ARTICLE pubs.acs.org/est
Human Nails Analysis as Biomarker of Exposure to Perfluoroalkyl Compounds Wei Liu,† Lei Xu,† Xiao Li,† Yi He Jin,*,† Kazuaki Sasaki,‡ Norimitsu Saito,‡ Itaru Sato,§ and Shuji Tsuda§ †
Key Laboratory of Industrial Ecology and Environmental Engineering, MOE, School of Environmental Science and Technology, Dalian University of Technology, Dalian 116024, China ‡ Research Institute for Environmental Sciences and Public Health of Iwate Prefecture, Morioka Iwate 020-0852, Japan § Laboratory of Veterinary Public Health, Department of Veterinary Medicine, Faculty of Agriculture, Iwate University, 3-18-8 Ueda, Morioka 020-8550, Japan
bS Supporting Information ABSTRACT: Extensive human exposure to perfluoroalkyl compounds (PFAA) together with their persistence and various toxicities have arisen increasing concern. A noninvasive method would improve exposure assessment for large population, especially the children susceptible to contaminants. The aim of the study was to assess the use of PFAA measurements in human nails as a biomarker of exposure to PFAAs. Fingernail, toenail, and blood samples were collected from 28 volunteers. The PFAA concentrations were determined by high performance liquid chromatography-tandem mass spectrometry (HPLC-MS/MS). Six PFAA were detected in nails, with perfluorooctane sulfonate (PFOS) being the compound with the highest median concentration (33.5 and 26.1 ng/g in fingernail and toenail, respectively). Followed was perfluorononanoate (PFNA), with the median concentrations of 20.4 and 16.8 ng/g, respectively, in fingernail and toenail. Other PFAA detected were perfluorooctanoate (PFOA), perfluorodecanoate (PFDA), perfluorododecanoate (PFDoA), and perfluorotetradecanoate (PFTA), with median levels ranging between 0.19 and 8.94 ng/g. PFOS and PFNA concentrations in fingernail significantly correlated with those in serum. Fingernail PFOS and PFNA levels were 2.8 and 24.4 times, respectively, higher than the serum levels. The accumulation of PFAA in nails, together with its advantages in noninvasive sampling and ability of reflecting long-term exposure, made nails PFAA an attractive biomarker of exposure.
’ INTRODUCTION The perfluoroalkyl compounds (PFAA) are a family of commonly used synthetic surfactants, consisting of a perfluorinated carbon backbone and a charged functional moiety. PFAA have found extensive application in clothing, carpets, and food packaging as well as in paints, polishes, and fire-fighting foams. The two most widely known PFAA include perfluorooctane sulfonate (PFOS) and perfluorooctanoate (PFOA). Ever-increasing reports come forth describing the distribution of PFOS, PFOA, and other PFAA in human bodies in many different geographical locations around the globe.13 Further, there has been a great deal of toxicological research, most focusing on PFOS and PFOA and recently extending to other PFAA, advancing understanding the hazards of these compounds.2 PFOS was included into Annex B of Stockholm Convention on persistent organic pollutants due to its negative impact on human health and the environment in May 2009.4 PFAA are persistent against the typical environmental degradation processes and are very slowly eliminated from the human body due, in part, to enterohepatic recirculation.5,6 Exposure to PFAA is widespread and some subpopulations, living in proximity r 2011 American Chemical Society
to or working in fluorochemical manufacturing plants, are highly contaminated.7,8 An increase in human exposure to PFAA over time was observed in some areas.9,10 PFAA bioaccumulation has become an increasing human health concern as emerging evidence suggests reproductive toxicity, neurotoxicity, and hepatotoxicity, and some PFAA are considered to be likely human carcinogens.2,11 Epidemiologic evidence remains limited, and to date data are insufficient for health risk assessment of PFAA. The lack of accurate, quantitative measures of exposure is one of the sources of uncertainty in epidemiologic studies, limiting the power of such studies to enable definitive conclusions about the association between exposure and disease.12 An extensive amount of data have recently become available describing concentrations of PFAA in human tissues. In most Special Issue: Perfluoroalkyl Acid Received: October 26, 2010 Accepted: March 11, 2011 Revised: February 16, 2011 Published: March 22, 2011 8144
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Environmental Science & Technology cases, the PFAA were analyzed in blood, including whole blood, plasma, and serum. In some studies, the statistical significance of the data has suffered from small sample size. Ease of collection and level of invasiveness are commonly cited reasons why study participants fail to provide biospecimens for research purposes.13 Especially for the children, very few data are available aside from a few cord blood samples and blood spot measurements.2,3,14 Furthermore, in view of the persistence and bioaccumulation properties of PFAA, the chronic health risk posed by low-level exposure should be determined by biomarker that could reflect long-term exposure. In comparison to other biological samples, there are many advantages in utilizing nails as biomarker of exposure, especially because specimen collection is noninvasive and the nails can be easily sampled, stored, transported, and handled.15 The noninvasive sampling would facilitate research concerning children and large population. Moreover, once compounds are incorporated into keratin of nails, the levels remain isolated from other metabolic activities in the body with no fluctuation due to changing body metabolic activities. Thus, nails could reflect long-term exposure. Besides, nails take several months to grow out and are used for the measure of past exposure.16 Human nails have been extensively employed as a biomarker of toxic element exposure and nutritional mineral status.15,17 The purpose of the present study is to assess the use of PFAA measurements in human fingernails and toenails as a biomarker of exposure to PFAA. The analytical methods were optimized and validated by serial quality assurance/quality control procedures. Furthermore, the correlation between PFAA concentrations in serum and nails were evaluated.
