FATE AND TRANSPORT PROPERTIES OF ARISTOLOCHIC ACIDS AS POTENTIAL EXPOSURE AGENTS RESPONSIBLE FOR BALKAN ENDEMIC NEPHROPATHY
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1 Proceedings of the 13 th International Conference on Environmental Science and Technology Athens, Greece, 5-7 September 2013 FATE AND TRANSPORT PROPERTIES OF ARISTOLOCHIC ACIDS AS POTENTIAL EXPOSURE AGENTS RESPONSIBLE FOR BALKAN ENDEMIC NEPHROPATHY C. TANGTONG 1, L. QIAO 1, D.T. LONG 1,2, AND T.C. VOICE 1,2 1 Civil and Environmental Engineering, Michigan State University, East Lansing, MI USA 2 Geological Sciences, Michigan State University, East Lansing, MI USA address: voice@msu.edu EXTENDED ABSTRACT Balkan endemic nephropathy (BEN) is a kidney disease that occurs in certain rural villages in Bosnia, Bulgaria, Croatia, Romania and Serbia and is thought to be linked to an unknown environmental toxin. In 1969, Professor Ivić of the University of Niš, first proposed that BEN could be caused by ingestion of Aristolochia clematitis, citing evidence of renal failure in horses thought to have consumed hay contaminated with this plant. He suggested that human exposure occurs as a result of Arisotolochia clematitis growing in wheat fields, resulting in contamination of flour by the seeds that are similar in size to the wheat grain, and consumption of bread baked from this flour. Studies have identified at least two compounds termed aristolochic acids (AA) that are found in Aristolochia species, exhibit both nephrotoxicity and carcinogenicity, and are likely responsible for what is termed Chinese herb nephropathy. Several recent toxicological studies offer a growing body of evidence AA is responsible for BEN, as Ivić hypothesized, however the exposure pathway is still unclear. In this study, we explore the basic fate and transport properties of aristolochic acids that could affect human exposure in the regions where BEN occurs. We hypothesize that exposure could occur as a result of release of AA from Arisotolochia clematitis, either as root exudates or through decomposition after the growing season. The released AA could be taken up by food crops, but transport would likely be affected by soil sorption/desorption processes. To evaluate the feasibility of this hypothesis, we measured the octanol-water partition coefficient (K ow) because this reflects the hydrophobicity of contaminants and typically correlates with several important environmental partitioning processes. We also directly measured soil sorption. Sorption isotherm experiments and kinetic studies were conducted using soils with different organic matter and clay contents. AA I and II were relatively hydrophyllic (log K ow < 2) under basic conditions and relatively hydrophobic (log K ow > 3) in acidic solutions. Since the pk as of AA I and II are 3.3 and 3.2, respectively, we could expect significant transport by water under natural environmental conditions. Sorption isotherms of AA conformed to both the linear and Freundlich models and a positive correlation between the partition coefficient (K d) and organic matter was observed. The linear organic-carbon-normalized partition coefficient (log K oc) was in the range of , suggesting significant uptake by high organic matter soils despite the fact that AA would be in an anionic form at the ph of the experiments. It was also observed that binding to dissolved organic matter could significantly affect transport, but this needs further study. We interpret these preliminary findings to suggest that plant uptake of AA is possible, but that additional work is necessary in order to produce quantitative estimates of exposure. Keywords: sorption, aristolochic acid, Balkan endemic nephropathy, octanol-water partition coefficient, plant uptake
2 1. INTRODUCTION Aristolochic acids (AAs) are chemicals that are naturally found in plants of Aristolochia and Asarum species, which have been used in traditional herbal medicines as antiinflammatory agents, diuretics, and in the treatment of edema (IARCS, 2002). The medicinal use of AA containing herbs has long been questioned due to concerns over their effects on the kidneys, and in the 1980s researchers suggested that AAs are also carcinogenic (Mengs, 1987, 1988). Their nephrotoxicity became clear in the 1990 s when over 100 cases of rapidly developing renal disease in young women in Belgium were linked to the use of an herbal preparation made from Aristolochia species (Vanherweghem et al., 1993). The disease has subsequently been termed Aristolochic acid nephropathy (AAN). Balkan endemic nephropathy (BEN) is a kidney failure disease that occurs in certain rural villages in Balkans countries (e.g. Bosnia, Bulgaria, Croatia, Romania and Serbia) that was first reported about 60 years ago. AAs were first suspected by Ivić (1969) who found renal failure in horses that had consumed hay contaminated with this plant, and he proposed that human exposure occurred through the contamination of flour resulting from Aristolochia species growing in wheat fields and co-mingling of the seeds and grain during harvest. Recently, several groups of