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,232 Journal of Food Protection, Vol. 47, No. 3, Pages 232-236 (March 1984) Copyright5, International Association ol Milk. Food and Environmental Sanitarians HOTICS: This material may fe# by copyright. Plant Contamination by PCBs from Amended Soils BRIJ L. SAWHNEY and LESTER HANKIN'* ' Departments ofSoil and Water andBiochemistry and Genetics, The ConnecticutAgricultural Experiment Station, Box 1106, New Haven. Connecticut06504 (Received for publication September 6.19S3) ABSTRACT Plants accumulated PCBs (Aroclors) from soil amended with lake sediment contaminated with Aroclors 1248, 12S4, and 1260. Uptake into different parts of vegetable plants was investigated in the field by growing beets (Beta vulgaris L.), turnips (Brassica rapa L.) and beans (Phaseolus vulgaris L.). In beets and turnips, leaves accumulated larger concentrations of PCBs than the roots. In beans, leaves and pods contained higher concentrations than the stems, while only low concentrations were detected in the seeds. Bioac cumulation of Aroclors by plants was in the following order: Aroclor 1248 > 1254 > 1260. Relative to their concentration in the soil, the lower chlorinated PCB isomers which are more soluble in water and more volatile were more abundant in plants then the higher chlorinated isomers. PCBs (polychlorinated biphenyls), a group of toxic and persistent organic compounds, have been extensively used in a number of industrial products. Although no longer man ufactured in this country, their prior manufacture, use and disposal have resulted in their entry into the environment, particularly in sediments of streams and rivers. Fish caught from contaminated water contain PCBs in excess of the 5 mg/ kg tolerance limit established by the U.S. Federal Food and Drug Administration (4). Tolerances for other food products vary from 0.3 mg/kg in eggs to 1.5 mg/kg (on a fat basis) in milk and manufactured dairy products [4). Presence of PCBs in river sediments continues to be a source for their entry into the food chain. A possible method to decontami nate rivers is to dredge and dispose the sediments on land.. However, it is essential to know whether plants growing on contaminated land would take up the PCBs, and thus become another pathway for their entry into the food chain. PCBs manufactured in the U.S. have been marketed under. the trade name Aroclors (Monsanto Chemical Co.). Most common preparations of Aroclors are 1242, 1248, 1254, and 1260; the last two digits indicate the average percentage of chlorine in the PCB molecule. Each Aroclor preparation con tains a number of chlorobiphenyl isomers. Investigations of PCB uptake by plants are sparse and mostly limited to either one or more individual chlori nated biphenyl isomers or a single PCB preparation added to the growth medium. Iwata et al. (9), in studies of up take of Aroclor 1254 by carrots, found that 97% of the Aroclor taken up from the soil was retained by the carrot peels. These researchers also detected the Aroclor in the foliage and attributed its presence primarily to absorption of contaminated soil dust. Fries and Marrow (5) used in-, dividual isomers in their study and attributed their pres ence in the foliage of soybean plants to contamination from vapor sorption. Accumulation of air-bome PCBs by plant foliage has recently been demonstrated by Buckley (2). Experiments with y4C-labelled Aroclor 1254 showed only small concentrations in soybean and fescue (20). Or chard grass and carrots grown in a soil contaminated with PBBs (polybrominated biphenyls) showed no or very minor uptake {11). Similarly, Chou et al. /J) found that when soybean and com seedlings were grown in a nutri ent medium containing ,4C-labelled PBB isomers for about