J.; Holmes, R. W.; Strickland, J. D. H. Fluorometric determination of chlorophyll. ICES J. Mar. Sci. 1965, 30, 3−15. (25) Sánchez-Quiles, D.; Tovar-Sánchez, A.; Horstkotte, B. Titanium determination by multisyringe flow injection analysis system and a liquid waveguide capillary cell in solid and liquid environmental samples. Mar. Pollut. Bull. 2013, 76, 89−94. (26) Tovar-Sánchez, A. Sampling approaches for trace element determination in seawater. In Comprehensive Sampling and Sample Preparation; Pawliszyn, J. M., Bayona, J. M., Eds.; Academic Press: Waltham, MA, 2012; Vol. 1, Chapter 1.17, pp 317−334. (27) Basterretxea, G.; Garcs, E.; Jordi, A.; Angls, S.; Mas, M. Modulation of nearshore harmful algal blooms by in situ growth rate and water renewal. Mar. Ecol.: Prog. Ser. 2007, 352, 53−65. (28) Wurl, O. Practical Guidelines for the Analysis of Seawater; CRC Press: Boca Raton, FL, 2009. (29) Hanson, K. M.; Gratton, E.; Bardeen, C. J. Sunscreen enhancement of UV-induced reactive oxygen species in the skin. Free Radical Biol. Med. 2006, 41, 1205−1212. (30) Allen, J. M.; Gossett, C. J.; Allen, S. K. Photochemical formation of singlet molecular oxygen in illuminated aqueous solutions of several commercially available sunscreen active ingredients. Chem. Res. Toxicol. 1996, 9, 605−609. (31) Inbaraj, J. J.; Bilski, P.; Chignell, C. F. Photophysical and photochemical studies of 2-phenylbenzimidazole and UVB sunscreen
of more than 60.6 million foreign tourists (5.6% more than 2012), and the Spanish Mediterranean coast represents more than 50% of the visits (i.e., Catalonia, Balearic Islands, and Valencia, with 15.5, 11.1, and 5.9 million of foreign visitors, respectively).20 Our results suggest that the increased tourist activities will have important ecological consequences in the coastal areas as a consequence of the increased input of sunscreen products, particularly in Mediterranean beaches, where tourism is more intense and where the water resident time is longer.
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AUTHOR INFORMATION
Corresponding Author
*Telephone: +34-971611726. Fax: +34-971611761. E-mail: [email protected]. Notes
The authors declare no competing financial interest.
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ACKNOWLEDGMENTS The authors thank A. Massanet, P. Vidal, and M. Makhani, from the Ses Salines lighthouse working team, and Ajuntament de Calvià for technical assistance and field support. David SánchezQuiles was supported by the JAE-predoc program of the Spanish National Research Council (CSIC).
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REFERENCES
(1) Lesser, M. P. Oxidative stress in marine environments: Biochemistry and physiological ecology. Annu. Rev. Physiol. 2006, 68, 253−278. (2) Clark, C. D.; De Bruyn, W. J.; Jakubowski, S. D.; Grant, S. B. Hydrogen peroxide production in marine bathing waters: Implications for fecal indicator bacteria mortality. Mar. Pollut. Bull. 2008, 56, 397− 401. (3) Forster, S. P.; Olveira, S.; Seeger, S. Nanotechnology in the market: Promises and realities. Int. J. Nanotechnol. 2011, 8, 592−613. (4) United States Environmental Protection Agency (U.S. EPA). Nanomaterial Case Studies: Nanoscale Titanium Dioxide (External Review Draft); U.S. EPA: Washington, D.C., 2009; EPA/600/R-09/ 057, http://cfpub.epa.gov/ncea/cfm/recordisplay.cfm?deid=210206. (5) Piccinno, F.; Gottschalk, F.; Seeger, S.; Nowack, B. Industrial production quantities and uses of ten engineered nanomaterials in Europe and the world. J. Nanopart. Res. 2012, 14, 1−11. (6) Tanaka, K.; Capule, M. F. V.; Hisanaga, T. Effect of crystallinity of TiO2 on its photocatalytic action. Chem. Phys. Lett. 1991, 187, 73− 76. (7) Carp, O.; Huisman, C. L.; Reller, A. Photoinduced reactivity of titanium dioxide. Prog. Solid State Chem. 2004, 32, 33−177. (8) Chen, H.; Nanayakkara, C. E.; Grassian, V. H. Titanium dioxide photocatalysis in atmospheric chemistry. Chem. Rev. 2012, 112, 5919− 5948. (9) Chen, C.; Wang, J. Nanoscale titanium dioxide: Environmental health and ecotoxicological effects. In Encyclopedia of Environmental Health; Nriagu, J. O., Ed.; Elsevier: Amsterdam, Netherlands, 2011; pp 12−21. (10) Auffan, M.; Pedeutour, M.; Rose, J.; Masion, A.; Ziarelli, F.; Borschneck, D.; Chaneac, C.; Botta, C.; Chaurand, P.; Labille, J.; Bottero, J.