Effects of Climate and Sewer Condition on Virus Transport to

Subscriber access provided by Northern Illinois University

Article

Effects of Climate and Sewer Condition on Virus Transport to Groundwater Madeline B. Gotkowitz, Kenneth R Bradbury, Mark A. Borchardt, Jun Zhu, and Susan K. Spencer Environ. Sci. Technol., Just Accepted Manuscript • DOI: 10.1021/acs.est.6b01422 • Publication Date (Web): 19 Jul 2016 Downloaded from http://pubs.acs.org on July 31, 2016

Just Accepted “Just Accepted” manuscripts have been peer-reviewed and accepted for publication. They are posted online prior to technical editing, formatting for publication and author proofing. The American Chemical Society provides “Just Accepted” as a free service to the research community to expedite the dissemination of scientific material as soon as possible after acceptance. “Just Accepted” manuscripts appear in full in PDF format accompanied by an HTML abstract. “Just Accepted” manuscripts have been fully peer reviewed, but should not be considered the official version of record. They are accessible to all readers and citable by the Digital Object Identifier (DOI®). “Just Accepted” is an optional service offered to authors. Therefore, the “Just Accepted” Web site may not include all articles that will be published in the journal. After a manuscript is technically edited and formatted, it will be removed from the “Just Accepted” Web site and published as an ASAP article. Note that technical editing may introduce minor changes to the manuscript text and/or graphics which could affect content, and all legal disclaimers and ethical guidelines that apply to the journal pertain. ACS cannot be held responsible for errors or consequences arising from the use of information contained in these “Just Accepted” manuscripts.

Environmental Science & Technology is published by the American Chemical Society. 1155 Sixteenth Street N.W., Washington, DC 20036 Published by American Chemical Society. Copyright © American Chemical Society. However, no copyright claim is made to original U.S. Government works, or works produced by employees of any Commonwealth realm Crown government in the course of their duties.

Page 1 of 25

Environmental Science & Technology

Effects of Climate and Sewer Condition on Virus Transport to Groundwater Madeline B. Gotkowitz* Wisconsin Geological and Natural History Survey, University of Wisconsin−Extension 3817 Mineral Point Road, Madison, Wisconsin 53705 [email protected] phone: (608) 262-1580 fax: (608) 262-8086 Kenneth R. Bradbury Wisconsin Geological and Natural History Survey, University of Wisconsin−Extension 3817 Mineral Point Road, Madison, Wisconsin 53705 Mark A. Borchardt USDA-Agricultural Research Service 2615 Yellowstone Drive, Marshfield, WI 54449 Jun Zhu Department of Statistics and Department of Entomology, University of Wisconsin−Madison 1300 University Avenue, Madison, Wisconsin 53706 Susan K. Spencer USDA-Agricultural Research Service 2615 Yellowstone Drive, Marshfield, WI 54449

1 Gotkowitz et al.

ACS Paragon Plus Environment


Page 2 of 25

Abstract Pathogen contamination from leaky sanitary sewers poses a threat to groundwater quality in urban areas, yet the spatial and temporal dimensions of this contamination are not well understood. In this study, 16 monitoring wells and six municipal wells were repeatedly sampled for human enteric viruses. Viruses were detected infrequently, in 17 of 455 samples, compared to previous sampling at these wells. Thirteen of the 22 wells sampled were virus-positive at least once. While the highest virus concentrations occurred in shallower wells, shallow and deep wells were virus-positive at similar rates. Virus presence in groundwater was temporally coincident, with 16 of 17 virus-positive samples collected in a six-month period. Detections were associated with precipitation and occurred infrequently during a prolonged drought. The study purposely included sites with sewers of differing age and material. The rates of virus detections in groundwater were similar at all study sites during this study. However, a relationship between sewer age and virus detections emerged when compared to data from an earlier study, conducted during high precipitation conditions. Taken together, these data indicate that sewer condition and climate affect urban groundwater contamination by human enteric viruses. Introduction Water-supply wells and sanitary sewers are common in cities and villages, and exfiltration (outward leakage) from sewer pipes threatens groundwater quality in these areas. Sewers are a widely recognized, significant source of fecal contamination to the subsurface.1-2 Contamination of shallow groundwater by sewage is common.3 Sewage exfiltration can impair groundwater quality supplied from wells and can affect water quality within subsurface distribution systems.4,5 The rate and location of exfiltration varies over time, complicating attempts to directly measure or repair leaks.6