a 1-week period, plant roots contained radioactive residues but no radioactivity was detected in the leaves. These authors also found PBB in concentrations ranging from about 38 to 535 pg/kg in radish, carrot, and onion roots grown in two soils contaminated with 100 mg of PBB/kg. Above ground portions of the crops, however, were not analyzed in these experiments. ' In contrast to these investigations, Babish et al. (/) found that cabbage grown on a 120-cm deep deposit of anaerobi cally digested sewage sludge contaminated with PCBs con tained about 400 pg of PCBs/kg and the liver from guinea pigs fed on this cabbage showed higher PCB concentrations. than the liver from guinea pigs fed on cabbage from the con trol plots. In a study by Strek etal. (16), beet and peanut tops accumulated as much as 815 and 473 pg of ;,,C-labelIed Aroclor 1254/kg, respectively, from a sandy soil to which 20 mg of Aroclor/kg was added. Uptake of ;4C-labelled di- and tri -chlorobiphenyl isomers by spruce seedlings over a 4-year growth period, as determined from total raioactive residue, was 401 pg/kg and 231 pg/kg in needles and stems, respec tively (13). In a sand culture experiment, Suzuki et al. (17) detected 150 pg/kg in soybean sprouts grown in sand treated with 100 mg of Aroclor 1242/kg. These authors inserted a 7-cm thick layer of uncontaminated sand through which the soybeans grew into the contaminated sand. As the analysis of the "barrier'' sand showed no PCBs, the uptake by the bean sprouts was considered to have occurred by PCB trans location through the plant roots. JOURNAL OF FOOD PROTECTION. VOL. 47. MARCH I9S4 PCB-ARCH-EXT0378331 PLANTS CONTAMINATED WITH PCBs 233 Thus PCB uptake by crop plants growing on a contami- , nated growth medium have been shown to occur either through sorption of the volatilized PCBs or through their translocation via root uptake. Quantitative determination of the uptake of different Aroclors from contaminated environ mental sources containing mixtures of Aroclors, however, has not been attempted. In the present investigation, we de termined uptake of different Aroclors, as well as individual chlorobiphenyl isomers present in the Aroclors, by plants grown in field soil amended with lake sediment containing . Aroclors 1248,1254and 1260. . .; . . . -~ .. . MATERIALS AND METHODS . " . Source erfPCBs and soil amendment " ' ' Bottom sediment from Woods Pond, which is contaminated with PCBs ~ and is obviously a source of PCBs in the Housatonic River system (6), was ' . |- used as an amendment for so3 on which vegetables were grown. The' sedi- \ ment contained 4.6 mg ofAroclor 1248,8.0 mg of Aroclor 1254, and 44.5 '' = mg/ of Aroclor 1260/kg on a dry-weight basis. Seven hundred and fifty-six ' 5, liters of sediment (about 30% solids) were poured on the surface of a ; - 2 mx 2 m soil plot isolated in the field by 2.5 cmx 15 cm wooden boards ' inserted into the ground. WhcB the amended plot appeared air-dried, the sur- . ; face 15 cm of soil was thorongly mixed. A control plot was similarly con structed and treated with water instead of sediment. ; '!, Sampling andpreparationofplant material , . ; In May 1981, turnips {Srassica rapa L.) and red beets (Bela vulgaris L.) . were planted in each plot. Both leaves and roots were harvested on October 15, 1981. washed with warm water while scrubbing with a brush to ensure removal of any adhering soil particles. All plant material was dried in a . forced-air oven at 1CTC. Tests showed no loss of PCBs by drying plant mate rial at this temperature. The dried parts were then ground in a stainless steel Wiley mill to pass through a 20-mesh sieve. In May 1982, turnips and snap beans (Paaseolus vulgaris L.) were planted in the same plots without any further addition of sediment. Turnip