-Y. Structural degradation at the surface of a TiO2-based nanomaterial used in cosmetics. Environ. Sci. Technol. 2010, 44, 2689− 2694. (11) Labille, J.; Feng, J.; Botta, C.; Borschneck, D.; Sammut, M.; Cabie, M.; Auffan, M.; Rose, J.; Bottero, J.-Y. Aging of TiO2 nanocomposites used in sunscreen. Dispersion and fate of the degradation products in aqueous environment. Environ. Pollut. 2010, 158, 3482−3489. (12) Brezová, V.; Gabčová, S.; Dvoranová, D.; Staško, A. Reactive oxygen species produced upon photoexcitation of sunscreens E
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2-phenylbenzimidazole-5-sulfonic acid. Photochem. Photobiol. 2002, 75, 107−116. (32) Fenton, H. J. H. Oxidation of tartaric acid in presence of iron. J. Chem. Soc. Trans. 1894, 65, 899−910. (33) Southworth, B. A.; Voelker, B. M. Hydroxyl radical production via the photo-Fenton reaction in the presence of fulvic acid. Environ. Sci. Technol. 2003, 37, 1130−1136. (34) Rodellas, V.; Garcia-Orellana, J.; Tovar-Sán chez, A.; Basterretxea, G.; López-Garcia, J. M.; Sánchez-Quiles, D.; GarciaSolsona, E.; Masqué, P. Submarine groundwater discharge as a source of nutrients and trace metals in a Mediterranean bay (Palma Beach, Balearic Islands). Mar. Chem. 2014, 160, 56−66. (35) Clark, C. D.; De Bruyn, W. J.; Hirsch, C. M.; Aiona, P. Diel cycles of hydrogen peroxide in marine bathing waters in southern California, USA: In situ surf zone measurements. Mar. Pollut. Bull. 2010, 60, 2284−2288. (36) Rochelle-Newall, E. J.; Winter, C.; Barrón, C.; Borges, A. V.; Duarte, C. M.; Elliott, M.; Frankignoulle, M.; Gazeau, F.; Middelburg, J. J.; Pizay, M.-D.; Gattuso, J.-P. Artificial neural network analysis of factors controlling ecosystem metabolism in coastal systems. Ecol. Appl. 2007, 17, S185−S196. (37) Diffey, B. Sunscreen isn’t enough. J. Photochem. Photobiol., B 2001, 64, 105−108. (38) Danovaro, R.; Bongiorni, L.; Corinaldesi, C.; Giovannelli, D.; Damiani, E.; Astolfi, P.; Greci, L.; Pusceddu, A. Sunscreens cause coral bleaching by promoting viral infections. Environ. Health Perspect. 2008, 116, 441−447.
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Sunscreens as a Source of Hydrogen Peroxide Production in Coastal Waters David Sánchez-Quiles*,† and Antonio Tovar-Sánchez†,‡ †
Department of Global Change Research, Mediterranean Institute for Advanced Studies (IMEDEA), Spanish National Research Council (CSIC)−University of the Balearic Islands (UIB), Miguel Marqués 21, 07190 Esporles, Balearic Islands, Spain ‡ Department of Ecology and Coastal Management, Andalusian Institute for Marine Science (ICMAN), Spanish National Research Council (CSIC), Campus Universitario Río San Pedro, 11510 Puerto Real, Cádiz, Spain ABSTRACT: Sunscreens have been shown to give the most effective protection for human skin from ultraviolet (UV) radiation. Chemicals from sunscreens (i.e., UV filters) accumulate in the sea and have toxic effects on marine organisms. In this report, we demonstrate that photoexcitation of inorganic UV filters (i.e., TiO2 and ZnO nanoparticles) under solar radiation produces significant amounts of hydrogen peroxide (H2O2), a strong oxidizing agent that generates high levels of stress on marine phytoplankton. Our results indicate that the inorganic oxide nanoparticle content in 1 g of commercial sunscreen produces rates of H2O2 in seawater of up to 463 nM/h, directly affecting the growth of phytoplankton. Conservative estimates for a Mediterranean beach reveal that tourism activities during a summer day may release on the order of 4 kg of TiO2 nanoparticles to the water and produce an increment in the concentration of H2O2 of 270 nM/day. Our results, together with the data provided by tourism records in the Mediterranean, point to TiO2 nanoparticles as the major oxidizing agent entering coastal waters, with direct ecological consequences on the ecosystem.
