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Isotope Tracers To Study the Environmental Fate and Bioaccumulation of Metal-Containing Engineered Nanoparticles: Techniques and Applications Yongguang Yin,†,‡ Zhiqiang Tan,† Ligang Hu,† Sujuan Yu,† Jingfu Liu,*,† and Guibin Jiang† †

State Key Laboratory of Environmental Chemistry and Ecotoxicology, Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences, Beijing 100085, China ‡ Institute of Environment and Health, Jianghan University, Wuhan 430056, China ABSTRACT: The rapidly growing applicability of metal-containing engineered nanoparticles (MENPs) has made their environmental fate, biouptake, and transformation important research topics. However, considering the relatively low concentration of MENPs and the high concentration of background metals in the environment and in organisms, tracking the fate of MENPs in environment-related scenarios remains a challenge. Intrinsic labeling of MENPs with radioactive or stable isotopes is a useful tool for the highly sensitive and selective detection of MENPs in the environment and organisms, thus enabling tracing of their transformation, uptake, distribution, and clearance. In this review, we focus on radioactive/stable isotope labeling of MENPs for their environmental and biological tracing. We summarize the advantages of intrinsic radioactive/stable isotopes for MENP labeling and discuss the considerations in labeling isotope selection and preparation of labeled MENPs, as well as exposure routes and detection of labeled MENPs. In addition, current practice in the use of radioactive/stable isotope labeling of MENPs to study their environmental fate and bioaccumulation is reviewed. Future perspectives and potential applications are also discussed, including imaging techniques for radioactive- and stable-isotope-labeled MENPs, hyphenated multistable isotope tracers with speciation analysis, and isotope fractionation as a MENP tracer. It is expected that this critical review could provide the necessary background information to further advance the applications of isotope tracers to study the environmental fate and bioaccumulation of MENPs.

CONTENTS 1. Introduction 2. Radioactive Isotopes as Tracers for Metal-Containing Engineered Nanoparticles 2.1. Need for Intrinsic Radioactive Isotopes for Metal-Containing Engineered Nanoparticle Labeling 2.2. Selection of Radioactive Isotopes for MetalContaining Engineered Nanoparticle Labeling 2.3. Preparation of Radioactive-Isotope-Labeled Metal-Containing Engineered Nanoparticles 2.4. Exposure of Radioactive-Isotope-Labeled Metal-Containing Engineered Nanoparticles for Various Evaluation Purposes 2.5. Detection of Radioactive-Isotope-Labeled Metal-Containing Engineered Nanoparticles 2.6. Applications of Radioactive-Isotope-Labeled Metal-Containing Engineered Nanoparticles 2.6.1. Uptake, Intracellular Dissolution, and Translocation of Metal-Containing Engineered Nanoparticles Revealed by Use of in Vitro Models

2.6.2. Uptake and Accumulation of MetalContaining Engineered Nanoparticles from Different Exposure Routes by Use of in Vivo Models 2.6.3. Environmental Transformation and Distribution of Metal-Containing Engineered Nanoparticles 3. Stable Isotopes as Tracers for Metal-Containing Engineered Nanoparticles 3.1. Advantages of Using Stable-Isotope-Labeled Metal-Containing Engineered Nanoparticles 3.2. Selection of Stable Isotopes for MetalContaining Engineered Nanoparticle Labeling 3.3. Synthesis of Stable-Isotope-Labeled MetalContaining Engineered Nanoparticles 3.4. Basis for Stable Isotope Tracing of MetalContaining Engineered Nanoparticles 3.5. Application of Stable-Isotope-Labeled MetalContaining Engineered Nanoparticles To Probe Their Environmental and Biological Behaviors

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4469 Received: October 9, 2016 Published: February 17, 2017

© 2017 American Chemical Society

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DOI: 10.1021/acs.chemrev.6b00693 Chem. Rev. 2017, 117, 4462−4487

Chemical Reviews 3.5.1. Environmental Fate of Metal-Containing Engineered Nanoparticles 3.5.2. Uptake and Accumulation of MetalContaining Engineered Nanoparticles from Different Exposure Routes 4. Summary and Future Perspectives 4.1. Methods for Preparing Radioactive-IsotopeLabeled Metal-Containing Engineered Nanoparticles 4.2. Effect of Surface Modification and Functionalization of Metal-Containing Engineered Nanoparticles on Their Environmental Fate and Bioaccumulation 4.3. Long-Term Exposure of Metal-Containing Engineered Nanoparticles at Low Doses 4.4. Imaging Techniques for Radioactive- and Stable-Isotope-Labeled Metal-Containing Engineered Nanoparticles 4.5. High-Precision Stable Isotope Ratio Measurements To Enhance the Sensitivity of MetalContaining Engineered Nanoparticle Tracing 4.6. Microcosm and Mesocosm Combined with Isotope Tracers To Study the Behavior of Metal-Containing Engineered Nanoparticles in the Environment 4.7. Hyphenated Multistable Isotope Tracers with Speciation Analysis To Compare the Behaviors of Different Engineered Nanoparticles and Metal Species 4.8. Isotope Fractionation as a Tracer for MetalContaining Engineered Nanoparticles Author Information Corresponding Author ORCID Notes Biographies Acknowledgments Abbreviations References

