Estrogen occurrence, transport, and biological effects resulting from wastewater reuse in irrigation and aquaculture

Open Access
Asem-hiablie, Senorpe
Graduate Program:
Agricultural and Biological Engineering
Doctor of Philosophy
Document Type:
Date of Defense:
November 01, 2013
Committee Members:
  • Herschel Adams Elliott, Dissertation Advisor/Co-Advisor
  • Herschel Adams Elliott, Committee Chair/Co-Chair
  • John Earl Watson, Committee Member
  • Rachel Alice Brennan, Committee Member
  • Albert R Jarrett, Committee Member
  • Clinton D Church, Special Member
  • Estrone
  • Estradiol
  • Ethynylestradiol
  • Endocrine disrupting compound
  • Emerging contaminant
  • Effluent
  • Africa
  • Ghana
ABSTRACT Wastewater treatment plant effluents (WWTPEs) are a major environmental source of endocrine-disrupting chemicals (EDCs) which have the potential to adversely affect the functioning of hormone systems in humans and wildlife. Most WWTPEs are directly discharged into surface waters where EDCs have been shown to influence reproduction and development of fish and other aquatic organisms. While beneficial reuse of effluents avoids direct discharge and ensuing effects on surface aquatic ecosystems, potential impacts on soils, crops, wildlife, groundwater, and human receptors are possible. Thus, it is important to understand the behavior, fate, and transport of EDCs in various wastewater reuse scenarios. The objective of this research was to investigate the behavior and potential risks associated with hormones (specifically, estrone (E1), 17β-estradiol (E2), and 17α-ethynlestradiol (EE2)), a ubiquitous and important class of EDCs, in three wastewater reuse scenarios: (i) spray irrigation of wastewater effluent for groundwater recharge, (ii) wastewater-fed aquaculture, and (iii) wastewater-irrigated vegetable production. The extent to which wastewater E1, E2, and EE2 applied at the Penn State University Living Filter site via effluent irrigation moved downward in the soil profile was investigated. Patterns of estrogen occurrence were first established by analyzing WWTPE samples (n = 269) for 12 months under different flow and seasonal conditions. The order of frequency of occurrence based on percentage of sample values above the limit of quantification (LOQ) was: E1 (60%) > E2 (34%) > EE2 (1%). Notably, E1 high-flow concentrations were statistically higher (p = 0.012) compared to low-flow, but no clear patterns were seen for E2 occurrence. The concentration medians (ranges) observed during the high-flow sampling times were E1 [6.1 (<LOQ – 17.0 ng L-1)] and E2 [<LOQ (<LOQ – 37.7 ng L-1)]. During low flows, all medians were <LOQ and ranges were E1 (<LOQ – 5.6 ng L-1), E2 (<LOQ – 37.4 ng L-1) and EE2 (<LOQ – 3.6 ng L-1). The EE2 levels were mostly <LOQ during both high and low flow. Diurnal patterns generally showed peak effluent E1 and E2 concentrations during morning sampling collections capturing peak evening flow of a student-dominated population. Observed variations in E1 occurrence were attributed to differences in the makeup of the service population during different flow regimes. After baseline estrogen concentrations were established, effluent spiked with 100 µg L-1 E1, E2, and EE2 and 6.7 mg L-1 Br- (inert tracer) was applied at 5 – 10 cm wk-1 for 6 months to undisturbed column lysimeters (60 x 60 x 60 cm) sampled from two soil types: Hagerstown (silt loam) and Morrison (sandy loam). By design, bypass flow along wall edges was separated from flow within the soil matrix and most (> 85%) of applied liquid bypassed the inner soil matrix. Inverse modeling of transport parameters by the CXTFIT model suggested that although the fractions of mobile water content were small (β = 0.37 ± 0.120 and 0.06 ± 0.023 for Br- in Hagerstown and Morrison soils, respectively) it appeared to be a major influence in the leaching of the estrogens. One Morrison soil lysimeter appeared to have one or more continuous macropores from top to bottom; the Br- tracer emerged at C/Co ≥ 1 at only 0.02 pore volumes (PV), and within 0.04 PV, the C/Co for estrogens measured as high as 0.91 (E1), 0.23 (E2), and 0.38 (EE2). At three peri-urban sites in Ghana (West Africa), the effects of wastewater-borne estrogens on growth and reproduction of cultured