researchers have established a number of similarities between BEN and AAN, and some now suggest that AAs are the likely cause of BEN. However, there is problem with the hypothesis that exposure occurs through contamination of flour because the seeds of Artistolochia clematitis do not mature until autumn, and are found only in a large fruit at the time of wheat harvest in early summer. It is highly likely that this fruit would be removed during either threshing or milling, where there are numerous safeguards in place to prevent contamination of the flour by foreign objects. The motivation for this study was to explore alternative pathways by which human exposure to AA could occur. We hypothesize that AAs could be released from plants, either as root exudates or through decomposition, and taken up by other plants that either serve as food crops, or are consumed by livestock. To evaluate this hypothesis, we need to understand the fate and transport properties of AA in soil environments. Based on our review of the literature, little basic information is available on the environmental behavior of AA, or even the critical properties affecting behavior. The purpose of this study is to produce this information and make a preliminary assessment of whether the hypothesized exposure pathway is feasible. 2. BACKGROUND Aristolochic acids are a family of compounds with similar chemical structures, the most common being AA I and AA II, shown in Table 1. In their pure form, AAs are yellow solids, slightly soluble in water and completely soluble in acetic acid, acetone, chloroform, diethyl ether and ethanol (IARCS, 2002). Their melting points are between o C (Barceloux, 2008). Their acidity constants, expressed as log pk a, were reported at 3.3 and 3.2 for AA I and II, respectively (Fu et al., 2011). A critical parameter for assessing environmental transport of a chemical is its octanolwater partition coefficient, K ow, because this can be related to solubility, soil-water partitioning, and bioaccumulation. To our knowledge, there are few reported values of K ow for AAs and most of these were calculated using quantitative structure activity relationships (QSAR). These are suspected to have large errors due to absence of reliable fragment values for the complex AA structure (Han et al., 2012). Recently, the log K ow of AA I and II were reported at 4.45 ± 0.07 and 3.99 ± 0.06, respectively using the
3 reverse-phase high pressure liquid chromatography (RP-HPLC) method (Han et al., 2012), indicating that these compounds are relatively hydrophobic. Although this method is appealing due to its simplicity, there are also questions about its accuracy related to the behavior of organic acids in the mobile phase and the selection of appropriate reference substances necessary for calibration. Table 1. Chemical structure of Aristolochic acid I and II Compound Structure Formula Aristolochic acid I C 17H 11NO 7 (8-methoxy-6-nitro-phenanthro (3,4-d)- 1,3-dioxolo-5-carboxylic acid) Aristolochic acid II C 16H 9NO 6 (6-nitro-phenanthro (3,4-d)- 1,3-dioxolo-5-carboxylic acid) Assessment of chemical transport in soils requires a quantitative understanding of soil sorption phenomena. It is established that hydrophobic compounds are strongly bound to soil organic matter in what is termed hydrophobic bonding, and this can be described by the organic carbon normalized soil-water partition coefficient, K oc, which in turn, correlates to K ow. However, there may be other bonding mechanisms involving specific functional groups on the chemicals. In the case of organic acids, such as AA, this can be complicated by the effect of ph which results in the possibility of two chemical forms of the chemical. Thus, the specific aim of this study was to measure K ow and K oc of AAs by direct methods in order to predict the sorption behavior of AAs in soil environments. 3. MATERIALS AND METHODS AA I and II were measured by RP-HPLC, using a C-18 column, a 70:30 methanol: water with 0.1% phosphoric acid mobile phase, an eluent flow of 1ml/min, and detection by ultraviolet absorption at 255 nm. Octanol-water partition coefficients (K ow ) were determined using the shake flask method following OECD 107(1995). K ow was also determined by RP-HPLC method using OECD 117(1989) for comparison. A set of aromatic organic acids with some structural similarity to AAs, and for which K ow values determined by shake flask were available, were selected as reference substances (Table 2). The ph of mobile phase was controlled at 3.07, which is lower than pk a of reference compounds to keep them in non-ionized form. Soil-water partition coefficients were measured in batch isotherm studies (OECD, 2000). Two different samples varying in organic carbon content of two different soil series (< 2 mm fraction) were studied (Table3). Isotherm conditions involved a 100:1 (0.01 M CaCl 2 solution: soil) ratio in glass centrifuge tubes with Teflon-lined caps, initial AA concentrations ranging from µg/ml, orbital shaking at 150 rpm for 24 h, separation by centrifugation at 7,500 rpm for 30 min, and analysis of the supernatant by RP-HPLC.