leaves were harvested three times dur ing the growing seasion, whereas beans were harvested only once. . Extraction and analyses ofPCBs '. ` '' Ten-g samples of dried, ground plant material were extracted with 150 ml of petroleum ether and 20 g of the amended soil were extracted with 150 ml 1:1 acetoneihexane mixture. The extracts were purified to remove inter- ' feting chlorinated compounds (18.19) and analyzed with a gas chromatog raph (GC) equipped with a^Ni electron capture detector. A 180-cm glass column (2 mm i.d.) filled with 3% OV-1 on Chromosorb W (80/100 mesh) w as used. Details of the purification of extracts, operating conditions of the chroma!ograph and the method for determination ofdifferent Aroclors from the resulting chromatograms are described in an earlier publication (75). RESULTS AND DISCUSSION Uptake of PCBs from amended soil Figure 1 shows gas chromatograms of PCB extracts from soil amended with sediment containing PCBs and from leaves of bean plants grown on the amended soil and on control soil. Leaf extracts were concentrated to 2 ml. whereas the soil extract was diluted to 200 ml to obtain optimum peak heights. Peaks 1 through 20 corres pond to different chlorobiphenyl isomer peaks present in individual preparations of Aroclors 1248, 1254, and 1260 (Table 1). The lower numbered peaks with lower reten tion times (RTs) correspond to the less chlorinated biphenyls and higher numbered peaks to more chlorinated biphenyls. The data in Table 1 also show that the peaks obtained from individual preparations of the three Aroc- Retention Time, min Figure 1. Gas chromatograms of extracts from field soil amended with lake sediment contaminated with PCBs and from leaves of bean plants grown on contaminated and control soils. lors overlap, with peaks of lower chlorinated biphenyls more abundant in Aroclor .1248 and peaks of higher .. chlorinated biphenyls more abundant in Aroclor 1260. The peaks in the gas chromatograms (Fig. 1) clearly show that leaves of the bean plant grown in the amended soil contained PCBs that were present in the amended soil while the bean plants grown on the control soil con tain no detectable PCBs. Heights of the different peaks, however, show that leaves contain relatively larger con centrations of the lower chlorinated biphenyls and smaller concentrations of the higher chlorinated biphenyls than . the amended soil. Bioaccumulation ofdifferent Aroclorsfrom soil Uptake of different chlorobiphenyls by plants in relation to their contents in the amended soil is illustrated in Fig. 2 by ratios of peak heights of individual chlorobiphenyls in ex tracts from the plants to those from the soil. The ratios appear to decrease with increasing retention times. Ratios of the low chlorinated biphenyls (the first 7 peaks), in leaves, to corres ponding biphenyls in soil, are greater than 1, while ratios of the remaining biphenyls are less than 1 and decrease with in- JOURNAL OF FOOD PROTECTION. VOL. 47, MARCH 1984 PCB-ARCH-EXT0378332 234 SAWHNEY and hankin , ; creasing chlorination. The relationship between the ratio of the lower chlorinated biphenyls. These results are in agree the GC peaks in leaves to peaks in soil and retention times ment with observations of Iwata et al. (9) and Suzuki et al. of peaks (Fig. 2) show that under experimental conditions (/ 7) who used individual Aroclors and found that peaks with used, bioaccumulation by plants of chlorobiphenyls with re early retention times, corresponding to less chlorinated tention times less than 12 min increases rapidly with decrease biphenyls, were higher in carrots and soybeans. in chlorination. Bioaccumulation of the less chlorinated Estimates of amounts of different Aroclors, 1248, biphenyls corresponding to the first seven GC peaks was 