’ EXPERIMENTAL SECTION Reagents. All reagents were used as received. Milli-Q water was cleaned using Waters Oasis HLB Plus cartridges (Milford, MA) to remove the potential residue of PFAA, called PFAA-free water. Mixed stock PFAA standard solution was prepared in methanol. All the equipments involved in the sample collection, preparation, and analysis were precleaned with methanol and PFAA-free water. No Teflon and glass equipment were used during the whole experiment. Details were presented in the Supporting Information. Samples Collection. Fingernail, toenail, and blood samples were obtained from 28 healthy volunteers, 2050 years old, during April-October, 2009. They are students and teachers in Dalian University of Technology, representative of the general population with no occupational exposure. Ten of the volunteers are females and 18 are males. Children were not recruited in the present study because serial nail and blood samples were collected from the subjects at different times, while multiple blood samplings from children are difficult. Three blood samples from each volunteer were collected in April, June, and August, respectively. Fingernail samples were collected behind the blood sampling in June, August, and October, considering the potential lag time between serum level and the detection in nails. Toenails were collected in August and October, since the toenails grow more slowly than the fingernails. Nail clippings were collected from all 10 fingers and toes with a stainless nail cutter. Nail varnish was prohibited for the volunteers during the sample collection to avoid possible contamination. The nature and purposes of the study were explained verbally and in writing to the subjects, who signed an informed consent document.
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Sample Pretreatment. Human nails have been extensively employed as a biomarker of toxic metal exposure and essential trace element. However, few studies use nails as biomarker of exposure to organic pollutants. Therefore, the preparation procedures adopted in the present study were developed based on the methods described in related literatures concerning element measurement in nails and further optimized according to the physical-chemical properties of PFCs as well as to facilitate the instrumental analysis. The preparation procedures of nail samples were optimized first. Then the optimal procedures were employed for preparing nail samples in the followed experiments. The procedures adopted during nails sample pretreatment are (1) washing, (2) desiccation, (3) digestion, (4) extraction, and (5) cleaning, which are procedures usually used for the preparation of nail samples.15 Approximately 0.1 g of nail samples were placed in 15 mL polypropylene (PP) tube and twice washed with a 1% solution of Triton X-100 in an ultrasonic bath for 20 min. After this treatment, the samples were rinsed three times with PFAA-free water samples and once with methanol to remove any residue detergent. The washed samples were allowed to dry at 60 °C overnight in a drying oven. After cooling, the dried samples were weighed. Then, samples were digested with 1 mL of HNO3/H2O2 (V:V = 1:1) in a water bath at 60 °C for 2 h. Then sodium hydroxide solution was added to the resultant digest to adjust pH to neutral. The ion pair extraction method (IPE) was employed, with 1 mL of 0.5 M tetrabutylammonium hydrogensulfate (TBAHS) added as ion-paired reagent. Subsequently, twice extraction with 5 mL of methyl tert-butyl ether (MTBE) for 5 min each time was conducted. After centrifuging for 10 min at 3500 rpm, the supernatant of MTBE was collected. The two supernatants were combined in another 15 mL PP tube. The MTBE solvent was evaporated to dryness under a gentle flow of high purity nitrogen. The analytes were redissolved in 1 mL of acetonitrile. Then the insoluble impurity was removed by centrifugation (4 °C, 12000 rpm, 30 min). The supernatant was collected and evaporated under a nitrogen gas flow and reconstituted in a 500 μL mixture of acetonitrile and 10 mM ammonium acetate (2:3, v/v). The resultant solution was then ready for instrumental analysis. The blood samples were analyzed as serum after centrifugation, and the serum was extracted by the IPE method described by Hansen et al.18 Details were presented in the Supporting Information. Washing and Digestion Efficiency. In order to investigate the influence of the washing and digestion procedures on measurements, pool fingernail samples collected from healthy volunteers were used, as there is no suitable nail certified reference material at this time. PFOS, the most prevalent PFAA, was measured after various treatments, because its relatively high detection frequency and levels enable the comparisons. The ultimate goal of washing is to completely remove loosely adhering external PFAA associated with fat, sweat, and dirt without altering the endogenous PFAA contents of the samples. The detergent was used instead of solvents to avoid the risk of extraction of PFAA bound to nail matrix, while the protocols of washing fall into two approaches, such as use of either detergents or organic solvents for metal measurement in nails.15,19 Further, detergent washing appears more advantageous in that it corresponds more closely to in situ washing.19 The nail samples were washed by 1% solution of the Triton X-100 in an ultrasonic bath for 20 min each time, and the washing efficiency was evaluated employing different washing times. Comparisons to determine 8145