4 The ph after equilibration for all soils was between 4.6 and 6.5, indicating that both AAs were in the anionic form. It was verified that losses due to sorption to the centrifuge tubes was less than 5% of the AA added. Table 2. pk a and log K ow of reference substances for RP-HPLC method Chemical MW pka Log Kow benzoic acid a 1.87 a 3-nitrobenzoic acid a 1.83 a 1-naphthoic acid b 3.1 b (1- naphthalene carboxylic acid 1-naphthaleneacetic acid c 2.24 d 1-naphthoxyacetic acid (1-naphthyloxyacetic acid) e 2.60 d a (Ming et al., 2009); b (Han et al., 2012) ; c (Dippy, Hughes, & Laxton, 1954); d (Burgos & Pisutpaisal, 2006) ; e ("1-Naphthoxyacetic acid,") Table 3. Physical and chemical characteristics of soils Soil ph* %OC Composition Soil texture % clay %silt %sand Wooster CT Wooster NF Bulk density (g/cm 3 ) Silt loam Silt loam 1.38 Hoytville CT Hoytville NF Silty clay loam Silty clay loam CT and NF refer to conventional tilled (CT) and native forest (NF) sites, respectively * Soil ph was determined in CaCl M at soil: solution ratio 1:5 Experimental data were fit to the linear partitioning and Freundlich isotherm models, and the organic carbon normalized partition coefficient was calculated using measured organic carbon results: C s = K d C e (1) C s = K f C e 1/n (2) K oc = K d 100% (3) %OC where C s is the equilibrium concentration in the solid phase (µg/ml), C e is the equilibrium concentration in the solution phase (µg/g), K d is the soil partition coefficient (ml/g), K f is the Freundlich capacity factor, 1/n is the Freundlich exponent, K oc is the organic carbon normalized partition coefficient (g/ml)and %OC is the mass percentage of organic carbon of the soil. The DOC content of the aqueous phase was measured by total organic carbon analyzer.
5 4. Result and discussion The average log K ow values of AA I and II from the shake flask method at three concentrations (5.3, 8.0 and 10.7 µg/ml) were 1.65 and 1.23, respectively. The average ph of solution was 6.05 indicating that the anion form of AA was dominant. However, the log K ow values obtained from the RP-HPLC method were 3.71 and 3.27, for AA I and II, respectively. These values suggest that the protonated acids exhibit moderate hydrophobicity as the ph of the mobile phase was well below the pk a values of both acids. The log K ow values of the neutral form for organic acids are typically two orders of magnitude higher than the anion form, and this result is consistent with that observation (Schwarzenbach et al., 2003). Kinetic studies showed that the sorption of AAs to all soils was rapid, reaching equilibrium within 24 hr of mixing (Figure 2). After this period, the standard deviation of sequential aqueous phase concentrations in time was less than 2%. Figure 3 shows the sorption isotherms and linear regression fits for AA I to all four soils. Correlation coefficients were > 0.9 in all cases. As some nonlinearity can be seen, these data were also fit to the Freundlich equation (Eq. 2), and similar coefficients were found (Table 4). These results are consistent with what is typical at low concentrations when sorption is dominated by partitioning to soil organic matter (Schwarzenbach et al., 2003). Table 4. Linear and Freundlich isotherm parameters for sorption of AA I to soil Soil Linear isotherm Freundlich isotherm K d (ml/g) K oc (ml/g) r 2 K f (µg 1-1/n g -1 )(ml 1/n ) 1/n r 2 Wooster CT , Wooster NF , Hoytville CT , Hoytville NF ,
6 Partition coefficients increased linearly with organic carbon content (Figure 4). This might suggest that even though the sorbates were anionic at the ph in the sorption experiments, partitioning to the soil occurs via a hydrophobic mechanism. No correlation was found between K d and clay or sand content, which could result from repulsion between the sorbate anions and negative surfaces of the minerals (Burgos & Pisutpaisal, 2006). However, the contradiction between moderately high K oc values and the low K ow values for the anion forms of AA, may suggest that other sorption mechanisms are operative. From the structure of AAs, we can assume that the phenanthrene group is responsible for hydrophobic interactions whereas the carboxylic acid and nitro groups may participate in other specific interactions such as H-bonding with polar groups in the organic matter (Westall et al., 1999). The high value of K oc may also result from the effect of CaCl 2 in the background solution. Ca 2+ can adsorb to the soil and make surface charge less negative, thereby decreasing electrostatic repulsion to AA anions (Jafvert et al., 1990). The average log K oc values for AA I and II, calculated from Eq. 3, are 3.22 and 2.95, respectively. This indicates that AA I is more hydrophobic than AA II, which may result from the methoxy group (OCH 3) of AA-I which is polar and may have specific interaction with carboxyl, hydroxyl or phenolic group of organic matter (Chefetz et al., 2004). DOC concentrations in the solution phase at the end of the sorption experiments increased with soil concentration (or with soil to solution ratio) (Figure 5) and K d decreased with increasing DOC (Figure 6). This suggests that AAs may form complexes with dissolved organic material or adsorb to colloids which cannot be separated from the aqueous phase by centrifugation (Delgado-Moreno et al., 2010). This implies that DOC can shift the distribution of AAs toward the solution phase and may play an important role in mobilizing AAs in the environment.