Review

consequent effects is crucial prior to their clinical use14 and in the development of safer MENPs for both the environment and human health.15 Currently, the identification and tracking of MENPs in environmental and biological systems remain a great challenge. A major difficulty is the effective differentiation between MENPs and interference or artifacts from natural or background-level metallic components.16 For example, in studying the biodistribution of iron oxide NPs as magnetic resonance contrast agents, a distinction must be made between the iron in iron oxide NPs and nutritional iron in organisms. A possible solution is to label and track MENPs in the matrix according to their specific labeling information. Fluorescence (e.g., by organic dye fluorescein isothiocyanate)17 or exogenous radioactive labeling (e.g., by 125I, 188Re, 111In)18−20 can provide sensitive and specific signals. However, these modification methods could potentially change the surface properties of MENPs and subsequently alter their environmental or biological behavior. Additionally, the labels (organic dye or exogenous radioactive tracer) could possibly break away from the MENP core21 and would thus not be representative of the behavior of MENPs. Labeling of MENPs by use of intrinsic radioactive or stable isotopes has recently become a research focus. Isotopic tracers have several advantages when compared to exogenous fluorescence and radioactive labeling. First, they have much greater sensitivity compared to conventional fluorescence labeling due to the range of detection techniques that can be used, including γ spectrometry, scintillation counting, or inductively coupled plasma mass spectrometry (ICP-MS).16 In addition, the specific label signals can be easily distinguished from those of the matrix.22 Furthermore, and importantly, labeled MENPs have essentially the same chemical composition and surface chemistry as unlabeled MENPs and therefore reflect the behavior of MENPs much better than conventional fluorescence and exogenous radioactive labeling, which require additional surface modification of the MENPs.16 Comparably, radioactive isotope tracking is favorable for in situ imaging at individual, tissue, cell, and even subcellular levels, while tracking using multiple stable isotopes can be used to simultaneously monitor the differential behaviors of MENPs of varying morphology, size, and coatings. This review article focuses on the techniques and applications of radioactive and stable isotope tracers to study the environmental fate and biological uptake and distribution of MENPs. We summarize the advantages of intrinsic radioactive/stable isotopes for MENP labeling and discuss the considerations in isotope selection, preparation of labeled MENPs, and exposure routes and detection of labeled MENPs (Figure 1). In addition, the current and future applications of radioactive/stable-isotopelabeled MENPs to study their environmental fate and bioaccumulation are reviewed. Radioactive (14C) and stable isotope (13C) labeling to track carbon-based ENPs are excluded from this review, as they have been previously reported in other studies and reviews.22−24

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1. INTRODUCTION Engineered nanoparticles (ENPs), defined as anthropogenic particles less than 100 nm in size in at least one dimension, have been extensively produced and applied in many sectors such as consumer products, health care, transportation, energy, and agriculture.1 In particular, metal-containing engineered nanoparticles (MENPs), composed of noble metal (Au, Ag, Pt, Pd), metal oxide (ZnO, CuO, CeO2), or quantum dot (QD; CdS, ZnSe) nanoparticles (NPs), are widely used for catalysis,2 sensing,3,4 imaging,5 and disease diagnosis and therapy.6 Nevertheless, during the production, transport, use, disposal, and recycling of MENPs and their products, the release of MENPs into the environment is inevitable.7 Thus, as a class of emerging contaminants,8 MENPs have drawn considerable attention with regard to their environmental fate, their transformation, and their uptake by and toxicity to organisms in recent years.9,10 Of particular concern is their use as diagnostic and therapeutic tools, including as contrast-enhancement agents, nanocarriers, and phototherapy agents,11−13 when the intentional human contact or administration of MENPs for these applications is considered. Therefore, understanding their uptake, distribution, and clearance in the human body and

2. RADIOACTIVE ISOTOPES AS TRACERS FOR METAL-CONTAINING ENGINEERED NANOPARTICLES 2.1. Need for Intrinsic Radioactive Isotopes for Metal-Containing Engineered Nanoparticle Labeling

Although exogenous radioactive elements (e.g., 99mTc, 111In) have been widely used to label MENPs through physical or 4463


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Figure 1. Preparation, exposure, and detection of radioactive- or stable-isotope-labeled MENPs for environmental fate and bioaccumulation studies.

Figure 2. Sketch of double-radiolabeled nanoparticles. Au cores were composed of the radioactive isotope 198Au, and diethylenetriaminepentaacetic acid-chelated radioactive 111In was integrated into the polymer shell. Reprinted with permission from ref 21. Copyright 2015 Macmillan Publishers Limited.

quantitative analysis independent of 198Au and 111In showed significantly different biodistributions for the two elements. While 198Au accumulates mostly in the liver, 111In shows a nonparticulate biodistribution similar to that seen after intravenous injection of chelated 111In (diethylenetriaminepentaacetic acid-111In). This finding strongly supported the contention that in vivo removal of the polymer shell (or the labeled

chemical adsorption, recent studies have demonstrated that these exogenous radioactive tracers can be removed from the MENP core and are thus not adequate for in vivo studies.21,25 Doubleradiolabeled NPs have been recently synthesized by Kreyling et al.21 (Figure 2), using radioactively labeled Au nanoparticles (198Au NPs) as the core and 111In-labeled polymer as a shell around the Au core. After intravenous injection into rats, 4464