20 1254, and 1260, obtained from analyses of peak heights 60 times as high as the most chlorinated biphenyl corres (15) in extracts from different plant materials harvested . ponding to the last peak. Other parts of these plants and other in 1981 are given in Table 2. Comparison of concentra plant species also showed uptake of larger concentrations of tions of different Aroclors in roots and leaves of both TABLE 1. Heights ofgas chromatographicpeaks obtainedfrom in dividual standardpreparations ofAroclors 1248.1254 and 1260... Heighi, mm Peak number 1248 1254 . 1260 1 2 3 . 4 5 6 7 : 8 9 . 10 11 12 4 - . ' - % 18 - * - 10 -' 42 * . ' .' 16 " ; ; .: ' 25 ' ' 14 ' - ''A . A*. ' , . . ' - - '. ' . v 23 ... 7 .v 21 2 '- ' ' 41 23. ' ... . 8 16 - .. 2 - ,3 . 9 21 .9 ` 6 12 4 beets and turnips suggest that leaves accumulate greater concentrations of each of the three Aroclors; for example, beet roots contain 15, 16, and 35 p.g/kg, respectively, of Aroclors 1248, 1254, and 1260 while beet leaves con tain 22, 94, and 52 p.g/kg of the three Aroclors. Total concentrations of the three Aroclors in beet roots and leaves and in turnips roots and leaves were 66 and 168 and 66 and 99 pg/kg, respectively. These results are in contrast to those of Iwata and Gunther (JO) who found. much higher concentrations of Aroclor 1254 in the carrot ` roots than in the foilage of carrots grown on a soil to which 100 pg/kg Aroclor 1254 was added. . -' ' Rarios of the concentrations of different Aroclors in the plants grown in 1981 to their concentrations in the soil,- the bioaccumulation .factor (BF), show that bioaccumula tion.by plants was Aroclor 1248 > 1254 > 1260 (Table . 13 8 19 6 2). The relative bioaccumulation factor (RBF), i.e. the 14 6 20 22 BF factor of .Aroclor 1248 or 1254 compared to Aroclor 15 16 ' 17 18 19 20 4 15 - . 3 . - 12 - 3 . - 2 - 2 29 ' 13 20 16 12 19 "2 p.lofO.2 |ig/m! standard solution of each Aroclor were used. . 1260, shows that bioaccumulation of Aroclor 1248 was 94 times more than 1260 by beet roots and 188 times more by turnip roots. Bioaccumulation of Aroclor 1254 was 4 times more than 1260 by the two root systems. The RBF for Aroclor 1248 was 69 for beet leaves and . 200 for turnip leaves and for Aroclor 1254 it was 12 for : beet leaves and 11 for turnip leaves. These trends would be expected whether PCBs are sorbed by the leaves as . vapors or translocated through the root system via passive transport in the water stream because both the vapor pres sure and the solubility of the Aroclors are in the order ' 1248 > 1254 > 1260 (8). . .' Figure 2. Ratios of GC peak heights from extracts of beet leaves grown on a soil amended with lake sediment contaminated with PCBs to the corresponding peaksfrom soil extracts. Numbers.with in the circles indicate peak number (see Table I). Ratios for peaks 2 and 4 are not shown infigure because they lie beyond the selected graph scale. Concentrations of PCBs in various parts of the vegetables grown in the amended soil during the second year are given in Table 3. A comparison of the PCB concentrations in tur nips grown in the amended soil in the two years (Table 2 vs. Table 3) shows a decrease in Aroclor 1248 uptake relative to Aroclors 1254 and 1260 in the second year. This decrease is likely due to a large reduction in the amount of Aroclor 1248 in the soil after the first year; indeed, only traces of Aroclor 1248 were detected in soil during the second year of cropping, and hence, no certain measurable concentration of 1248 in the second year is given here. Iwata et al. (9) also noted the lower GC peaks corresponding to less chlorinated biphenyls in the Aroclor 1254 applied to soil disappeared fas ter than higher peaks; a 20% decrease occurred in peak number 1 in 10 months, whereas