7 5. CONCLUSIONS Octanol-water and soil sorption data suggest while AAs in the natural environment are anionic they are highly adsorbed to organic matter in soil, apparently by hydrophobic interactions. AAs also can associate with dissolved organic matter. This study shows the need to better understand the mechanisms by which both the anionic and neutral forms of AA interact with both soils and dissolved organic matter in order to assess possible human exposure. ACKNOWLEDGEMENT We thank for Dr. Alvin Smucker for contributing the soil samples. LITERATURE CITED 1. 1-Naphthoxyacetic acid. Retrieved March 10, 2013, from Naphthoxyacetic%20acid.asp 2. Barceloux, D. G. (2008). Medical Toxicology of Natural Substances: Foods, Fungi, Medicinal Herbs, Plants, and Venomous Animals Aristolochic Acid and Chinese Herb Nephropathy: John Wiley & Sons. 3. Burgos, W. D., & Pisutpaisal, N. (2006). Sorption of naphthoic acids and quinoline compounds to estuarine sediment. Journal of Contaminant Hydrology, 84(3-4), doi: /j.jconhyd Chefetz, B., Bilkis, Y. I., & Polubesova, T. (2004). Sorption-desorption behavior of triazine and phenylurea herbicides in Kishon river sediments. Water Research, 38(20), doi: /j.watres Delgado-Moreno, L., Wu, L., & Gan, J. (2010). Effect of Dissolved Organic Carbon on Sorption of Pyrethroids to Sediments. Environmental Science & Technology, 44(22), doi: /es102277h 6. Dippy, J. F. J., Hughes, S. R. C., & Laxton, J. W. (1954). Chemical constitution and the dissociation constants of monocarboxylic acids.14. monomethylcyclohexanecarboxylic acids. Journal of the Chemical Society(DEC), doi: /jr Fu, X. F., Liu, Y., Li, W., Bai, Y., Liao, Y. P., & Liu, H. W. (2011). Determination of dissociation constants of aristolochic acid I and II by capillary electrophoresis with carboxymethyl chitosan-coated capillary. Talanta, 85(1), doi: /j.talanta Han, S. Y., Qiao, J. Q., Zhang, Y. Y., Lian, H. Z., & Ge, X. (2012). Determination of n- octanol/water partition coefficients of weak ionizable solutes by RP-HPLC with neutral model compounds. Talanta, 97, doi: /j.talanta IARCS - International Agency for Research on Cancer Staff. (2002). Some Traditional Herbal Medicines, Some Mycotoxins, Naphthalene and Styrene Iarc Monographs (pp. 590 p.). Retrieved from Ivić, M. (1969). Etiology of Endemic Nephropathy (in Serbian). Lijec Vjesn., 91, Jafvert, C. T. (1990). Sorption of organic-acid compounds to sediments - initial model development. Environmental Toxicology and Chemistry, 9(10), doi: / (1990)9[1259:sooact]2.0.co;2 12. Mengs, U. (1987). Acute toxicity of aristolochic acid in rodents. Archives of Toxicology, 59(5), doi: /bf
8 13. Mengs, U. (1988). Tumor-induction in mice following exposure to aristolochic acid. Archives of Toxicology, 61(6), doi: /bf Ming, X., Han, S. Y., Qi, Z. C., Sheng, D., & Lian, H. Z. (2009). Chromatographic retention prediction and octanol-water partition coefficient determination of monobasic weak acidic compounds in ion-suppression reversed-phase liquid chromatography using acids as ion-suppressors. Talanta, 79(3), doi: /j.talanta OECD. (1989). OECD Guideline for the testing of chemicals Partition Coefficient (noctanol/water), High Performance Liquid Chromatography (HPLC) Method. 16. OECD. (1995). OECD Guideline for the testing of chemicals Partition Coefficient (noctanol/water): Shake Flask Method. 17. OECD. (2000). OECD Guideline for the testing of chemicals Adsorption - Desorption Using a Batch Equilibrium Method. 18. Vanherweghem, J. L., Depierreux, M., Tielemans, C., Abramowicz, D., Dratwa, M., Jadoul, M.,... Vanhaelen, M. (1993). Rapidly progressive interstitial renal fibrosis in young-women - association with slimming regimen including chinese herbs. Lancet, 341(8842), Schwarzenbach, R. P., Gschwend, P. M., & Imboden, D. M. (2003). Environmental Organic Chemistry (2nd Ed.). New Jersey: John Wiley & Sons, Inc. 20. Westall, J. C., Chen, H., Zhang, W. J., & Brownawell, B. J. (1999). Sorption of linear alkylbenzenesulfonates on sediment materials. Environmental Science & Technology, 33(18), doi: /es
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