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Environmental Science & Technology the utility of the washing procedures were evaluated with the use of two “identical” samples. Because PFAA concentrations can vary from one nail to another, the comparison samples resulted from splitting each individual nail clipping into two equal portions vertically with respect to the axis of growth. It was reported that essentially identical samples could be prepared by this splitting technique.19,20 Hence, the influence of the variation in the PFAA concentrations in different samples was avoided. Each half sample accounts to approximately 0.1 g in weight. The paired samples were treated by no washing, once, twice, or thrice washing. The complete digestion of the nail samples is crucial for the extraction of PFAA due to the compact structure of nails. Besides, some precipitate is formed after acid digestion and dilution because nail samples contain a large concentration of proteins.20 This can cause problems such as inhomogeneity of digested sample solutions and affect extraction efficiency. The nail samples are usually digested by acid for element measurement, 15 and alkaline digestion has been used for measure PFAA in bivalve tissues.21,22 Digestion efficiencies using HNO3, HNO3/H2O2, HNO3/HClO4, or KOH, heated or under room temperature, were compared. Instrumental Analysis of PFAA. The PFAA were analyzed via high performance liquid chromatography-tandem mass spectrometry (HPLC-MS/MS, Agilent, Palo Alto and Santa Clara, CA) under optimum instrumental conditions. Details were presented in the Supporting Information and elsewhere.23 Quality Assurance/Quality Control. Data quality assurance and quality control protocols included matrix spikes, laboratory blanks, and continuing calibration verification. The QC materials were prepared from cattle hoof, as a surrogate matrix for human nail samples, because a piece of cattle hoof could provide enough amounts of materials for test method blanks, method recovery, and matrix effect. And neither blank nail material nor enough low concentration human nail samples were available. Matrix effect caused by human nails is expected to be reflected by cattle hoof, considering both are mainly composed by keratin. The cattle hoof was grounded to powders, mixed uniformly, and divided into subpools. One subpool was used as a matrix blank QC and to prepare the calibration standards, and the other two were spiked with PFAA as needed to afford low-concentration and highconcentration subpools. The internal standards, 13C4PFOS and 13C2PFOA, were added into the QC samples before extraction. No PFAA were detected in the cattle hoof. During the analysis, procedural blanks were run with the same protocol as actual samples after every twenty samples to check for possible contamination occurring in the pretreatment process. Solvent blanks were also run after every ten samples to monitor the instrumental background. Calibration standards were run after every twenty samples to ensure the precision and accuracy of each run. In consideration of the matrix effect, calibration standards were matched with cattle hoof sample extracts. Nine extracted standard analyte concentrations encompassing the entire method were used to construct the calibration curves (0.1100 ng/g). The peak area ratio of each analyte to internal standards, 13C4PFOS for the sulfonates and 13C2PFOA for the carboxylates, were used for quantification of QC samples. The LOD was defined as the analyte peak required yielding a signal-to-noise (S/N) ratio of 3:1. The limit of quantification (LOQ) was defined as the analyte peak required yielding a signalto-noise (S/N) ratio larger than 10:1 or the lowest point on the calibration curve calculated to be within 30% of its actual value. Both recovery and reproducibility of the extraction were validated in six replicate analysis by spiking 1 ng and 10 ng of each
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Table 1. LOD, LOQ, and Recovery for the Analytical Method of Nail Samples Evaluated by Surrogate Matrix recovery (%) compound
LOD (ng/g)
LOQ (ng/g)
10 ng/g
100 ng/g
PFOA
0.12
0.38
104 ( 19
112 ( 9.8
PFHxS
0.08
0.25
76.2 ( 8.4
72.4 ( 4.6
PFNA PFDA
0.39 0.13
1.3 0.42
85.2 ( 7.2 81.7 ( 7.8
99.6 ( 16 85.6 ( 4.9
PFOS
0.07
0.24
95.2 ( 10
97.0 ( 11
PFDoA
0.24
0.81
76.8 ( 8.7
79.5 ( 8.1
PFTA
0.10
0.33
66.9 ( 5.4
76.1 ( 9.3
standard into QC blank samples (0.1 g). Reproducibility was further confirmed by analyze identical human nail samples prepared as described above. No significant difference was observed between results of QC samples quantified with or without using internal standards, possibly because the standards extracted from the surrogate matrix effectively amend for the matrix effect on extraction and instrumental analysis. Therefore, the human nails/serum samples were extracted and quantified without using internal standards. Statistical Analysis. All statistical analysis was performed using SPSS 15.0 (Chicago, IL, USA). For data calculating, concentrations below LOQ were assigned a value of half the LOQ. Spearman’s correlation coefficient was used to assess the association between PFAA concentrations in fingernail, toenail, and serum samples. Wilcoxon matched pairs ranks test were used for comparison between concentrations in various groups.