peak 10 remained essen tially the same during this period. Greater losses of the less chlorinated biphenyls can occur either by volatilization or by degradation. Our experiments (7) on microbial degradation of PCBs in soil cultures show that the less chlorinated JOURNAL OF FOOD PROTECTION. VOL. 47. MARCH 19S4 PCB-ARCH-EXT0378333 PLANTSCONTAMrNATEDWTTH PCBs * ' 235 biphenyls degraded more readily in soils. Also, the degree of degradation was different in different soils and varied with , cropping history of the soil. For example, 90% of Aroclor 1248 in sediment added to a fine sandy loam soil in com was degraded in a 2-week period, while only 20% was degraded in a similar soil in a pine forest. The losses of PCBs due to volatilization would be minimal in culture experiments be cause the reaction was carried out in flasks stoppered with cotton plugs that prevented direct exposure of the reaction . mixture to the atmosphere. .' . ' Although the mechanism of PCB degradation is not clear, ease of degradation of the less chlorinated Aroclors may be related to their higher solubility in water. Data in Table 3 show that turnip leaves harvested on three different dates contained similar concentrations of the Aroc- lors, except that Aroclors 1254 and 1260 were somewhat higher in the last harvest. Greater concentrations in unpeeled ' than peeled turnips are in accord with results with unpeeled and peeled carrots (9). High concentrations in peels of crop roots likely result from diffusion and dissolution of PCBs in organic constituents of peels which are in close proximity to contaminated soil particles. Presence of PCBs in leaves, . stems, pods and small amounts in seeds may be attributed, at least in part, to their uptake and translocation into various plant parts. These results and uptake of PCBs by soybean sprouts grown in sand culture (17) and their detection in rice grains (74), demonstrate that PCBs can be taken up by plant roots and translocated to above ground parts of plants.The mechanism by which these non-polar, neutral large organic molecules are taken up and translocated into the plant is not clear at present, but must be similar to uptake of organo- chlorine pesticide residues in soils (72). Results of this investigation thus show that plants grown in soil contaminated with PCBs can absorb these compounds. How-ever, the amounts taken up by the plant are relatively small compared to amounts in soil. The up take may occur through sorption of vapors from volatili zation of PCBs or through root absorption and transloca tion. Greater uptake of the less chlorinated biphenyls than their more chlorinated counterparts can be due to their higher volatility in the former and to higher water solubil ity in the latter process. ACKNOWLEDGMENTS The authors thank J. Damschroder and M. Birks for able technical assistance during this investigation and to W. Glowa for gas chromatog raphic analyses. . , REFERENCES 1. Babish, J. G., G. S. Stoewsand, A. K. Furr, T. P. Parkinson, C. A. Bache, W. H. Gutenmann, P. C. Wszolek, and D. J. Lisk. 1979. Elemental and polychlorinated biphenyl content of tissues and intestinal aryl hydrocarbon hydroxylase activity of guinea pigs fed cabbage grown on municipal sewage sludge. J.- Agric. Food Chem. 27:399-402. . 2. Buckley, E. H. 1982. Accumulation of airborne polychlorinated biphenyls in foliage. Science 216:520-522. ` 3. Chou, S. F., L. W. Jacobs, D. Penner, and J. M. Tiedje. 1978. . Absence of plant uptake and translocation of polybrominated biphenyls (PBBs). Environ. Health Perspectives 23:9-12. . 4. Food and Drug Administration. 1980. Code of Federal regulations. CFR 109.15, 109.30. , . ; 5. Flies, G- F-. and G. S. Marrow. 1981. Chlorobiphenyl movement . from soil to soybean plants. J. Agric. Food Chem. 29:757-759. 