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INTRODUCTION
labeled according to the European Union (EU) CLP regulation (classification, labeling, and packaging; EC 1272/2008).16 Because of the physical−chemical properties (i.e., high particle reactivity, very low solubility, and binding to organic compounds), nano-TiO2 tends to become concentrated on the surface microlayer (SML) of the water column.14 In the SML of the seawater column, many processes take place (i.e., atmospheric inputs, solar energy flux, water transpiration, etc.) and where organic and inorganic components are enriched compared to the rest of the water column.17 With more than 202 million international tourist arrivals in 2013, the Mediterranean is the world’s leading destination for both international and domestic tourism.18 According to the World Tourism Organization, the Mediterranean expects to reach 264 million tourists in 2030, representing an average increase of some 3 million visitors a year.19 In fact, this prediction could be even higher because new data from the Spanish Ministry of Industry, Energy, and Tourism indicate that Spain broke the barrier of 60 million international visitors, with 60.6 million arrivals during this year.20 However, despite the increased awareness of the economic and environmental significance of tourism, scientific research on the environmental
Hydrogen peroxide (H2O2) is a common agent with a potential chemical and biological reactivity that can cause oxidative stress on marine organisms.1 Traditionally, the main sources of H2O2 in the marine environment involve the absorption of ultraviolet (UV) radiation from dissolved organic matter, atmospheric inputs via dry and wet deposition, and biological production by algae, with a maximum of the H2O2 concentration around 102 nM in coastal, estuarine, and offshore superficial waters.2 Nanotechnology is one of the fastest growing industries in the world, with multiple social applications.3 The most produced nanoparticles worldwide are titanium dioxide (nano-TiO2). Nano-TiO2 is widely used in many industrial applications, such as self-cleaning surface coatings, lightemitting diodes, solar cells, water treatment, and especially sunscreens and coatings for UV protection.4,5 It is well-known that nano-TiO2 can lead to the formation of reactive oxygen species (ROS) by photocatalytic reactions under UV radiation.6−9 To prevent photoreactivity and the consequent reactive effect on the human skin, nano-TiO2 particles in sunscreens are coated with silica or alumina. Nonetheless, this coating layer is quickly dissolved in aqueous media,10,11 enabling the production of ROS.12,13 It has recently been demonstrated that nano-TiO2 from sunscreens are released in coastal seawater directly from beachgoers and could be accumulating in sediments.14,15 Because of its chemical composition, it has been suggested that sunscreens should be © XXXX American Chemical Society
Received: April 28, 2014 Revised: July 9, 2014 Accepted: July 28, 2014
A
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risks associated with the use of sunscreen in a coastal area is very scarce. Here, we demonstrate from laboratory and field experiments that nanoparticles from sunscreens produce H2O2 in seawater and that it causes a toxic effect on marine phytoplankton. We studied the in situ concentration and distribution of Ti and H2O2 in the water column of a populated beach of Majorca Island (Spain) during a summer day.