2 Gotkowitz et al.


Page 3 of 25


Sewage exfiltration is of particular concern in communities that rely on groundwater supply; fecal pathogens cause acute water-borne disease and have low infectious doses, on the order of 100 to 102.7 Neither the federal Safe Drinking Water Act or Groundwater Rule requires disinfection of groundwater used at public water systems. Approximately 70 million people in the US are served groundwater that is untreated or with treatment insufficient to remove 99.99 percent of viruses.8 Poor water quality at these systems accounts for about 30 percent of the water-borne disease outbreaks in the U. S. and may account for as much as 8 to 30 percent of endemic acute gastrointestinal illness experienced in these communities.9-11 Waterborne disease outbreaks are associated with high rainfall events.12-14 Recent studies indicate that this association extends specifically to drinking water from an untreated groundwater source.9,15 Viral pathogens can contaminate groundwater and wells in confined and unconfined aquifers.16-17 Several studies report virus occurrence rates of about 30 percent of groundwater samples.18,19 Virus transport in groundwater is associated with a high degree of temporal variability, which is often attributed to absorption, filtration, and climatic conditions.20 During sampling conducted in 2008 and 2009, our research group repeatedly detected viruses in six municipal wells with an overall detection rate of 46 percent (n = 147).21 Viruses in groundwater were correlated with their concentrations in wastewater and with groundwater recharge events. Bradbury et al.21 suggested that exfiltration from sanitary sewers are the most likely source of human enteric viruses to this groundwater system, and leakage from sewers during heavy precipitation enhanced virus transport. The work reported here builds on previous sampling from deep municipal wells by investigating the temporal and spatial distribution of viruses in shallow groundwater, between municipal wells and the presumed virus source (sanitary sewers). The study design included repeated sampling for one year for human-specific viruses and indicator bacteria from a network of 22 wells at 3 Gotkowitz et al.



Page 4 of 25

seven sites. Sites included sewers with a variety of ages and material, allowing evaluation of the impact of sewer conditions on virus occurrence in groundwater. In contrast to heavy precipitation throughout the previous, 2008 study,21 a portion of this project (the “2012 study") coincided with severe drought conditions. Taken together, these studies provide data to evaluate the hypothesis that local climatic conditions contribute to the episodic nature of pathogen presence in groundwater. Understanding conditions that promote virus transport from sewers to the water table aids in protecting groundwater quality near supply wells and in assessing human health risks related to untreated source water. Experimental Section Groundwater system The neighboring cities of Madison and Fitchburg, Wisconsin (Figure 1) rely on 28 deep groundwater wells to meet an annual public water supply demand of about 42.4 x 106 m3. The region is underlain by approximately 250 m of sedimentary geologic formations, including a confined lower bedrock aquifer separated from the upper, unconfined aquifer by a thin aquitard (Figure 2). The water table occurs in glacial deposits (sand, gravel or fine-grained till) across much of the region; in upland areas, the water table is within the Tunnel City Formation. Crystalline Precambrian rock forms the base of the groundwater system. Vertical hydraulic gradients are generally downward from the water table across the Eau Claire aquitard due to extensive pumping. Two types of well construction are common in the region. “Lower aquifer” wells refer to those cased through the upper aquifer and the Eau Claire aquitard and are open to the confined Mount Simon Formation (Figure 2). “Multiaquifer” wells have a similar total depth but casings that extend only into the upper aquifer. Multiaquifer wells hydraulically connect the upper and lower aquifers.

4 Gotkowitz et al.


Page 5 of 25


Infectious human enteric viruses have been detected in both types of wells. Fractures in the sandstone formations may facilitate rapid transport of pathogens through the groundwater system.22 Sanitary sewers and site development The first sanitary sewers were installed in the study area in 1899, and the system now includes more than 2,100 km of gravity-drained mains and laterals (Figure 1). A regional sewer collection system, including gravity and pressurized mains, directs all wastewater to a single treatment plant. Separate storm water collection systems route runoff to area lakes. The study communities provided records of sewer age and material. The sewer pipe density at each site was calculated by summing the length of mains and laterals within a capture zone delineated for the municipal well at each site, then dividing total pipe length by the area of the capture zone (Table 1). Capture zones were simulated with a 1-year time of travel particle tracking method applied to a three dimensional groundwater flow model developed for this region. 23 The sites selected for this study include a range of sewer characteristics and municipal well design (Table 1). Five sites are in neighborhoods developed prior to 1970 and have older sewers, constructed with vitrified clay pipe. The other two sites, FB Well 11 and Well 30, are located in newer developments with PVC plastic sewer pipe. Municipal records indicate that major sewer repairs near the sites is limited to Well 7, where approximately 4% (85 m) of vitrified clay pipe was replaced in 2001 and an additional 4% of pipe was relined during the 2008 study. Four of the seven sites include confined municipal wells completed in the lower aquifer. Two sites have multiaquifer municipal wells, open to the upper and lower aquifers. The Lake Edge site provides a sampling location over 1 km distant from an active municipal well. Five of the six municipal wells were sampled previously in our 2008 study and were virus-positive on multiple

5 Gotkowitz et al.



Page 6 of 25

occasions.21 The water utility increased disinfection levels in light of study results, but there were no changes in practice that affected the subsurface at wells or pump houses during the 2008 and 2012 projects. Monitoring wells were sited close to sewer networks to provide samples from shallow groundwater relative to the depth of municipal wells (Figure 2). Borehole geophysical logs collected in drillholes at each site were used to identify fractured intervals or dissolution openings that might provide preferential transport pathways. This characterization informed selection of screen depth in monitoring wells. SI Section 1 shows well configuration at each site. Overall, the study included 16 monitoring wells and six municipal wells. Table 1. Site sewer and well characteristics Site name

Well type

Well construction year

Well depth (m)

Casing depth (m)