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Table 1. Summary of Metal-Containing Engineered Nanoparticles and Their Radioactive and Stable Metal Isotopes radioactive possible isotope 44

Ti 45 Ti

52

Fe Fe

59

60

Cu Cu 64 Cu 67 Cu 61

62

Zn Zn 65 Zn 63

69m

Zn Zn 72 Zn 71m

103

Ag 104 Ag 104m Ag 105 Ag 106 Ag 106m Ag 108m Ag 110m Ag 111

Ag 112 Ag 113 Ag 115 Ag 104

Cd 105 Cd

half-life

stable main decay modea

isotope

radioactive

natural relative abundance (%)

Titanium (TiO2 Nanoparticles) 46 60.4 years γ, ε Ti 47 3.08 h β+ Ti 48 Ti 49 Ti 50 Ti Iron (Iron Oxide Nanoparticles) 54 8.275 h β+ Fe − 56 44.495 β Fe days 57 Fe 58 Fe Copper (Cu, CuO, CuS Nanoparticles) 63 23.7 min β+ Cu + 65 3.333 h β Cu 12.70 h β+, β− 61.83 h β− Zinc (ZnO, ZnS, ZnSe, ZnTe Nanoparticles) 64 9.186 h β+ Zn + 66 38.47 min β Zn 67 244.06 β+ Zn days 68 55.6 min β− Zn − 70 3.97 days β Zn 46.5 h β− Silver (Ag, AgCl, Ag2S Nanoparticles) 107 65.7 min β+ Ag + 109 69.2 min β Ag 33.5 min β+ 41.29 days β+ 23.96 min β+ 8.28 days β+ 418 years β+ 249.78 β− days 7.45 days β− 3.13 h β− 5.37 h β− 20.0 min β− Cadmium (CdS, CdSe, CdTe Nanoparticles) 106 57.7 min β+ Cd 108 55.5 min β+ Cd

possible isotope 107

8.0 7.5 73.7 5.5 5.3

Cd 109 Cd 113m Cd 115 Cd 115m Cd 117 Cd 117m Cd 118 Cd

5.8 91.7 2.14 0.31

189

Au Au 191 Au 192 Au 193 Au 194 Au 195 Au

190

69 31

196

48.9 27.8 4.1

Au Au 199 Au 200 Au 200m Au 201 Au 198

18.6 0.62

130

Ce Ce 133 Ce 133m Ce 134 Ce 135 Ce 137 Ce 139 Ce

51.4 48.7

132

141

Ce

143

Ce Ce

144

a

half-life

stable main decay modea

isotope

natural relative abundance (%)

Cadmium (CdS, CdSe, CdTe Nanoparticles) 110 6.5 h β+ Cd 12.4 111 461.4 days EC Cd 12.8 112 14.1 years β− Cd 24.0 113 53.46 h β− Cd 12.3 114 44.56 h β− Cd 28.8 116 2.49 h β− Cd 7.6 3.36 h β− 50.3 min β− Gold (Au Nanoparticles) 197 28.7 min β+ Au 100 42.8 min β+ 3.18 h β+ 4.94 h β+ 17.65 h β+ 38.02 h β+ 186.10 EC days 6.17 days β+, β− 2.685 days β− 3.169 days β− 48.4 min β− 18.7 h β− 26 min β− Cerium (CeO2 Nanoparticles) 136 22.9 min β+ Ce 0.2 + 138 3.51 h β Ce 0.3 140 97 min β+ Ceb 88.5 142 4.9 days β+ Ce 11.0 3.16 days EC 17.7 days β+ 9.0 days β+ 137.640 EC days 32.501 β− days 33.04 days β− 284.893 β− days

EC, electron capture. bOnly

140

Ce is a stable isotope.

1.2 0.9

lower-energy state can emit a γ photon. The emission of an α particle or an Auger electron (e−) in vivo results in tissue damage and could thus be used in radiotherapy. However, the short penetration distance of these particles in the body prevents their application in imaging. In contrast, radioactive isotopes emitting β+ or γ rays, which have good penetration, are widely used for MENP labeling, tracing, and imaging.27 The physical half-life is another important factor in radioactive isotope selection. A radioactive isotope with too short a half-life is not convenient for experimental operation, while a radioactive isotope with too long a half-life is not favorable for post-treatment of radioactive waste. Table 2 summarizes the recent applications of radioactiveisotope-labeled MENPs to trace their environmental and biological behaviors, including the preparation method, exposure

exogenous radioactive elements) from MENPs is inevitable. When this is considered, the use of intrinsic metal isotopes to label MENPs is appropriate and can essentially guarantee an accurate reflection of MENP behavior by the isotope tracer. 2.2. Selection of Radioactive Isotopes for Metal-Containing Engineered Nanoparticle Labeling

Table 1 provides a list of the possible radioactive isotopes that can be used as MENP tracers, along with their respective halflives. Suitable radioactive isotopes should be first selected according to their nuclear emission properties, physical half-life, cost, availability, and measurement method.26,27 Radioactive isotope decay can be mainly categorized as α, β [β−, β+, and electron capture (EC)], and γ decay. Following α and β decay, the nucleus is often at a high-energy state, and the transition to a 4465