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MATERIALS AND METHODS Chemical Analysis. H2O2 was determined following the methodology previously described by Price et al.21,22 Briefly, a flow injection system with chemiluminescence detection (Felume System Waterville Analytical, Waterville, ME) was used to monitor the oxidation of luminol at pH 10.8 in the presence of H2O2 using cobalt(II) as the catalyst. All samples were filtered through a 0.22 μm polypropylene cartridge filter and analyzed immediately after collection. The concentration of the stock H2O2 solution was determined spectrophotometrically using the molar absorptivity of 38.1 ± 1.4 M−1 cm−1 at 240 nm.23 The chlorophyll a (Chl a) concentration was determinate fluorimetrically following the method described by HolmHansen et al.24 TiO2 was determined according to Sánchez-Quiles et al., where a multisyringe flow injection analysis coupled with a liquid waveguide capillary cell (MSFIA−LWCC) was used for the spectrophotometric determination of TiO2 after prior digestion with potassium peroxodisulfate.25 Metals in commercial sunscreens were previously reported.14 All sampling and analytical operations were performed following trace metal clean techniques.26 All chemical analysis was performed in triplicate. Kinetic Experiment. A total of 1 g of a commercial sunscreen (sunscreen A; see Table 1) was diluted in 1 L of
Figure 1. Map of sampling locations.
During the experiment, the UV radiation was monitored using an UV radiometer (PCE-UV34). Field Sampling. Coastal seawater samples were collected from Palmira beach (Peguera, Majorca Island; Figure 1) during August 7−8, 2013. Palmira beach is a semi-enclosed crenulated beach (300 m) situated between a headland and a groin. Depths of up to 5 m are reached in the offshore side of an embayment, which has an approximate volume of 1.2 × 105 m3 and water residence time of 3 days.14,27 Samples of the water column were collected in triplicate at various times during 24 h. Water (5 cm depth) was collected using a pneumatic boat that was anchored at 1.5 m depth in the bathing area of the beach. Water samples at 1 m depth and at the bottom (i.e., 1.5 m depth) were collected manually by a scuba diver. The surface microlayer was collected using the glass plate (GP) sampler. This procedure has been found to be one of the most reliable methods for collecting trace metals and consists of a rectangular GP with a handle attached, which is immersed and retrieved vertically through the water surface. The film adhering to the glass surface is wiped off into a sample bottle using Teflon wiper blades.17 Before sampling, glasses were acid-cleaned overnight and then rinsed thoroughly with ultrapure water (Milli-Q water). To check for procedural contamination, we collected SML blanks on board the pneumatic boat by rinsing the GP with ultrapure water and collecting 500 mL using the GP system. We estimated a surface microlayer thickness of 26 μm, calculated using the formula by Wurl28 (we used a GP with 975 cm2 surface area, and about 100 dips were required to collect 500 mL of water). UV radiation was directly measured in the field, and H2O2 concentrations were analyzed after collection in a field laboratory installed on the beach.
Table 1. Mean Concentration (±SD) of Metal Oxides within Commercial Sunscreens (mg g−1 of Sunscreen)
a
sunscreen
aspect
SPF
TiO2
ZnO
A B C
solar milk cream solar spray
50 30 30
77.6 ± 3.0 nd nd
nda 90.5 ± 0.1 nd
nd = not detected.
filtered seawater from a pristine coastal area and stirred in the lab for 55 h under UV radiation (Osram Germicidal Puritec HNS 30WG13; radiated wavelength of 200−280 nm). Aliquots of 5 mL were sampled at different times up to 55 h and filtered through a 0.22 μm polypropylene cartridge filter prior to H2O2 analysis. Incubation Experiment. Teflon bags filled with 2 L of untreated seawater collected in a pristine area of Ses Salines Cape (Majorca Island; Figure 1) were used for phytoplankton incubations. Triplicate treatments were inoculated with 125 mg L−1 [that is the half maximal effective concentration (EC50) measured for acute toxicity in marine diatoms]14 of three commercial sunscreens with different composition and protection factors (Table 1) and incubated for 24 h under natural solar radiation in a 1000 L open tank with temperature control to guarantee the environmental seawater temperature conditions. During the experiment, H 2 O 2 and Chl a concentrations were analyzed every 6 h in all treatments.