Number of monitoring wells

Sewer material

Sewer construction year

Sanitary sewer pipe, m

Capture zone 2 area, m

Pipe density, 2 m/m

Well 11

MAW

1959

229

34

2

Clay

1956

3,207

179,920

1.80E-02

Well 13

MAW

1959

238

39

2

Clay

1958-1969

6,683

405,607

1.60E-02

Well 19

LA

1970

219

79

2

Clay

1960

732

159,648

4.60E-03

Well 30

LA

2003

224

95

2

Plastic

1996

1,497

188,771

7.90E-03

Well 7

LA

1939

224

73

3

Clay

1939-1946

2,172

99,807

2.20E-02

FB Well 11

LA

2007

305

123

2

Plastic

2003

220

43,468

5.10E-03

Lake Edge

NA

NA

NA

NA

3

Clay

1952

574

30,324

1.90E-02

MAW multi aquifer well; LA lower aquifer well; NA not applicable; “FB Well 11” denotes the site in the City of Fitchburg; Lake Edge site does not include a municipal well

Groundwater Sampling Program Monitoring wells were sampled for viruses and indicator bacteria approximately every two weeks between June 2012 and May 2013, with a total of 24 sampling events at each site. A 4-L sample of clarified and settled influent (72-hour composite) (i.e., primary effluent) was collected at the 6 Gotkowitz et al.


Page 7 of 25


same schedule from the wastewater treatment plant. The six municipal wells were sampled monthly over this period. The municipal well and monitoring wells at each site were sampled on the same day. Sampling procedures differed slightly at monitoring wells and municipal wells. Monitoring wells were sampled with stainless steel submersible pumps after purging a minimum of five well volumes and obtaining stable pH, specific conductance and temperature measurements. Municipal wells were sampled while the high-capacity pumps were running, from a tap located at the well head, prior to any treatment. At both types of wells, glass wool filters were used to concentrate viruses from groundwater samples in the field.24,25 Samples were collected at a rate of approximately 5 L per minute, with an average sample volume of 920 L and a range of 814 – 1,117 L. At wells where groundwater pH exceeded 7.5, 1 M HCl was injected prior to filtration to obtain a pH between 6.5 and 7.0. Samples for total coliforms and Escherichia coli were collected aseptically in 100 mL sterile bottles. Equipment field blanks were collected quarterly by pumping 11 liters of sterilized, deionized water through a glass wool filter using decontaminated field equipment. All four blanks were negative for viruses, suggesting field and equipment-related procedures did not lead to sample contamination. Decontamination of field equipment is described in SI Section 1. Glass wool filters, sewage samples, and coliform samples were placed on ice and processed within 24 to 48 hours. Coliform and E.coli were evaluated with the Colilert® Quanti-Tray test (IDEXX Laboratories, Westbrook, ME) and expressed as MPN per 100 ml. Glass wool filters were eluted with beef extract/glycine and the eluate flocculated and concentrated with polyethylene glycol.11 Sewage samples were concentrated using the same secondary concentration procedure as for the filter eluates. Concentrated samples of the filters and sewage were stored at −80 °C until analysis.

7 Gotkowitz et al.



Page 8 of 25

Samples were analyzed for seven human viruses: adenovirus A; adenovirus B; adenoviruses C D, and F; enterovirus; norovirus genogroup I; norovirus genogroup II, and human polyomavirus (HPyV). Viruses were detected by real-time quantitative PCR (qPCR) or reverse-transcription qPCR (RT-qPCR). Assays were quantitative and in duplicate, using the LightCycler 480 (Roche Diagnostics, Mannheim, Germany) and hydrolysis probes. Borchardt et al.11 describe the qPCR and RT reaction conditions and calculations for virus concentrations. Primers, probes, standard curve parameters, and recovery controls are reported in SI Section 1. All samples were analyzed for RT and PCR inhibition following methods described in Gibson et al.26 No-template controls were performed for every batch of extractions, RT reactions, and PCR. All no-template controls were negative (i.e., no Cq value) throughout the study. Samples were not evaluated for virus infectivity. Data analysis Graphical and non-parametric techniques were used to evaluate the presence of viruses in groundwater and potential relationships with well characteristics, biological constituents, and inorganic indicators of groundwater quality. The nonparametric Kruskal-Wallis test was used to compare data of differing sample size. These highly censored data were ranked by assigning a value of zero to samples below detection limits. Virus concentrations were summed for samples positive for more than one virus type. Sample results were aggregated in two-week intervals, because this was the typical amount of time required for a round of sampling. Inclement weather resulted in only four wells sampled during a two-week period in late December, 2012. Relationships between virus occurrence in groundwater and several variables were assessed by applying linear regression analysis. Wastewater virus concentrations were examined for trends over time and their relationship to the presence of viruses in groundwater. The rate of virus detections at the study sites were compared to the age and density of near-by sanitary sewer systems. Temporal 8 Gotkowitz et al.