’ RESULTS AND DISCUSSION Quality Assurance/Quality Control. The calibration standards using spiked cattle hoof were prepared to compensate for the matrix effects on the analytes’ recovery during the extraction procedure and in their extent of ionization, thus resulting in highly accurate and precise methods. The LOQ for the preferred analytical procedure ranged from 0.24 to 1.3 ng/g for the PFAA analyzed (Table 1). Further, the procedure achieved the recoveries in the range of 66.9104% and 72.4112% from the 10 ng/g and 100 ng/g PFAA-spiked matrices, respectively (Table 1). Among the six paired human nail samples, PFOS, perfluorononanoate (PFNA), perfluorododecanoate (PFDoA), and perfluorotetradecanoate (PFTA) were detected, while other PFAA were below LOQ in parts of or all the subjects. The deviation between the replicates of the nail samples were less than 20% (Table S1). The chromatography of PFAA standards, blank, and human nails were presented in Supporting Information (Figures S1 and S2). No obvious variations in the retention time, response, and peak width of the chromatography for PFAA standards before and after 20 injections were observed, suggesting a robust analytical method (Figure S3). Although internal standards were not used for quantification of all the samples, the reproducibility of the analytical procedure tested by the QA/QC strategies ensure the accuracy of the results of the present study. Washing and Digestion Efficiency. Among the acid and alkaline digestion solutions, HNO3/H2O2 exhibited strong digestion capability and heating with a water bath at 60 °C obviously accelerate the digestion process. The addition of HClO4 showed no enhanced digestion efficiency. The nail samples could 8146
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Table 2. Descriptive Statistics of PFAA in Fingernail, Toenail (ng/g), and Serum (ng/mL) Samples PFHxS fingernails
toenails
serum
a
PFOS
PFOA
PFNA
PFDA
PFDoA
PFTA
∑PFAAb
detection (%)a
0
100
30
100
100
100
mean ( SD
-
44.7 ( 36.5
1.75 ( 3.14
28.7 ( 31.9
7.41 ( 5.10
11.8 ( 9.20
9.82 ( 7.01
203 ( 116
median
-
33.5
0.19
20.4
5.84
8.94
8.42
178
GMc
-
27.3
0.48
18.4
5.95
9.36
7.86
170
range
-
1.41165
0.05(), analyzed by Spearman analysis. b Range in parentheses was presented due to small sample size and high scatter.