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RESULTS AND DISCUSSION Production of H2O2 from Commercial Sunscreen. Kinetic experiments demonstrate that, under controlled UV ambient radiation, a commercial sunscreen (i.e., 1 g L−1 of sunscreen A; Table 1) may produce up to 10 202 ± 606 nM of H2O2 in seawater in 22 h, which is equivalent to 447 times the initial levels in coastal water (22.8 ± 2.6 nM) (Figure 2). The net hydrogen peroxide production rate (NHPPR), calculated as the difference between the highest (after 22 h) and initial H2O2 concentrations during the experiment, was 462.7 nM h−1 for the sunscreen and 10.1 nM h−1 for the control, leading to a B
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797.7 and 424.8 nmol/mg of nanoparticles from sunscreen containing TiO2 and ZnO in its formulation, respectively) (panels B and C of Figure 3). Even though sunscreen without metal oxides in its formulation (i.e., sunscreen C in Table 1) can generate H2O2, this showed up to 59 and 31 times lower ROS production than those commercial sunscreens with nanoTiO2 and nano-ZnO, respectively (Figure 3D). Although these two metal oxides are likely to be mainly responsible for H2O2 production,12,13 as shown in panels B and C of Figure 3, we are aware that other elements included in the formulation of sunscreen (i.e., benzophenone-3, octocrylene, octilmethoxycinnamate, p-aminobenzoic acid, and 2-phenylbenzimidazole-5sulfonic acid) may also contribute to ROS production29−31 (Figure 3D). Our results show that a concentration of H2O2 above 1.7 μM (measured during the maximum solar radiation) causes toxicity in the phytoplankton population, as reflected by a dramatic decrease of Chl a in the incubation treatments (i.e., from 0.36 ± 0.07 mg m−3 at 9:00 h to 0.07 ± 0.02 mg m−3 at 15:00 h; Figure 3D). H2O2 Coastal Concentration. We investigated the H2O2 and Ti4+ concentrations and distributions in the water column at Palmira beach (Majorca Island; Figure 1) during a 24 h diurnal cycle (Figure 4). The highest concentrations of H2O2 and Ti4+ were measured at noon in the SML (278.0 ± 11.6 and 833.7 ± 50.1 nM of H2O2 and Ti4+, respectively) and in the bottom water (1.5 m; 264.7 ± 13.3 and 689.3 ± 104.3 nM of H2O2 and Ti4+, respectively; Figure 5). As previously stated,14,15 TiO2 is mostly accumulated in the SML and in the sediments, and consequently, the production of H2O2 is the highest in these compartments, even in the bottom water (1.5 m depth), where UV radiation is much lower than in the SML (2.8 and 0.6 mW cm−2, respectively) but enough to produce the photocatalytic reaction.
Figure 2. Kinetic experiment of H2O2 production in seawater: (●) control and (○) treatment of 1 g L−1 of sunscreen A (see Table 1) (n = 3).
kinetic production of H2O2 in samples contained in sunscreens of 46 times faster than controls. Although the concentration of sunscreen used in the experiment is probably higher than its usual concentration found in the marine environment, our results clearly demonstrate that sunscreens lead to H2O2 production in seawater. As previously suggested,11 inorganic nanoparticle oxides (i.e., nano-TiO 2 ) included in the formulation of commercial sunscreens are photocalatytic under UV radiation, even though these nanoparticles are coated to avoid photoreactivity on human skin. A field sunscreen incubation experiment carried out under solar radiation in a diurnal cycle showed a maximum production of H2O2 during the highest UV radiation (up to
Figure 3. Incubation experiment: (A) control without sunscreen, (B) 0.125 g L−1 of sunscreen A, (C) 0.125 g L−1 of sunscreen B, and (D) 0.125 g L−1 of sunscreen C. The solid line represents Chl a (n = 3, except control at 15:00 h, where n = 1), and the dashed line represents UV radiation. Bars represent the H2O2 concentration (n = 3). C
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Figure 5. Field sampling at Palmira beach. Solid and dashed lines represent the UV radiation at 23:30 and 12:00, respectively. Black and white circles represent the Ti concentration at 23:30 and 12:00, respectively. Black and white bars represent the H2O2 concentration at 23:30 and 12:00, respectively. The dark sample of the bottom was collected at 8:00.