Page 9 of 25


relationships between viruses in groundwater and several hydrologic conditions were evaluated. The response variable was the log concentration of total virus concentration in a groundwater sample and the predictor variables were depth to the water table, daily precipitation, and clear-water inflow to sewers on the same day as sample collection and from one to seven days previous. Infiltration and inflow of clear-water to the sewer system was calculated by subtracting the average dry-weather sanitary flow from the daily flow volume record. Cumulative precipitation and cumulative inflow to sewers from two and up to seven days previous were also used as predictor variables. Results and Discussion Virus occurrence in wells and sewage Groundwater was positive for viruses in 17 of 455, or 3.7 percent of the samples collected, and concentrations ranged from non-detectable to 12.7 gc/L (Figure 3). The mean concentration of viruspositive samples was 1.6 gc/L, with a median of 0.9 gc/L. Although the overall virus detection rate was low, repeated sampling over time demonstrated that most of the wells are susceptible to virus contamination. Of the 16 monitoring wells in the study, 11 (69 percent) were virus-positive at least once. Two of the six municipal wells were virus-positive during this study, but the four wells with no virus detections were virus-positive during the 2008 study (see Table S4, SI section 2). Samples from the seven study sites exhibit a coincidence in the timing of virus presence, and in the timing of highest concentrations. With the exception of one sample collected in June 2012, virus occurrence was limited to the months of September through February; the five highest concentrations occurred in January and February. Virus detection data from all wells are presented in SI Section 2. Five of the seven viruses enumerated in this study were detected in at least one groundwater sample. Adenovirus B and norovirus GI were never detected in groundwater (Table 2). Wastewater

9 Gotkowitz et al.



Page 10 of 25

samples were positive for all enumerated viruses on multiple occasions, however adenovirus B, norovirus GI, and enterovirus were less frequent. Wastewater contained high concentrations of viruses, ranging from 2.4 x 105 to 3.2 x 106 gc/L, with a mean of 1.2 x 106. The sum of the seven enumerated virus concentrations in wastewater decreased over time during the present study (linear regression, p-value < 0.001) (Figure 4). When considered separately, not every virus type decreased over time (SI Section 5). Inflow and infiltration to the sanitary sewers increased from February, 2013 through the end of the study (Figure 4), generally coincident with the decrease in total virus concentration in wastewater. The decrease in virus concentration in wastewater could be attributed to lower infection rates in the population during early 2013, or to dilution of wastewater during periods of high inflow and infiltration (groundwater or surface water) into sewers. Although low virus concentrations in sewer exfiltration may contribute to the lack of virus-positive wells in March through May, 2013, there was no statistically significant relationship identified in the rate of groundwater virus detections as a function of virus concentration in wastewater (statistical analysis presented in SI Section 5). Table 2. Groundwater and wastewater samples positive for viruses Virus Groundwater Wastewater detections detections N = 455 N =24 Adenovirus A 6 20 Adenovirus B 0 9 Adenovirus C, D, and F 5 23 Enterovirus 1 17 Norovirus GI 0 17 Norovirus GII 5 23 Human polyomavirus 2 24

Bacterial indicators Groundwater samples were tested for total coliform bacteria to investigate potential correlations between indicator bacteria and the presence of human-specific viruses. Total coliform 10 Gotkowitz et al.


Page 11 of 25


detections were more frequent in shallow wells compared to deeper wells, with 31 percent (119 of 383) of monitoring well samples and 3 percent (2 of 71) of municipal well samples coliform-positive. Monitoring wells were not disinfected following construction, and contamination could have occurred through soil transferred by drilling equipment. A Spearman’s rank correlation test was applied to paired samples for indicator bacteria and enteric viruses. There was not a significant correlation between the two (rs = -0.02, n = 454, p = 0.61). One of the coliform-positive samples (collected August 16, 2012 from monitoring well MW19D) was also positive for E. coli., but the well was not virus-positive on this date. The lack of correlation is not surprising because the viruses enumerated in this study are human-specific, and their presence indicates human fecal contamination. Coliform bacteria are common in soil and surface water, but their presence does not necessitate a fecal source.27 SI Section 3 contains examination of the coliform data with respect to well depth, soil temperature, and virus occurrence. Relationships between virus occurrence, wells, and sewers Data from each of the seven study sites were examined for relationships between pathogen susceptibility and the characteristics of wells and sewers. Monitoring wells and municipal wells were virus positive at similar rates: 3.9 % (15 of 384) at monitoring wells and 2.8 % (2 of 71) at municipal wells. Although there was no association between well depth and detection frequency, there is weak evidence that virus concentrations were higher in shallow wells than in deeper wells (p = 0.07). These data are illustrated in SI Section 5. Virus occurrence was examined in relation to the age and density of near-by sanitary sewers. Sewer material (clay or plastic pipe) was not explicitly evaluated because it is closely tied to sewer age (see Table 1). The rate of virus detections at the seven sites ranged from about 3 to 5 percent (Table 3),

11 Gotkowitz et al.



Page 12 of 25

with no evidence of difference between the sites (χ 2 = 12.6, p-value = 0.99). Regression analyses (SI, Section 5) indicate no difference in virus occurrence at sites based on the age of the sewer systems or the density of sewer pipe (p-value = 0.32 and 0.57, respectively). This result was surprising, because sites with a greater density of sewers and older sewers are intuitively prone to more sewage exfiltration compared to sites with a smaller quantity of newer sewers. Although some monitoring wells had elevated concentrations of wastewater indicators, including chloride, nitrate and specific conductance, these wells did not have higher rates of virus detections than other wells. SI Section 4 presents this additional water quality data and analysis of sewer conditions. Table 3. Virus occurrence in groundwater seven sites

