Pharmaceutical and Trace Metal Interaction within the Water-Soil-Plant Continuum: Implications for Human and Soil Health

Abstract

Unplanned water reuse for crop irrigation may pose a global health risk due to the entry of contaminants into the food chain, undesirable effects on crop quality, and impact on soil health. In this study, we evaluate the impact derived from the co-occurrence of pharmaceuticals (Phs), trace metals (TMs), and one metalloid within the water-soil-plant continuum through bioassay experiments with Lactuca sativa L. Results indicate that the co-occurrence of Phs and TMs has synergistic or antagonistic effects, depending on target contaminants and environmental compartments. Complex formations between drugs and TMs may be responsible for enhanced sorption onto the soil of several Phs and TMs. Concerning plant uptake, the co-occurrence of Phs and TMs exerts antagonistic and synergistic effects on carbamazepine and diazepam, respectively. With the exception of Cd, drugs exert an antagonistic effect on TMs, negatively affecting their uptake and translocation. Drug contents in lettuce edible parts do not pose any threat to human health, but Cd levels exceed the maximum limits set for leafy vegetable foodstuffs. Under Ph-TM conditions, lettuce biomass decreases, and a nutrient imbalance is observed. Soil enzyme activity is stimulated under Ph-TM conditions (β-galactosidase) and Ph and Ph-TM conditions (urease and arylsulfatase), or it is not affected (phosphatase).

Keywords: drug–metal complexes; human health risk assessment; interaction; interstitial water; lettuce; pharmaceuticals; soil; soil health; trace metals; transformation products.

Figure 1

Pharmaceutical (a) and transformation product (b) concentrations in the interstitial water from Ph and Ph−TM conditions over the 45-day irrigation period. The boxplots show the lower quartile, the median, and the upper quartile, with whiskers extending to the most extreme data point. Compounds are represented in order of decreasing concentrations.

Figure 2

Temporal trends of pharmaceutical (a) and transformation product (b) concentrations in interstitial water from Ph and Ph-TM conditions over the 45-day irrigation period. Compounds appear in order of decreasing concentrations.

Figure 3

Total average soil contents of pharmaceuticals (a) and transformation products (b) (dry weight) from Ph and Ph-TM conditions after the 45-day irrigation period. Error bars are standard deviation. For comparative purposes, compounds appear in order of decreasing concentrations in interstitial water. Differences between Ph and Ph-TM conditions were calculated by a Student’s t-test. * indicates significant differences at p < 0.05. In the case where there are no significant differences, nothing is indicated.

Figure 4

Total average amount of pharmaceuticals (a) and transformation products (b) in external leaves, internal leaves, and roots of lettuce plants grown in Ph and Ph-TM conditions after the 45-day irrigation period. Error bars are standard deviation. The absence of bars in external leaves of METRO and internal leaves of OVEN is due to only one replica being >LOQ. For comparative purposes, compounds appear in order of decreasing concentrations in the interstitial water. Different letters indicate significant differences among tissues for each condition at p < 0.05 after one-way analysis of variance. The amount of some compounds was lower than the LOQ in the internal leaves (NIC and OVEN) or in the roots (FAA); thus, significant differences for each condition were calculated by a Student’s t-test. Differences between Ph and Ph-TM conditions for each tissue were also calculated by a Student’s t-test. * and ** indicate significant differences at p < 0.05 and p < 0.01, for DIA and CBZ, respectively. In cases where there are no significant differences, nothing is indicated.

Figure 5

Trace metal and metalloid concentrations (a) and their temporal trends (b) in the interstitial water from C, TM, Ph, and Ph-TM conditions over the 45-day irrigation period. The boxplots show the lower quartile, the median, and the upper quartile, with whiskers extending to the most extreme data points. Trace metals and metalloid appear in order of decreasing concentration. Different letters indicate significant differences among conditions for each TM at p < 0.05 after one-way analysis of variance.

Figure 6

Total average content of trace metals and metalloid (dry weight) in soils from C, TM, Ph, and Ph-TM conditions after the 45-day irrigation period. Error bars are standard deviation. For comparative purposes, TMs appear in order of decreasing concentrations in the interstitial water. Different letters indicate significant differences among conditions at p < 0.05 after one-way analysis of variance. In cases where there are no significant differences, nothing is indicated.

Figure 7

Total average amount of trace metals and metalloid in external leaves, internal leaves, and roots of lettuce plants grown in C, TM, Ph, and Ph-TM conditions after the 45-day irrigation. Error bars are standard deviation. For comparative purposes, trace metals and metalloid appear in order of decreasing concentrations in the interstitial water. Different letters indicate significant differences, among conditions for each tissue (uppercase) or among tissues for each condition (lowercase), at p < 0.05 after one-way analysis of variance. The amount of As in internal leaves was lower than the LOQ; thus, significant differences between external leaves and roots for each condition were calculated by a Student’s t-test. *** indicates significant differences at p < 0.001.

Figure 8

External leaf, internal leaf, and root biomass (dry weight) and total average amount of major elements in external leaves, internal leaves, and roots of lettuce plants grown in C, TM, Ph, and Ph-TM conditions after the 45-day irrigation. Error bars are standard deviation. Different letters indicate significant differences, among conditions for each tissue (uppercase) or among tissues for each condition (lowercase), at p < 0.05 after one-way analysis of variance.

Figure 9

β-Galactosidase (BGAL), urease (URE), aryl sulfatase (ARYS), and phosphatase (PHOS) activity average values in soils from C, TM, Ph, and Ph-TM conditions after the 45-day irrigation. Error bars are standard deviation. Different letters indicate significant differences among conditions at p < 0.05 after one-way analysis of variance.