that in the subsurface water (from 5 cm to 1 m), were 2.0 and 1.9 for H2O2 and 1.6 and 1.3 for Ti4+, respectively. According to Clark et al., concentrations of H2O2 between 200 and 300 nM do not cause cell lysis but do contribute to oxidative stress.2 The concentrations measured in this study are higher than data reported in oligotrophic surface waters of the Mediterranean Sea (91 ± 21 nM)22 and higher than the maximum concentration reported by Clark et al. in bathing waters of the southern California coast (182 ± 14 nM).35 Therefore, tourist beaches in the Mediterranean, such as Palmira beach, may have significant concentrations of H2O2, with a direct effect on the marine coastal phytoplankton. The NHPPR estimated after 4 h of solar irradiation (from 8:00 to 12:00) was 50.5, 28.9, 13.9, and 51.8 nM h−1 in the SML, 5 cm, 1 m, and bottom, respectively. SML and bottom, where TiO2 is accumulated, presented the highest NHPPR. Although the same order of magnitude, these ratios are higher than NHPPR previously reported from marine bathing waters of California (15.6 ± 3.5 nM h−1)35 and consistent with rates from estuarine and coastal waters with a high content of dissolved organic matter from rivers (from 17 to 56 nM h−1).2 Because riverine inputs are non-existent in the Balearic Islands and organic matter concentrations in these coastal waters are very low,36 the H2O2 production from organic matter is expected to be low. Estimation of H2O2 Production from Sunscreen in a Touristic Beach. A simple calculation seems to validate the magnitude and importance of H2O2 production from sunscreen in coastal waters. Provided that the reported content of nanoTiO2 in commercial sunscreens is 46 mg/g of cream15 and assuming that the typical application by an adult is approximately 36 g/application (which is half the recommended usage per adult)37 and that 25% of sunscreen applied could washed off the skin into the water,38 we estimate a summer daily release of nano-TiO2 of approximately 4 kg at Palmira beach (where the number of beachgoers per summer day is of approximately 10 00014). Combining the H2O2 production from sunscreen obtained from our experiments (i.e., 797.7 nmol/mg of TiO2 nanoparticles) and the volume of water of the bathing zone in Palmira beach (i.e., 1.2 × 107 L, assuming an area of 1.6 × 104 m2 and 1.5 m depth), we estimate an increase of NHPPR of H2O2 of 270 nM day−1. A recent Spanish Ministry report indicates that tourism in Spain is increasing rapidly, with a new tourism record in 2013
Figure 4. (A) UV radiation, (B) H2O2 concentration, and (C) Ti4+ concentration in the water column of Palmira beach: (▲) SML, (△) 5 cm, (●) 1 m, and (○) bottom.
We are aware that dissolved Fe(II)/Fe(III), occurring naturally in the seawater, can generate ROS via a photo-Fenton reaction (eqs 1 and 2)32 Fe(II) + H 2O2 → Fe(III) + OH− + OH*
(1)
Fe(III) + H 2O + hν → Fe(II) + H+ + OH*
(2)
However, the Fenton reaction achieves the optimal yields at micromolar concentrations of Fe.33 Because dissolved Fe concentrations in seawater of Majorca are lower than 15 nM,34 the contribution of the Fenton reaction to the ROS production in these waters is unlikely. Enrichment factors (EF) of H2O2 and Ti4+ in the SML and bottom, calculated as the ratio between the concentration in the SML or bottom over D
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containing titanium dioxide (an EPR study). J. Photochem. Photobiol., B 2005, 79, 121−134. (13) Lewicka, Z. A.; Yu, W. W.; Oliva, B. L.; Contreras, E. Q.; Colvin, V. L. Photochemical behavior of nanoscale TiO2 and ZnO sunscreen ingredients. J. Photochem. Photobiol. Chem. 2013, 263, 24−33. (14) Tovar-Sánchez, A.; Sánchez-Quiles, D.; Basterretxea, G.; Benedé, J. L.; Chisvert, A.; Salvador, A.; Moreno-Garrido, I.; Blasco, J. Sunscreen products as emerging pollutants to coastal waters. PLoS One 2013, 8, No. e65451. (15) Botta, C.; Labille, J.; Auffan, M.; Borschneck, D.; Miche, H.; Cabié, M.; Masion, A.; Rose, J.; Bottero, J.-Y. TiO2-based nanoparticles released in water from commercialized sunscreens in a life-cycle perspective: Structures and quantities. Environ. Pollut. 