Site

Positive samples / total samples

Virus positive rate, percent

Lake Edge 11 13 19 30 7 FB11

2 / 72 2 / 60 3 / 59 2 / 60 2 / 60 3 / 84 3 / 84

2.8 3.3 5.1 3.3 3.3 3.6 5.0

Sanitary sewer density m/m2 1.9E-2 1.8E-2 1.6E-2 5.0E-3 8.0E-3 2.2E-2 5.0E-3

Relationships between virus occurrence and hydrologic conditions in 2008 and 2012 The coincidence in timing of virus detections at the study wells (Figure 3) supports a conclusion of the 2008 study, that a regional driver, common across the seven sites, promotes leakage and transport of enteric viruses in the subsurface.21 Figure 4 illustrates virus occurrence and hydrologic conditions prevalent during both studies. The high rate of virus-positive samples in 2008 occurred during a period of elevated sewer inflows and water table conditions, and large magnitude rainfall events. Regression analyses of the combined 2008 and 2012 data support the relationship

12 Gotkowitz et al.


Page 13 of 25


between virus detections and precipitation, with strong evidence that virus concentrations are associated with precipitation events on the day prior to sampling (p-value = 0.0001) and a weak association with precipitation occurring six days prior to sampling (p-value = 0.09). The relationship between sewer inflow and log concentration in groundwater revealed strong evidence of a positive association in 2008, but there is no evidence of this association in 2012. When the data are combined for the two studies, there is only weak evidence for a positive association, after accounting for the year effect. No significant relationship was found between virus presence in groundwater and depth to the water table. Viruses were infrequent in groundwater samples collected during drought conditions. The 2012 study began during a dry period, in June through mid-July. Concentrations of viruses in wastewater were high during this time, but only 1 of 54 groundwater samples collected from June through early September, 2012 were virus positive. There was little to no infiltration of clear water into the sewers during the drought (Figure 4). Although largely speculative, it is possible that the low volume of sewer inflow may have resulted in low rates of sewage exfiltration. With little to no infiltrating precipitation, any sewer leakage would remain for a longer period of time in the vadose zone. Increased virus sorption and inactivation during unsaturated transport compared to saturated conditions is expected.28,29 Several mechanisms have been postulated to explain enhanced retention of colloids in the vadose zone, including increased sorption at the solid-water interface or inactivation at the air-water interface.30 Although not conclusive, exposure to higher soil temperatures during the drought could also have contributed to virus inactivation in the vadose zone.31 The virus-positive rate of groundwater samples increased to 7.5 percent (16 of 212) from mid-September, 2012 through February, 2013. This period coincided with recovery of the water table and some limited precipitation. Inflow to sanitary sewers remained low and wastewater concentrations 13 Gotkowitz et al.



Page 14 of 25

remained at similar levels to preceding months. The final six rounds of virus sampling occurred during a period of frequent precipitation, water table rise, and related episodes of high inflow to the sanitary sewer. However, there were no virus-positive samples during these months. Although the reason for this is not clear, soil temperatures appear elevated in April and May of 2013, and this might contribute to inactivation in the vadose zone and the lack of detections in groundwater. Comparison of hydrologic conditions during the 2012 study to those in 2008 suggests that the temporal variability in virus transport in this groundwater system results from short-term changes in climate. Infiltration into sewers was much less in 2012 than in 2008, and the depth to the water table was greater (Figure 4). If, as suggested by Bradbury et al.,21 high precipitation events promote increased sewer exfiltration, the source of viruses to the subsurface during the 2008 study would have been more steady over time compared to 2012. The surfeit of precipitation in the earlier study is striking; August 2007 rainfall in Madison totaled 38.56 cm, the wettest month since record keeping began in 1897.32 Storms in June 2008 included a 1-day rainfall of 105 mm, over twice the magnitude of the highest daily rainfall (47 mm) during the 2012 study. However, the role of precipitation is not intuitively clear. While an increase in clear water inflow to sewers and the subsurface environment would logically dilute virus concentrations, the introduction of low-ionic strength water and any increases in fluid velocity would be expected to enhance virus transport in porous media.33 Periods of increased precipitation and infiltration through the vadose zone would thus increase transport to groundwater. The 2008 and 2012 studies provide a contrast in the relationship between virus detections and local sewer conditions. Figure 5 illustrates higher rates of virus occurrence at sites with older sewers during 2008 conditions, but this is not evident in the 2012 data. Regression analysis supports the relationship observed in 2008, with weak evidence that sites with older sewers have a higher rate of 14 Gotkowitz et al.