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Table 2. Application of Radioactive-Isotope-Labeled Metal-Containing Engineered Nanoparticles in Tracing Their Environmental and Biological Behaviorsa In Vitro Exposureb radiolabeled MENPs or metal species 198g

Au NP 59 Fe NP, 60Co NP 192 Ir NP (18 nm)

NA of Au NP NA of Fe NP and Co NP synthesis from 192Ir metal precursor synthesis from 241AmO2 synthesis from 241AmO2 NA of CeO2 NP NA of CeO2 NP

241

AmO2 AmO2 141 CeO2 141 CeO2 (28.4 nm), 141CeO2 coated with SiO2 (28.4 nm), nm) 65 ZnO (28 nm), 65ZnO coated with SiO2 (27.6 nm) 57 Co3O4 (300, 700, 800, 1700 nm) 57 Co3O4 (500 nm) 241

exposure route

exposed cell, organism, or environmental matrix

radioactive labeling method

141

CeO2 (119

NA of ZnO NP synthesis from 57Co(NO3)2 synthesis from 57Co(NO3)2 In Vivo Exposurec

radiolabeled MENPs or metal species

ref

MDCK and HepG2 cells SKOV-3 and U87 cell lines isolated lung from male WKY rats

42 43 115

rat, dog, and monkey alveolar macrophages dog alveolar macrophages mouse fibroblast cell line Balb/3T3 human lung epithelial cells

46 45 44 48

human lung epithelial cells human and canine alveolar macrophages Fischer (F-344) rat alveolar macrophages

48 47 116

radioactive labeling method

exposed cell, organism, or environmental matrix

ref

d

iv iv

64

iv iv iv iv iv iv iv it

198

Au NP Au-incorporated Au nanostructure 198 Au nanocage 198 Au NP protein-coated 198Au NP [14C]CIT-[198Au]Au NP 198 Au NP gum arabic-coated 198Au NP

iv

(−) 198Au NP (1.4, 5, 18, 80, 200 nm); (+) 198Au NP (2.8 nm) sulfonated Ph3P-coated 198Au NP (1.4, 18, 80 nm)

iv

Cu nanocluster 64 Cu−Au alloy

198

Injection synthesis from 64CuCl2 precursor synthesis from 64CuCl2 precursor NA of Au NP synthesis from H198AuCl4 precursor synthesis from H198AuCl4 precursor NA of Au NP NA of Au NP NA of Au NP synthesis from

198

Au foil

NA of Au NP NA of Au NP

iv iv iv iv iv iv iv iv, ip iv iv iv iv iv iv iv iv iv iv, it

59

Fe3O4 Fe2O3 59 Fe2O3 59 Fe oxide 59 Fe oxide with different coatings 59 Fe oxide 59 Fe oxide with different sizes and surface charges 59 Fe oxide 59 Fe oxide 65 ZnO NP (10, 71 nm), 65Zn(NO3)2 65 ZnO NP, 69mZnO NP 141 CeO2 uncoated, silica-coated 141CeO2 141 CeO2, 141CeCl3 57 [ Co]CoO@SiO2 131 BaSO4 CIT- or PEG-coated [64Cu]CuS PEG-coated [64Cu]CuS

synthesis from 59FeCl3 precursor synthesis from 59FeCl3 precursor synthesis from 59FeCl3 precursor synthesis from 59FeCl3 precursor synthesis from 59FeCl3 precursor synthesis from 59FeCl3 precursor synthesis from 59FeCl3 precursor synthesis from 59FeCl3 precursor synthesis from 59FeCl3 precursor NA of ZnO NP NA of ZnO NP synthesis from 141CeCl3 precursor NA of CeO2 NP NA of CeO2 NPs and CeCl3 synthesis from 57CoCl2 precursor NA of BaSO4 NP synthesis from 64CuCl2 precursor synthesis from 64CuCl2 precursor

iv iv is it it it

CdSe/CdS/65ZnS CdSe/109CdZnS, CdTeSe/109CdZnSe, 109CdSe, 109CdTeSe 59 Fe2O3 198 Au0 composite nanodevice gum arabic-coated 198Au NP 198 Au NP with EGCg coating

synthesis from 65ZnCl2 precursor synthesis from 109Cd precursor synthesis from 59FeCl3 precursor NA of Au NP synthesis from 198Au foil synthesis from H198AuCl4 precursor

59

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lung tumor-bearing mice normal BALB/c mice and mouse breast cancer model female WKY rats EMT6 tumor-bearing BALB/c mice EMT-6 tumor- bearing mice female WKY rats female C57Bl/6 mice male Sprague-Dawley rats male ICR mice SCID mice bearing human prostate cancer xenografts female WKY rats pregnant rat model on day 18 of gestation mice mice mice wild-type FVB mice healthy adult male Wistar rats mice Swiss mice wild-type FVB mice wild-type FVB mice mice ICR mice female nude mice male Wistar Han rats Wistar Han rats nude mice male Wistar rats Harlan Sprague-Dawley mice male athymic nude mice with anaplastic thyroid carcinoma wild-type FVB/N mice female nude mice mice tumor-bearing male C57BL/6J mice prostate tumor-bearing dogs PC-3 tumor-bearing female SCID mice