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Environmental Science & Technology 8.5, 5.4, and 3.8 years, respectively, for PFHxS, PFOS, and PFOA.33 Therefore, serum PFAA levels also represent past exposure, although it is prone to be affected by recent exposure. The overlaps existing among exposure periods reflected by the nails and the serum possibly resulted in the missing correlation between samples collected concurrently or with an interval. Mean PFAA levels in nail/serum samples collected at different times offset partly for the effect of overlap among exposure periods, thus a correlation between mean nail and serum PFAA levels was observed as mentioned above. The correlation between fingernail and toenail PFOS levels appeared to be more significant, as a higher correlation coefficient was observed with longer sampling interval. The correlation coefficients were 0.54, 0.63, and 0.70, respectively, between the fingernail and toenail samples collected concurrently, with an interval of 2 months or 4 months. The lag time between PFAA intake and detection in toenails is expected to be longer than fingernails, because toenails have a lower growth rate than fingernails (up to 50% slower). As Buzalaf reported, the lag times for fluoride detection in fingernail and toenail were 101 and 123 days, respectively.29 However, such a trend was not observed for PFDA, PFNA, PFDoA, and PFTA. More research is needed to determine the lag time between PFAA intake and nail detection and nail/serum samples collected from subjects with known increased PFAA intake would be valuable for such research. Buzalaf et al.29 suggested that the overlaps in the expected lag time existed among the digits caused by different growth rate and would affect data analysis when using all fingernails and/or toenails. As for PFAA analysis in nails, using all fingernails and/or toenails collected is warranted to obtain enough samples for accurate analysis at trace level. The overlaps in the lag time between different digits are expected to have a slight effect on data interpretation when the nails analysis is mainly used for long-term exposure assessment. The limitations of nail as a biomarker of exposure mainly resulted from the debate about the ability to distinguish between endogenous target compounds and the exogenous derived from external contamination.34 The washing method employed appeared to be able to remove the exogenous PFAA effectively. The similar fingernail/toenail PFAA levels further confirmed the less possibility of exogenous contamination. Before nails analysis can become an alternative biomarker, reliable data on baseline or background nail contamination levels in the general population are needed for evaluation of the results from a given site. Moreover, interlaboratory study on analytical technique for trace level PFAA in nails samples is warranted to validate the application of nails analysis in exposure assessment. Besides, the influence of the growth rate on the PFAA level measured in the nails, dependent on gender, age, and sampling time, will be evaluated in a future study, which is helpful for determining the predictive values and specificity of nails. Another argument about the application of nails PFAA concentrations for exposure assessment and health effect diagnosis may be that serum samples are likely needed to measure other biomarkers of health effects/disease. It is expected that the nail samples are collected and analyzed for the exposure assessment of the general population, especially large population and children. For the subject with high PFAA levels in nails and potential health effects, the serum will be only collected where it is necessary to evaluate health effects and disease. Thus, the blood drawing could be avoided or remain minimal.
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Besides, nails have been employed along with hair in measuring elemental status for nutritional evaluation, disease diagnosis, and exposure profile because they are similar in structural composition and development.15 Both are easily and noninvasively collected, with minimal cost, and easily stored and transported. The accumulation of PFAA might also be detected in hair, while further research is needed. Compared with nails, more biological factors influence compounds levels in hair, including length, color, types, growth rate, and cycle. In another hand, hair samples are advantageous to monitor historical exposure by segment analysis.35 PFAA analysis in hair is ongoing in our laboratory. In summary, the accumulation of PFAA in nails and the correlation with blood level suggest that the utility of nails as a biomarker is as good as that of blood PFAA. Furthermore, the ability of reflecting long-term exposure would improve the assessment for the chronic health risk of PFAA. And the ease of noninvasive sampling, transportation, and storing facilitate the epidemiologic studies for large population or track exposure over long period, making nails an attractive biomonitoring substrate for exposure assessment. Both the fingernails and toenails are appropriate materials due to similar detection levels. The choice would depend on the purpose of the study, considering that fingernails grow faster and provide a large amount of samples, whereas toenails grow slowly and may provide a longer integration of exposure. Besides, using the total ten nails are suggested to provide enough samples for accurate analysis at trace level.
’ ASSOCIATED CONTENT
bS
Supporting Information. Additional information on materials and methods. Chromotography of PFAA standard, blanks, human nails, and repeated injections. Replicate analysis of human nail samples. Washing efficiency for nail samples. Correlation between PFAA concentrations in serum, fingernail, and toenail samples collected concurrently or with an interval. This material is available free of charge via the Internet at http://pubs.acs.org.
’ AUTHOR INFORMATION Corresponding Author
*Phone/Fax: þ86 411 84708084. E-mail:
[email protected].
’ ACKNOWLEDGMENT We gratefully acknowledge the volunteers who donated nails and blood samples for this study. We are also grateful to Dr. Christopher Lau and Dr. Andrew B. Lindstrom, from the National Exposure Research Laboratory, U.S. Environmental Protection Agency, for their valuable comments and to Dr. Xiaorong Ran and Zhixu Zhang, from Agilent Technologies, for assistance in instrumental analysis. The study is financially supported by National Nature Science Foundation of China (20837004), National science & technology pillar program during the eleventh five-year plan period (2006BAI06B02), and Program for Changjiang Scholars and Innovative Research Team in University (IRT0813) ’ REFERENCES (1) Houde, M.; Martin, J. W.; Letcher, R. J.; Solomon, K. R.; Muir, D. C. G. Biological monitoring of polyfluoroalkyl substances: A review. Environ. Sci. Technol. 2006, 40 (11), 3463–3473. 8149
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