Page 15 of 25


virus occurrence than sites with newer sewer systems (p-value = 0.07). Thus, under conditions of sufficient precipitation, older clay sewer pipe appears more prone to sewage exfiltration than newer, PVC-plastic sewers. Implications This study characterized the temporal and spatial distribution of pathogen contamination of shallow groundwater beneath urban sanitary sewers of varying age and condition. Data reflect a year of repeated sampling for human enteric viruses at a network of sites in both older neighborhoods, with dense networks of clay sewers, and in recently developed areas with relatively new plastic sewer systems. Unexpectedly, a severe regional drought occurred during the initial months of this project, resulting in reduced infiltration through the vadose zone, an increase in soil temperature, and low water table elevation. We suggest that these conditions inhibited virus transport from sewers to the water table, resulting in a low virus detection rate, 3.7%, compared to a 2008 study at some of the same sites and wells. The 2008 sampling occurred during a historically wet period, which brought about a 46% virus-positive rate. The sharp contrast in weather patterns dominating these two field studies provides insight into the transport of human enteric viruses from sewers to the water table. These studies demonstrate that the episodic nature of pathogen presence in groundwater results from climatic and hydrologic conditions. Precipitation events were associated with virus concentrations in groundwater during both studies, and during the large storm events in 2008, inflow to sanitary sewers was also positively associated with virus concentrations in groundwater. Although the 2012 study had a low overall detection rate, a return of frequent precipitation and periods of high sanitary sewer flow resulted in several virus detections following the drought. Significantly, there was a coincidence in timing of viruses in groundwater across the seven sites, with 16 of the 17 positive samples collected during a six-month period. Data from the earlier study also exhibited this similarity 15 Gotkowitz et al.



Page 16 of 25

across the sites, such that wells throughout the urban area were virus-positive or negative at similar times.21 Each of the six wells sampled during the 2008 study were virus positive at some time during that study, and 59% (13 of 22 wells) sampled in 2012 were virus-positive, demonstrating that urban groundwater systems are vulnerable to widespread, episodic virus contamination. These results support infrastructure repair and replacement to reduce sewage exfiltration under specific climatic conditions. A relationship between sewer age and virus contamination emerged during the historically wet conditions in 2008, with sewer age positively correlated with the rate of virus detections in near-by groundwater. This relationship was not apparent during the droughtaffected study, suggesting that although sewer condition has a discernible effect on virus contamination of groundwater, weather and transient hydrologic conditions dominate pathogen transport to the water table. Annual precipitation across the US has increased about 5% over the last 50 years, while the amount of rain falling in very heavy storms has increased by about 20 percent.34 Climate models suggest both the frequency and intensity of heavy downpours will increase across the continental U.S. Thus, the conditions shown here to promote virus transport from sewer to the water table may persist, adding to the value of investment in sanitary sewer renewal and replacement. The association between wet conditions and higher concentrations of pathogens in wells demonstrated in these studies is consistent with an association between acute gastrointestinal illness and precipitation observed in communities receiving untreated municipal groundwater supplies.15 This holds significant implications for public health, due to the large number of public water systems in the U.S. that do not adequately or routinely disinfect groundwater8. In communities that rely on wells in close proximity to sanitary sewers, assessing well vulnerability to pathogens with a groundwater testing program will require repeated sampling under a variety of short-term (i.e., months to years) climate patterns. Although the lack of correlation between total coliform test results and virus 16 Gotkowitz et al.


Page 17 of 25


occurrence during this study is not surprising, local officials responsible for their community water systems may benefit from a greater understanding of indicator bacteria and pathogens. Absent a federal requirement for groundwater disinfection, local officials might see value in risk reduction provided by routine and adequate disinfection practices. The increased frequency of large storms and the significant cost associated with replacing aging sewer infrastructure support both the public health benefit and the cost-effective nature of routine disinfection of groundwater supplies in urban settings. Supporting Information More explanation of (1) the hydrogeologic setting, instrumentation, and field procedures; (2) well-bywell results; (3) coliform bacteria in wells; (4) evaluation of water quality indicators; and (5) statistical analyses of relationships between virus detections, and site and hydrologic conditions. This information is available free of charge via the Internet at http://pubs.acs.org. Acknowledgements This work was funded by U.S. EPA STAR grant 834869. We thank the Madison and Fitchburg Water Utilities, Madison Metropolitan Sewerage District, Madison Parks Department, and field technicians Jacob Krause, Robert Bradbury, Jackson Borchardt, and Peter Chase. Suggestions from three anonymous reviewers greatly improved this manuscript. Literature Cited 1. Rutsch, M.; Rieckermann, J.; Cullmann, J.; Ellis, J. B.; Vollertsen, J.; Krebs, P., Towards a better understanding of sewer exfiltration. Water Res. 2008, 42, 2385-2394. 2. Wolf, L.; Eiswirth, M.; Hotzl, H., Assessing sewer-groundwater interaction at the city scale based on individual sewer defects and marker species distributions. Environmental Geology 2006, 49 (6), 849-857. 17 Gotkowitz et al.