77 57 21 73 63 54 74 58 36 117 62 70 50 51 59 25 56 61 72 75 68 71 69 60 64 53 65 55 52 118 67 66 51 119 120 76


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Table 2. continued In Vivo Exposurec exposure route it

inh inh inh endo inh endo

radiolabeled MENPs or metal species gum arabic glycoprotein- functionalized

192

Au NP

195

inh endo inh trp trp

57

Injectiond synthesis from H198AuCl4 precursor

Tracheal Perfusion or Inhalation Exposuree aerosol (15, 80 nm) synthesis from 192Ir metal precursor aerosol synthesis from 192Ir metal precursor aerosol (17−20 nm) synthesis from 192Ir metal precursor aerosol (primary particle size 2−4 nm) synthesis from 192Ir metal precursor aerosol (nominal particle diameter 10, 15, 35, 75 synthesis from 192Ir metal precursor

UF Ir UF 192Ir UF 192Ir UF 192Ir UF 192Ir nm) 195 Au NP (23 nm)

inh

trp trp

198

Au NP (20 nm)

Co3O4 (1100 nm) Co3O4 (800, 1700 nm) 131 BaSO4 198 Au NP (−) 198Au NP (1.4, 2.8, 5, 18, 80, 200 nm); (+) 198Au NP (2.8 nm) 59 Fe3O4 59 Fe2O3 57

SI generation of proton-activated gold electrodes SI generation of proton-activated gold electrodes synthesis from 57Co(NO3)2 synthesis from 57Co(NO3)2 NA of BaSO4 NP NA of Au NP NA of Au NP synthesis from 59FeCl3 precursor irradiation of Fe2O3 NP in heavy-water nuclear reactor synthesis from Fe(NO3)3 precursor NA of ZnO NP NA of CeO2 NP and CeCl3 synthesis from 141Ce(NO3)3 precursor NA of CeO2 NP NA of BaSO4 NP Oral Exposuref NA of Co core/Co3O4 shell NP NA of Fe NP NA of Ag NP NA of Au NP

trp trp trp trp trp trp

59

dietary gavage gavage gavage gavage

60

gavage gavage gavage gavage

NA of ZnO NP NA of CeO2 NP and CeCl3 NA of CeO2 NP NA of BaSO4 NP Implant 110m Ag NP-coated catheter synthesis from 110mAgNO3 precursor Waterborne Exposure for Aquatic Organismsg 110m 110m CIT- and PVP- Ag NP, AgNO3 synthesis from 110mAgNO3 precursor carbonate-coated 110mAg NP adsorption of 110mAg+ to Ag NP 110m Ag NP, 110mAgNO3 synthesis from 110mAgNO3 precursor 110m 110m Ag NP, AgNO3 synthesis from 110mAgNO3 precursor 110m Ag NP with different sizes (20, 50, 100 nm) and adsorption of 110mAg+ to Ag NP coatings (CIT, tannic acid) CIT-110mAg NP (80 nm), 110mAgNO3 adsorption of 110mAg+ to Ag NP 110m Ag NP (80%. The 65Cu-enriched snails were subsequently exposed to benthic algae mixed with natural Cubearing Fe−Al particles. The trace Cu bioavailability from the natural particles could therefore be calculated by measuring the 65 Cu/63Cu ratio in the tissues (Figure 10). Similar techniques could also be applied to study the biological uptake of MENPs, and the main advantage is that the synthesis of isotope-labeled MENPs is not needed.