2011, 159, 1543−1550. (16) Sobek, A.; Bejgarn, S.; Rudén, C.; Molander, L.; Breitholtz, M. In the shadow of the Cosmetic DirectiveInconsistencies in EU environmental hazard classification requirements for UV-filters. Sci. Total Environ. 2013, 461−462, 706−711. (17) Stortini, A. M.; Cincinelli, A.; Degli Innocenti, N.; TovarSánchez, A.; Knulst, J. Surface microlayer. In Comprehensive Sampling and Sample Preparation; Pawliszyn, J., Ed.; Academic Press: Waltham, MA, 2012; Chapter 1.12, pp 223−246. (18) World Tourism Organization (UNWTO). UNWTO World Tourism Barometer; UNWTO: Madrid, Spain, 2014; http://mkt. unwto.org/en/barometer. (19) World Tourism Organization (UNWTO). Tourism Towards 2030/Global Overview; UNWTO: Madrid, Spain, 2011; http://www.eunwto.org/content/w45127/?p= 189899a5998f428f99f66ca0e17d2218. (20) Spanish Ministry of Industry, Energy, and Tourism. Frontur; Spanish Ministry of Industry, Energy, and Tourism: Madrid, Spain, 2014; http://www.iet.tourspain.es/es-es/estadisticas/frontur/paginas/ default.aspx. (21) Price, D.; Worsfold, P. J.; Fauzi, R.; Mantoura, C. Determination of hydrogen peroxide in sea water by flow-injection analysis with chemiluminescence detection. Anal. Chim. Acta 1994, 298, 121−128. (22) Price, D.; Mantoura, R. F. C.; Worsfold, P. J. Shipboard determination of hydrogen peroxide in the western Mediterranean sea using flow injection with chemiluminescence detection. Anal. Chim. Acta 1998, 371, 205−215. (23) Miller, W. L.; Kester, D. R. Hydrogen peroxide measurement in seawater by (p-hydroxyphenyl)acetic acid dimerization. Anal. Chem. 1988, 60, 2711−2715. (24) Holm-Hansen, O.; Lorenzen, C. J.; Holmes, R. W.; Strickland, J. D. H. Fluorometric determination of chlorophyll. ICES J. Mar. Sci. 1965, 30, 3−15. (25) Sánchez-Quiles, D.; Tovar-Sánchez, A.; Horstkotte, B. Titanium determination by multisyringe flow injection analysis system and a liquid waveguide capillary cell in solid and liquid environmental samples. Mar. Pollut. Bull. 2013, 76, 89−94. (26) Tovar-Sánchez, A. Sampling approaches for trace element determination in seawater. In Comprehensive Sampling and Sample Preparation; Pawliszyn, J. M., Bayona, J. M., Eds.; Academic Press: Waltham, MA, 2012; Vol. 1, Chapter 1.17, pp 317−334. (27) Basterretxea, G.; Garcs, E.; Jordi, A.; Angls, S.; Mas, M. Modulation of nearshore harmful algal blooms by in situ growth rate and water renewal. Mar. Ecol.: Prog. Ser. 2007, 352, 53−65. (28) Wurl, O. Practical Guidelines for the Analysis of Seawater; CRC Press: Boca Raton, FL, 2009. (29) Hanson, K. M.; Gratton, E.; Bardeen, C. J. Sunscreen enhancement of UV-induced reactive oxygen species in the skin. Free Radical Biol. Med. 2006, 41, 1205−1212. (30) Allen, J. M.; Gossett, C. J.; Allen, S. K. Photochemical formation of singlet molecular oxygen in illuminated aqueous solutions of several commercially available sunscreen active ingredients. Chem. Res. Toxicol. 1996, 9, 605−609. (31) Inbaraj, J. J.; Bilski, P.; Chignell, C. F. Photophysical and photochemical studies of 2-phenylbenzimidazole and UVB sunscreen
of more than 60.6 million foreign tourists (5.6% more than 2012), and the Spanish Mediterranean coast represents more than 50% of the visits (i.e., Catalonia, Balearic Islands, and Valencia, with 15.5, 11.1, and 5.9 million of foreign visitors, respectively).20 Our results suggest that the increased tourist activities will have important ecological consequences in the coastal areas as a consequence of the increased input of sunscreen products, particularly in Mediterranean beaches, where tourism is more intense and where the water resident time is longer.
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AUTHOR INFORMATION
Corresponding Author
*Telephone: +34-971611726. Fax: +34-971611761. E-mail: [email protected]. Notes
The authors declare no competing financial interest.
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ACKNOWLEDGMENTS The authors thank A. Massanet, P. Vidal, and M. Makhani, from the Ses Salines lighthouse working team, and Ajuntament de Calvià for technical assistance and field support. David SánchezQuiles was supported by the JAE-predoc program of the Spanish National Research Council (CSIC).
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