Page 18 of 25

3. Hunt, R. J.; Borchardt, M. A.; Richards, K. D.; Spencer, S. K., Assessment of Sewer Source Contamination of Drinking Water Wells Using Tracers and Human Enteric Viruses. Environ. Sci. Tech. 2010, 44 (20), 7956-7963. 4. Ellis, J. B.; Revitt, D. M., Sewer losses and interactions with groundwater quality. Water Sci. Technol. 2002, 45 (3), 195-202. 5. Lambertini, E.; Spencer, S. K.; Kieke, B. A., Jr.; Loge, F. J.; Borchardt, M. A., Virus contamination from operation and maintenance events in small drinking water distribution systems. J. Water Health 2011, 9 (4), 799-812. 6. Blackwood, D. J.; Ellis, J. B.; Revitt, D. M.; Gilmour, D. J., Factors influencing exfiltration processes in sewers. Water Sci. Technol. 2005, 51 (2), 147-154. 7. Sair, A. I.; D' Souza, D. H.; Jaykus, L. A., Human enteric viruses as causes of foodborne disease. Compr. Rev. Food Sci. Food Saf. 2002, 1 (2), 73-89. 8. National Primary Drinking Water Regulations: Groundwater Rule. In 71, Agency, U. E. P., Ed. Federal Register 2006; 216, 65660. 9. Wallender, E. K.; Ailes, E. C.; Yoder, J. S.; Roberts, V. A.; Brunkard, J. M., Contributing Factors to Disease Outbreaks Associated with Untreated Groundwater. Ground Water 2014, 52 (6), 88697. 10. Messner, M.; Shaw, S.; Regli, S.; Rotert, K.; Blank, V.; Soller, J., An approach for developing a national estimate of waterborne disease due to drinking water and a national estimate model application. J. Water Health 2006, 4, 201-240. 11. Borchardt, M. A.; Spencer, S. K.; Kieke, B. A.; Lambertini, E.; Loge, F. J., Viruses in nondisinfected drinking water from municipal wells and community incidence of acute gastrointestinal illness. Environ. Health Perspect. 2012, 120 (9), 1272-9.

18 Gotkowitz et al.


Page 19 of 25


12. Curriero, F. C.; Patz, J. A.; Rose, J. B.; Lele, S., The Association Between Extreme Precipitation and Waterborne Disease Outbreaks in the United States, 1948-1994. American Journal of Public Health 2001, 91 (8), 1194-1199. 13. Auld, H.; MacIver, D.; Klaassen, J., Heavy rainfall and waterborne disease outbreaks: The Walkerton example. J. Toxicol. Environ. Health 2004, 67 (20-22), 1879-1887. 14. Thomas, M. K.; Charron, D. F.; Waltner-Toews, D.; Schuster, C.; Maarouf, A. R.; Holt, J. D., A role of high impact weather events in waterborne disease outbreaks in Canada, 1975 - 2001. Int. J. Environ. Health Res. 2006, 16 (3), 167-180. 15. Uejio, C. K.; Yale, S. H.; Malecki, K.; Borchardt, M. A.; Anderson, H. A.; Patz, J. A., Drinking water systems, hydrology, and childhood gastrointestinal illness in Central and Northern Wisconsin. Am. J. Public Health 2014, 104 (4), 639-46. 16. Powell, K. L.; Taylor, R. G.; Cronin, A. A.; Barrett, M. H.; Pedley, S.; Sellwood, J.; Trowsdale, S. A.; Lerner., D. N., Microbial contamination of two urban sandstone aquifers in the UK. Water Res. 2003, 37 (2), 339-352. 17. Borchardt, M. A.; Bradbury, K. R.; Alexander, E. C.; Kolberg, R. J.; Alexander, S. C.; Archer, J. R.; Braatz, L. A.; Forest, B. M.; Green, J. A.; Spencer, S. K., Norovirus Outbreak Caused by a New Septic System in a Dolomite Aquifer. Ground Water 2011, 49 (1), 85-97. 18. Abbaszadegan, M.; LeChevallier, M.; Gerba, C., Occurrence of viruses in US groundwaters. Journal of American Water Works Association 2003, 95, 107-120. 19. Lambertini, E.; Borchardt, M. A.; Kieke, B. A., Jr.; Spencer, S. K.; Loge, F. J., Risk of viral acute gastrointestinal illness from nondisinfected drinking water distribution systems. Environ. Sci. Tech. 2012, 46 (17), 9299-307.

19 Gotkowitz et al.



Page 20 of 25

20. Hunt, R. J.; Borchardt, M. A.; Bradbury, K. R., Viruses as Groundwater Tracers: Using Ecohydrology to Characterize Short Travel Times in Aquifers. Ground Water 2014, 52 (2), 187193. 21. Bradbury, K. R.; Borchardt, M. A.; Gotkowitz, M. B.; Spencer, S. K.; Zhu, J.; Hunt, R. J., Source and Transport of Human Enteric Viruses in Deep Municipal Water Supply Wells. Environ. Sci. Tech. 2013, 47 (9), 4096-4103. 22. Gellasch, C. A.; Bradbury, K. R.; Hart, D. J.; Bahr, J. M., Characterization of fracture connectivity in a siliciclastic bedrock aquifer near a public supply well (Wisconsin, USA). Hydrogeol. J. 2013, 21 (2), 383-399. 23. Parsen, M. J.; Bradbury, K. R.; Hunt, R. J.; Feinstein, D. T. The 2016 Groundwater Flow Model for Dane County, Wisconsin. Wisconsin Geological and Natural History Survey Bulletin 110: 2016. 24. Lambertini, E.; Spencer, S. K.; Bertz, P. D.; F.J. Loge; Kieke, B. A.; Borchardt, M. A., Concentration of enteroviruses, adenoviruses, and noroviruses from drinking water by use of glass wool filters. Appl. Environ. Microbiol. 2008, 74 (10), 2990-2996. 25. Millen, H. T.; Gonnering, J. C.; Berg, R. K.; Spencer, S. K.; Jokela, W. E.; Pearce, J. M.; Borchardt, J. S.; Borchardt, M. A., Glass Wool Filters for Concentrating Waterborne Viruses and Agricultural Zoonotic Pathogens. Jove-Journal of Visualized Experiments 2012, (61). 26. Gibson, K. E.; Schwab, K. J.; Spencer, S. K.; Borchardt, M. A., Measuring and mitigating inhibition during quantitative real time PCR analysis of viral nucleic acid extracts from largevolume environmental water samples. Water Res. 2012, 46, 4281-4291.