efficiency of TiO2 NPs and high natural Ti background in organisms indicate a slow accumulation of TiO2 in internal organs and that long-term exposure is needed to evaluate the uptake and assimilation of TiO2 NPs by organisms. 3.5.2.2. Dermal Exposure. Skin is the largest organ, acting as a primary barrier protecting the body from external substances. However, hazardous substances on the dermal surface are potentially absorbed into the body through the stratum corneum and the epidermis toward the dermis and are subsequently transported to other organs through blood flow.159 The interaction of NPs with the skin can occur through unintentional occupational and environmental exposure (e.g., contact with MENP-containing textiles160) or intentional medical or daily application (e.g., photothermal and photodynamic therapy agents,161 sunscreen162). However, the present data on dermal absorption and skin penetration of MENPs remain controversial. Some studies suggest that MENPs cannot penetrate the skin,163,164 while other argue that MENPs are skin-penetrable, depending on the role of intrinsic characteristics of MENPs (e.g., size,165 charge, and surface properties166), solvent or dosage forms,167 and skin condition (damaged or intact).168,169 Therefore, a highly sensitive stable isotope tracing method is required to ensure the detection of very low levels (if any) of dermally absorbed MENPs and distinguish them from background metal signals.143 ZnO NPs are widely used as sunscreen due to their protection against sunburn.151 However, for a long time, the ability of these small-sized NPs to penetrate through human skin remained unknown. Gulson et al.143 were the first to assess this by synthesizing 68ZnO NPs (19 nm) and 68ZnO bulk particles (110 nm), incorporating them into an oil−water formulation of sunscreens, and testing whether the Zn from these particles was absorbed following sunscreen outdoor application on humans. As shown in Figure 9, small amounts of 68Zn from both ZnO NPs and bulk particles were observed in venous blood following sunscreen exposure; nevertheless, comparably higher levels of 68 Zn from ZnO NP exposure were observed in blood. In addition, the Δ68Zn (percent) and amounts of 68Zn tracer in blood following NP exposure were significantly higher than that following bulk exposure for females with the same treatment, but no difference were observed between the NP and bulk groups for males. However, generally, the amount of 68Zn detected in blood after the 5-day application period accounted for only approximately 0.1% of the total Zn in the blood compartment and less than 0.001% of the applied dose, which is minute when compared with the dietary intake of Zn. Nevertheless, as the 68Zn levels in blood continued to increase beyond the 5-day application, it is proposed that the absorbed 68Zn may be concentrated in particular tissues (e.g., epidermis and liver) and is released slowly into the blood. Further studies152,153 confirmed the above results and demonstrated the dermal absorption of Zn from different sunscreen formulations and differing UV exposure conditions.152 Recently, the uptake and distribution of 68Zn tracer in the internal organs of virgin or pregnant hairless mice were reported after application of nanosized and larger 68ZnO particles. 151 Similar to the result of human exposure, concentrations of 68Zn in organs of virgin mice treated with 68 ZnO NPs were significantly higher than in mice treated with larger 68ZnO particles. More importantly, increased concentrations 68Zn tracer was also observed in the fetal livers, demonstrating transplacental transfer of 68Zn. It is estimated that 0.0007−0.02% of bulk ZnO and 0.001−0.04% of ZnO NPs applied were absorbed in different organs, with liver having the

Figure 10. 65Cu/63Cu in soft tissue of freshwater snails (L. stagnalis) after pre-exposure to 65Cu and then dietary exposure to Cu-bearing Fe− Al particles with diatoms. Reprinted from ref 171. Copyright 2013 American Chemical Society.

4. SUMMARY AND FUTURE PERSPECTIVES Radioactive or stable isotope tracers, due to their advantage of intrinsic labeling, have proved helpful in the enhancement of detection of MENPs in the environment and organisms. An increase in their application in the tracing of MENP environmental fate, biouptake, and transformation is expected. Although isotope tracers provide great opportunities to further elucidate the behavior of MENPs in biological and environmental systems, there remain many unresolved issues and areas that require further exploration. The following advancements could enhance the significance of isotope tracer methods and contribute to understanding the distribution and fate of MENPs. 4.1. Methods for Preparing Radioactive-Isotope-Labeled Metal-Containing Engineered Nanoparticles

Currently, the reported radiolabeled MENPs are still very limited, possibly due to the lack of adequate preparation methods. There remain great challenges in the preparation of more radioactive-isotope-labeled MENPs with suitable half-lives and radioactivity to trace their behavior in biological and environmental systems. The synthesis of radiolabeled MENPs 4478


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multicollector (MC)-ICP-MS.139,141,142,153As the concentration of isotope-labeled MENPs is quantified by the variation of isotope ratio, the precision of stable isotope ratio measurements is very important for the sensitivity of MENP tracing. The use of high-resolution MC-ICP-MS could provide high-precision data with minimal levels of uncertainty and, thus, offer low detection limits and allow the detection of ENPs at environmentally or ecotoxicologically relevant concentrations against background levels.139,141 For example, by use of quadruple ICP-MS, 107 Ag/109Ag ratios can generally be measured with a precision no better than 1%. However, improved data with a precision of more than 0.02% can be obtained for 107Ag/109Ag by use of MCICP-MS coupled with an effective cleanup technique.142 Thus, the application of stable isotope labeling enhances the tracing sensitivity by at least 40-fold (for quadruple ICP-MS) and possibly by up to approximately 4000-fold (for MC-ICP-MS).142 Therefore, the application of high-precision MC-ICP-MS is highly promising to decrease the exposure concentration of MENPs to environmental or toxicologically realistic scenarios in further studies.

from their radioactive precursors or the direct radiolabeling of MENPs by use of ion-beam or neutron irradiation need to be optimized to produce MENPs of similar chemical composition, morphology, and surface modification to those we commonly used. 4.2. Effect of Surface Modification and Functionalization of Metal-Containing Engineered Nanoparticles on Their Environmental Fate and Bioaccumulation

Surface modification and functionalization of MENPs is an essential prerequisite for their successful applications,172 determining their interactions with environmental173 and biological interfaces.174 These interactions have a crucial impact not only on the colloidal stability (e.g., dissolution175 and aggregation176,177), transport,178 and environmental fate179 of MENPs but also on their uptake,180−182 blood circulation time,13,54,183 organ- or tumor-specific distribution,184,185 and toxicity186,187 in organisms. Intrinsic labeling with radioactive or stable isotopes provides a powerful tool for probing the fate of MENPs in environmental and biological systems. More importantly, coexposure of different coated/functionalized MENPs labeled with various stable isotopes (e.g., 107Ag for CIT-Ag NP and 109Ag for PVP-Ag NP) makes it possible to compare their environmental and biological behaviors simultaneously in one system.