6. Frink, C. R., B. L. Sawhney, K. P. Kulp, and C. G._Fredette. 1982. Polychlorinated biphenyls in Housalonic River sediments in ' Massachusetts and Connecticut: Determination, distribution, and transport. Bull. 800, The Conn. Agr. Exp. Sin., New Haven, CT. 7. Hankin, L., and B. L. Sawhney. 1983. Microbial degradation of PCBs in soil. Soil Sci. (in press). . 8. Hutzinger, O., S. Safe, and V. Zitko. 1977. The chemistry of PCBs. CRC Press, Inc., Boca Raton, FL. 9. Iwata, Y., F. A. Gunther, and W. E. Westlake. 1974. Uptake of a PCB (Aroclor 1254) from soil by carrots under field condi tions. Bull. Environ. Contam. Toxicol. 11:523-528. 10. Iwata, Y., and F. A. Gunther. 1976. Translocation of the polychlorinated biphenyl Aroclor 1254 from soil into carrots under field conditions. Arch. Environ. Contam. Toxicol. 4:44-59. 11. Jacobs, L. W., S. F. Chou, and J. M. Tiedje. 1976. Fate of polyb- rominated biphenyls (PBB's) in soils. Persistence and plant uptake. J. Agric. Food Chem. 24:1198-1201. ' TABLE 2. PCBs (A roclors) in soil and in vegetables grown in soil amended with contaminated sediment during 1981. Aroclor Soil . Beet roots Beet leaves Turnip roots Turnip leaves pg/ke pg/kg BP RBP P-gAg BF RBF P-gAg BF RBF PgAg BF RBF 1248 80 15 1254 1,880 16 1260 14,440 35 .187 94 .008 4 .002 1 22 .275 69 94 .050 12 52 .004 1 30 .375 188 32 .400 200 . 16 .008 4 40 .021 11 20 .002 1 27 .002 1 Total 16.400 66 168 66 99 BF is bioaccumulation factor calculated by dividing the amount (pgAg) of an Aroclor in the plant part by its amount in the soil. RBF is the ratio of Aroclor 1248 or 1254 compared to 1260. TABLE 3. PCBs (\sg:'kg) in vegetables grown in amended soil during 1982. Turnips Beans Leaves Roots Aroclor Harvest date (1982) 7/31 8/4 8/12 Unpeeled Peeled Leaves Stems Pods Seeds 1248 ' 27 31 20 32 3 44 37 44 13 1254 59 49 91 61 22 40 0 22 4 1260 52 79 156 204 10 107 36 98 0 JOURNAL OF FOOD PROTECTION. VOL. 47. MARCH 1984 PCB-ARCH-EXT0378334 l236 SAWHNEY AND HANKIN' 12. Lichtenstein, E. P., G. R. Myrdal, and K. R. Schulz. 1965. Absorption of insecticidal residues from contaminated soils into five carrot var ieties. J. Agric. Food Chem .13:126-131. 13. Moza, P. N., 1. Scheunert, W. Klein, and F. Forte. 1979. Long term uptake of lower chlorinated biphenyls and their conversion products by spruce trees (Picea abies) from soil treated with sew age sludge. Chemosphere 6:373-375. . r 14. Nakanishi, H., S..Nakamura, andM. Tsutsumi. 1977. Translocation of polychlorinated biphenyl (PCB) in rice plant. Chem. Abst. 91:134. 15. Sawhney, B. L., C. R. Frink, and W. Glowa. 1981. PCBs in the , Housatonic River Determination and distribution. J. Environ. Qua!. 10:444-448. . .. , 16. Strek, H. J., J. B. Weber, P. J. Shea,E. Mrozek, Jr., andM. R. Over- . cash. 1981. Reduction of polychlorinated biphenyl toxicity and uptake * of carbon-14 activity by plants through the use activated carbon.J. Agric. Food Cnem. 29:288-293. 17. Suzuki. M.. N. Aizawa, G. Okano, and T. Taizrashi. 1977. Translo- . cation of polychlorobiphenyls in soil into plants: A study by a method of culture of soybean sprouts. Arch. Environ. Comm. Toxicol. 5:343 352. " . 18. Trotter, W. J. 1975. Removing the interference of DDT and itsanalogs in the analysis for residues of polychlorinated biphenyls. J. Assoc. Off. - Anal. Chem. 58:461-473. 19. U.S. Environmental Protection Agency. 1979. Guidelines establishing test procedures for the analysis of pollutants; proposed regulations. Fed. Reg. 44:69464-69574. . 20. Weber, J. B., and E. Mrozek, Jr. 1979. Polychlorinated biphenyls: Phytoioxiciry, absorption and translocation by plants, and inactivation by activated carbon. Bull. Environ. Contain. Toxicol. 23:412-417. JOURNAL OF FOOD PROTECTION. VOL. 47. MARCH 1984 PCB-ARCH-EXT0378335