20 Gotkowitz et al.


Page 21 of 25


27. Payment, P.; Waite, M.; Dufour, A., Introducing Parameters for the Assessment of Drinking Water Quality. In Assessing Microbial Safety Of Drinking Water, Improving Approaches and Methods, World Health Organization, OECD Publishing: London 2003; 47-77. 28. Lance, J. C.; Gerba, C. P., Virus Movement in Soil During Saturated and Unsaturated Flow. Appl. Environ. Microbiol. 1984, 47 (2), 335-337. 29. Wan, J. M.; Wilson, J. L.; Kieft, T. L., Influence of the Gas-Water Interface on Transport of Microorganisms through Unsaturated Porous-Media. Appl. Environ. Microbiol. 1994, 60 (2), 509516. 30. DeNovio, N. M.; Saiers, J. E.; Ryan, J. N., Colloid movement in unsaturated porous media: Recent advances and future directions. Vadose Zone J. 2004, 3 (2), 338-351. 31. Yates, M.; Gerba, C.; Kelley, L., Virus persistence in groundwater. Appl. Environ. Microbiol. 1985, 49 (4), 778-781. 32. Fitzpatrick, F. A.; Peppler, M. C.; Walker, J. F.; Rose, W. J.; Waschbusch, R. J.; Kennedy, J. L., Flood of June 2008, Southern Wisconsin. U.S. Geological Survey Scientific Investigations Report 2008-5235 2008, 24. 33. Johnson, W., P. Mechanisms of Retention of Biological and Non-biological Colloids in Porous Media: Wedging and Retention in Flow-Stagnation Zones in the Presence of an Energy Barrier to Deposition. In Microbial Surfaces: Structure, Interactions, and Reactivity; Camesano, T. A., Mello, C. M., Eds.; Oxford University Press: Cary, NC 2008; (984), 43-47. 34. Karl, T. R.; Melillo, J. M.; Peterson, T. C., Global Climate Change Impacts in the United States. Cambridge University Press: New York, NY, 2009.

21 Gotkowitz et al.



Page 22 of 25

FOR TABLE OF CONTENTS ONLY: abstract art

Figure 1. Study sites (triangles), water table monitoring well 1297 (dot), regional wastewater treatment plant (star) in Madison, Wisconsin. Fitchburg neighbors Madison, to the south. See Table 1 for site details. Regional sewer collection mains, pressurized in blue lines and gravity in brown lines, are also shown.

22 Gotkowitz et al.


Page 23 of 25


Upper Aquifer

monitoring wells Depth (m) Well 19 19D 19S sanitary sewer 0 Holy Hill Fm. 5 water table Tunnel City Group 34

217

Eau Claire aquitard Lower Aquifer

67

Wonewoc Formation casing 79.3 m

Mount Simon Formation

open borehole

well depth 218.8 m

crystalline rock

not to scale

5/13

4/13

3/13

2/13

1/13

12/12

11/12

10/12

9/12

8/12

7/12

6/12

Concentration, gc/L

Figure 2. Hydrostratigraphy, lower aquifer municipal well, and monitoring well construction at study site 19. Two sites included a multiaquifer municipal well, with casing extending only into the upper aquifer.

Figure 3. Virus-positive samples in groundwater. Concentrations are summed for samples that contained more than one virus type.

23 Gotkowitz et al.



sewer infiltration & inflow

Page 24 of 25

wastewater virus concentration

8

10

6x10

4

4x10

4

7

10

6

10

2x104

5

10

104

0x10

0

3

100 groundwater

wells

75

4

50 5

25 0

6 30

100

precipitation and soil temperature

75

20

50 25

10

0

2008 Study

Date

2012 Study

Figure 4. Comparison of virus occurrence and hydrologic conditions in 2008 (left) to 2012 (right). The total load of seven viruses in wastewater and infiltration and inflow to sanitary sewer (top), percent virus-positive samples during each sampling period and depth to water table (middle), daily precipitation and soil temperature (bottom). Groundwater levels from well 1297 (see Figure 1).

24 Gotkowitz et al.


Page 25 of 25


11

7

60

19 50

12

40

13 30

30 6

2012

13 5

FB11 4 7

11

19

30

3 Lake Edge 2 1925

1950

1975

2000

Year of sewer construction

Figure 5. Virus occurrence at sites as a function of sewer age during 2008 (top) and 2012 (bottom) studies.

25 Gotkowitz et al.


Effects of Climate and Sewer Condition on Virus Transport to

Recommend Documents