4.6. Microcosm and Mesocosm Combined with Isotope Tracers To Study the Behavior of Metal-Containing Engineered Nanoparticles in the Environment

The fate and behavior of MENPs in the environment are highly sensitive to factors such as temperature, sunlight, natural organic matter, ionic strength, and the presence of plants, sediments, and bacteria.192 Therefore, the behavior of MENPs in highly controlled laboratory settings is unlikely to be reflective of their behavior under environmentally relevant conditions.192 Micro- or mesocosm studies could provide a more realistic approach by linking environmental scenarios with the behavior of MENPs. For example, a pond microcosm could include water, sediment, aquatic plants, and animals with varying trophic levels, which could simulate the distribution of MENPs in different compartments as well as food chain biouptake and possible bioaccumulation. Unfortunately, micro- or mesocosm experiments without the involvement of isotope tracers require high MENP concentration to distinguish their signal from that of the background. Consequently, the experimental settings do not accurately reflect the fate of environmental-level MENPs. However, the use of isotope tracers in micro- or mesocosm experiments could enhance the detection sensitivities for MENPs, and thus environmental levels of MENPs could be applied to better reflect a more realistic condition. In addition, the use of stable or radioactive isotopes with a suitable half-life allows the long-term monitoring of MENPs in environmental and biological systems, thus elucidating the long-term impacts of MENPs.

4.3. Long-Term Exposure of Metal-Containing Engineered Nanoparticles at Low Doses

The toxic effects of MENPs are usually observed under acute or subacute conditions at high doses. However, realistic exposure scenario studies of the effect of long-term (over 3 months) lowdose exposure are extremely important, but missing to a large extent, to elucidate the toxicity of MENPs.188,189 Long-term studies on the uptake, accumulation, distribution, and toxicity of MENPs are urgently needed to fully evaluate the toxicity of low MENP concentrations by using in vivo and in vitro models. Radioactive- and stable-isotope-labeled MENPs could play a critical role in tracing ultralow concentrations of MENPs in various organisms. 4.4. Imaging Techniques for Radioactive- and Stable-Isotope-Labeled Metal-Containing Engineered Nanoparticles

Imaging MENPs, in vivo or ex vivo, can provide direct information on their biodistribution and fate in organisms.190 Unfortunately, there are only a few reports on tissue imaging of radioactive-isotope-labeled MENPs in organisms by macroautoradiography and ECT techniques.32−36 High-resolution autoradiography (e.g., light microscope autoradiography37,38 and electron microscope autoradiography39,40) is suitable for cellular and subcellular localization of radioactive-isotope-labeled MENPs in biological organisms and should be further evaluated in future studies. Laser ablation−ICP-MS190 and secondary ion mass spectrometry191 could also potentially be used for 2D imaging of stable-isotope-labeled MENPs in organisms, although its spatial resolution needs to be further improved. Nevertheless, the utilization of imaging techniques will undoubtedly enrich our knowledge on the biological uptake, distribution, clearance, and possible effects of MENPs.

4.7. Hyphenated Multistable Isotope Tracers with Speciation Analysis To Compare the Behaviors of Different Engineered Nanoparticles and Metal Species

Multi-isotope tracing coupled with speciation analysis has been widely applied in species transformation and biological uptake studies of various toxic elements, especially Hg.193−195 However, to date, there are no reports on the transformation, uptake, and distribution of ENPs and metal species with multistable isotope tracers. Various speciation analytical methods have been developed to distinguish and quantify MENPs and metal ions (e.g., different-sized Ag NPs, AgCl, Ag2S, and Ag+) including ultrafiltration,196,197 cloud point extraction,198,199 size-exclusion chromatography,200 capillary electrophoresis,201 and field-flow fractionation.155,202 Multistable isotope tracers to label MENPs

4.5. High-Precision Stable Isotope Ratio Measurements To Enhance the Sensitivity of Metal-Containing Engineered Nanoparticle Tracing

The stable isotope ratio could be measured by conventional ICPMS (e.g., quadrupole ICP-MS)140,144,145 or high-resolution 4479


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and ions could be used to compare their behavior and study their intertransformation in the same system. For example: (1) through the synthesis of MENPs of varying size, morphology, or crystallinity (e.g., different-sized nano-ZnO labeled with 64Zn, 66 Zn, and 68Zn) and integration with speciation analytical techniques, their differential ion dissolution, uptake, and distribution can be compared in the same environmental or biological system. (2) In addition, different behaviors (e.g., adsorption from water to sediment, uptake by organisms) between MENPs and the corresponding metal ions can be compared by use of double stable isotope tracers (e.g., 107Ag NP and 109Ag+). (3) Last, but not least, double stable isotope tracers coupled with speciation analysis techniques could be used to measure the individual gross rates of two co-occurring transformation processes (e.g., dissolution and adsorption) simultaneously.

environmental fate and transformation of engineered nanomaterials/ toxic metals, especially by use of isotope tracing. Zhiqiang Tan was born in Shandong, China, in 1982. He obtained his B.S. in environmental sciences at Hebei University, China, in 2005 and then received his M.S. in environmental sciences under the supervision of Professor Xiandeng Hou from Sichuan University, China, in 2008. He obtained his Ph.D. in environmental sciences in 2011 under the supervision of Professor Jingfu Liu at RCEES, CAS, Beijing, China, and then became a postdoctoral researcher with Professor Guibin Jiang from 2011 to 2013. He is currently an associate professor at RCEES, CAS. His research focuses on analytical methods, environmental processes, and applications of micro/nanomaterials. Ligang Hu was born in Hubei, China, in 1976. He received his B.S. in chemistry at the University of Science and Technology, Beijing, China, in 1997 and obtained his Ph.D. in environmental sciences in 2006 from RCEES, CAS. He then continued his research at Florida International University and the University of Hong Kong as a postdoctoral fellow. He is now a professor of environmental chemistry at RCEES, CAS, with his current research focusing on environmental health and biogeochemical cycling of heavy metals.