fish were assessed. African catfish (Clarias gariepinus) raised in a wastewater stabilization pond (WSP) of a functioning municipal wastewater treatment plant, a wastewater polishing holding pond (WWP) of a dysfunctional treatment plant, and a reference pond (RP) unimpacted by wastewater were studied. Pond water estrogenicity (E2Eq) assayed by E-SCREEN and E2 concentrations followed the trend WWP > WSP > RP and estrogen levels in wastewater ponds were comparable to other reports for effluents worldwide. Fish serum estrogenicity assayed by E-SCREEN showed significantly higher concentrations in female vs. male catfish in the RP and WSP but not in the WWP (α = 0.05). Histological examination of liver and gonad tissue showed no apparent signs of intersex or pathology. The similarities in various measures of body indices between fish of this study and African catfish from freshwater systems suggest that aquaculture may be a suitable reuse option for treated municipal wastewater in regards to estrogenic effects. Plant uptake of environmental E1, E2, and EE2 as a result of wastewater irrigation were studied by evaluating the occurrence of estrogens in irrigation water, vegetables, and soils from three study sites in Ghana where raw wastewater (site RWW), partially treated wastewater (site PTWW), or impounded drinking water (reference site IDW) were used to irrigate vegetables in peri-urban agriculture. Samples of irrigation waters and vegetables [spring onions (Allium wakegi), green bell pepper (Capsicum annuum), and lettuce (Lactuca sativa)] were collected weekly for six weeks from the three sites. Soils were also collected and tested. Estrone concentrations in irrigation water were not found to be significantly different (α = 0.05) with median values as follows: RWW (5.5 ng L-1) > PTWW (3.6 ng L-1) > IDW (<LOQ). The E2 occurrence in water at the sites were statistically different with median concentrations at PTWW being 2.0 ng L-1 while both IDW and RWW were <LOQ. The median EE2 concentration at site RWW was 15.1 ng L-1 (comparable only to upper limits reported in wastewater treatment plant influent by a few other studies) while both IDW and PTWW were <LOQ. The higher than average concentration of EE2 at site RWW suggest high use of oral contraceptives in the service population. No estrogens were detected in soils from the study sites. Results of estrogen concentrations in plant tissue were limited and levels in all vegetables from all sites were mostly below the LOQ of 0.1 ng g-1. Lettuce showed the highest estrogen concentrations but these levels may be due to foliar deposition during wastewater application rather than direct uptake and translocation in plant tissue. At site RWW, lettuce E1, E2, and EE2 concentrations of up to 1430.4, 28.2, and 4.3 ng g-1 (dry weight), respectively, and 53.4 ng g-1 E1 in spring onions were recorded. Estimated human dietary intake of EE2 (18 µg d-1) based on the highest observed estrogen levels in lettuce were found to be comparable to therapeutic doses in oral contraceptives (10 – 50 µg d-1). Results indicated that although E1 and EE2 concentrations comparable to those of previous studies were detected in irrigated wastewater, these levels were not reflected in plant tissue estrogen levels most of the time or in soils. Based on the estrogen attenuation mechanisms in soils (sorption and microbial degradation), and uptake and effects in biota (plant and fish) in the scenarios studied, spray irrigation of treated wastewater effluent for groundwater recharge, wastewater-fed aquaculture, and wastewater-irrigated vegetable production may be viable reuse options for mitigating the impacts of wastewater-borne estrogens. It is recommended that fate and transport studies of wastewater-borne hormones recognize and account for the high variability in effluent concentrations arising from seasonal and service population changes. Secondly, studies and assessments of leached compounds at effluent irrigation sites should recognize macropore flow as an important transport mechanism. Finally, attention should be given to human risks of exposure to endocrine disrupting compounds as a result of foliar deposition on irrigated vegetables consumed raw and potential bioaccumulation in wastewater-raised fish.