4.8. Isotope Fractionation as a Tracer for Metal-Containing Engineered Nanoparticles

It has been reported that isotope fractionation can occur in the physical and chemical transformation of many elements, including Fe, Zn, Cu, and Cd. Isotope fractionation could be used as an intrinsic tracer to probe the source and transformation of these elements.203 Nevertheless, isotope fractionation in the transformation of MENPs is still not well understood, although studies have observed Fe isotope exchange between aqueous Fe2+ and nanoparticulate mackinawite,204,205 goethite,206 and magnetite,207 indicating possible isotope fractionation during the dissolution, adsorption, and redox transformation. Furthermore, a study found significant differences in Ag isotope ratios among a colloidal Ag dietary supplement, decanethiol-functionalized Ag NPs, and Ag in X-static socks.208 It was since demonstrated that the formation and dissolution of Ag NPs under natural conditions (e.g., under sunlight) caused significant variations in the ratio of natural Ag isotopes, with an isotopic enrichment factor of up to 0.86‰, and that engineered Ag NPs have distinctly different isotope fractionation effects than their naturally formed counterparts.209 These results suggest that the isotope ratio is a potential intrinsic tracer to differentiate between naturally occurring nanoparticles and synthetic MENPs, and to probe MENP sources as well as the transformation of MENPs in the environment.

Sujuan Yu received her Ph.D. in environmental sciences from University of Chinese Academy of Sciences in 2014 and then joined Professor Jingfu Liu’s research group. Her research focuses on the environmental behavior and effects of silver nanoparticles. Jingfu Liu is a professor of environmental chemistry at RCEES, CAS. He received his B.Sc. in 1986 from Jiangxi University and his Ph.D. in 2002 from CAS. In 2006, he finished his postdoctoral research in Lund University in Sweden and joined RCEES with the 100 Talents Project of Chinese Academy of Sciences. He was awarded the National Science Fund for Distinguished Young Scholars in 2010. He is the author and coauthor of over 200 peer-reviewed original research papers and invited reviews and coeditor of two books. His research interests involve environmental analytical chemistry, as well as environmental processes and effects of persistent toxic substances and emerging contaminants such as engineered nanomaterials. Guibin Jiang is a professor of environmental science at RCEES. He received his B.Sc. from Shandong University in 1981 and his Ph.D. from CAS in 1991. He completed his research work at the National Research Council of Canada (1989−1991) as a visiting scholar and at the University of Belgium (1994−1996) as a postdoctoral fellow. He has published more than 500 papers in peer-reviewed international scientific journals and has given more than 380 lectures, including plenary and keynote lectures at international and national meetings. Since 2006, he has been an associate editor of the journal Environmental Science & Technology, published by the American Chemical Society. He was honored with the prestigious Chang Jiang Scholars Achievement Award in 2007 and the Agilent Thought Leader Award in 2013. He was elected as a member of the Chinese Academy of Sciences in 2009 and as a fellow of the Third World Academy of Sciences in 2012. His research mainly focuses on environmental analytical chemistry and toxicology of persistent toxic substances.

AUTHOR INFORMATION Corresponding Author

*Telephone +86-10-62849192; fax +86-10-62849192; e-mail jfl[email protected]. ORCID

Jingfu Liu: 0000-0001-7134-7026 Notes

The authors declare no competing financial interest. Biographies

ACKNOWLEDGMENTS We thank the National Key Research and Development Program of China (2016YFA0203102), the National Natural Science Foundation of China (21337004, 21522705, 21377156), the Strategic Priority Research Program of the Chinese Academy of Sciences (XDB14020101), and Key Projects for Frontier Sciences of the Chinese Academy of Sciences (QYZDB-SSWDQC018) for their support. Y.Y. acknowledges support from the Youth Innovation Promotion Association of the Chinese

Yongguang Yin was born in Hebei, China, in 1981. He received his B.S. in chemistry at Chongqing University, China, in 2002 and then received his M.S. in analytical chemistry under the supervision of Professor Zhining Xia from Chongqing University in 2005. He obtained his Ph.D. in environmental sciences in 2008 with the guidance of Professor Guibin Jiang at Research Center for Eco-Environmental Sciences (RCEES), Chinese Academy of Sciences (CAS), Beijing, China. Currently, he is an associate professor at RCEES, CAS. His research focuses on 4480


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Academy of Sciences. We also express our sincere thanks to the anonymous reviewers for their valuable comments and suggestions on this paper.

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