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Environmental engineering paper: Wastewater in the developing world
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Wastewater Infrastructure for Small Cities in an Urbanizing World: Integrating Protection of Human Health and the Environment with Resource Recovery and Food Security Matthew E. Verbyla,* ,Stewart M. Oakley, and James R. Mihelcic Civil and Environmental Engineering, University of South Florida, 4202 E. Fowler Avenue, ENB 118, Tampa, Florida 33620, United States Civil Engineering, California State University, Chico, California, 95929, United States ABSTRACT: The majority of population growth in develop- ing countries will occur in small cities closely linked to agricultural zones, with poor access to water and sanitation. Wastewater management priorities in these regions will be dierent from those in larger cities and developed countries. Two wastewater treatment systems in Bolivia, one with an upow anaerobic sludge blanket (UASB) reactor and polishing ponds, the other with three stabilization ponds, are assessed to determine their resource recovery potential. The UASB reactor produces biogas with 500-650 MJ per day. In six months, both systems discharge wastewater with the same mass of nutrients as fertilizers used to produce crops containing 10-75 daysworth of the recommended food energy intake for each person using the system. Both systems also discharge detectable levels of helminth eggs, Giardia cysts, and Cryptosporidium oocysts, but the UASB reactor system discharges higher concentrations, implying limited reuse potential. From a regional management standpoint, small cities should not expend resources to treat wastewater to levels suitable for discharge into surface waters. Rather, they should focus on removing pathogens to reclaim water and nutrients. Biogas recovery may be a priority that should be subservient to water and nutrient recovery in these settings. 1. INTRODUCTION More than half of the urban population in developing countries lives in cities with less than 500,000 inhabitants, which are generally more connected with agricultural production zones than they are with other urban areas. 1 These small cities are expected to double both in number and in population by 2025. 2 Residents of these areas have some of the worst access to water, sanitation, and hygiene services, and their economic prosperity and health is dependent on food security and ecosystem management. 3 Water and sanitation solutions for these areas are complex; for example, dry sanitation technologies such as composting latrines have been promoted and provide an appropriate solution for some areas, but will not work in others for social and cultural reasons. 4 Between 1990 and 2000, 248 million urban dwellers in Asia, Africa, and Latin America made new connections to sewer systems, representing a third of the total urban population gaining access to improved sanitation during that time. 5 Growing populations in small cities of developing countries will likely continue to connect to sewer systems; however, without adequate treatment, the discharges from those systems will degrade surface waters in areas that already have poor water quality, leading to increased health risks and decreased economic opportunities for those who depend on water quality for their livelihood. 6 In larger industrialized cities, wastewater is often treated via mechanized processes that require energy inputs, only a fraction of which can be recovered by harvesting biogas from the anaerobic digestion of sludge. While anaerobic wastewater treatment processes can potentially increase overall energy recovery yields, 7 wastewater reuse also provides signicant energy and carbon emission savings by osetting energy needed for manufacturing and distributing fertilizers and supplying irrigation water. 8 Wastewater reuse is also one solution to provide global food security amidst the looming phosphorus crisis. 9 In developing countries, community-managed infrastructure often fails prematurely due to maintenance deciencies that result from decreasing nancial durability and community activity as the system ages. 10 Small cities in developing countries tend to fall into what has been termed an infrastructure management gap 11 they are large and compact enough to have centralized utilities (such as sewer collection systems), but they are too small to have the resources within the community to manage highly mechanized infrastructure. Received: December 12, 2012 Revised: March 7, 2013 Accepted: March 8, 2013 Published: March 8, 2013 Policy Analysis pubs.acs.org/est © 2013 American Chemical Society 3598 dx.doi.org/10.1021/es3050955 | Environ. Sci. Technol. 2013, 47, 3598-3605
Transcript
Page 1: Wastewater Infrastructure

Wastewater Infrastructure for Small Cities in an Urbanizing World:Integrating Protection of Human Health and the Environment withResource Recovery and Food SecurityMatthew E. Verbyla,*,† Stewart M. Oakley,‡ and James R. Mihelcic†

†Civil and Environmental Engineering, University of South Florida, 4202 E. Fowler Avenue, ENB 118, Tampa, Florida 33620, UnitedStates‡Civil Engineering, California State University, Chico, California, 95929, United States

ABSTRACT: The majority of population growth in develop-ing countries will occur in small cities closely linked toagricultural zones, with poor access to water and sanitation.Wastewater management priorities in these regions will bedifferent from those in larger cities and developed countries.Two wastewater treatment systems in Bolivia, one with anupflow anaerobic sludge blanket (UASB) reactor and polishingponds, the other with three stabilization ponds, are assessed todetermine their resource recovery potential. The UASB reactorproduces biogas with 500−650 MJ per day. In six months, bothsystems discharge wastewater with the same mass of nutrientsas fertilizers used to produce crops containing 10−75 days’worth of the recommended food energy intake for each personusing the system. Both systems also discharge detectable levels of helminth eggs, Giardia cysts, and Cryptosporidium oocysts, butthe UASB reactor system discharges higher concentrations, implying limited reuse potential. From a regional managementstandpoint, small cities should not expend resources to treat wastewater to levels suitable for discharge into surface waters.Rather, they should focus on removing pathogens to reclaim water and nutrients. Biogas recovery may be a priority that shouldbe subservient to water and nutrient recovery in these settings.

1. INTRODUCTION

More than half of the urban population in developing countrieslives in cities with less than 500,000 inhabitants, which aregenerally more connected with agricultural production zonesthan they are with other urban areas.1 These small cities areexpected to double both in number and in population by 2025.2

Residents of these areas have some of the worst access to water,sanitation, and hygiene services, and their economic prosperityand health is dependent on food security and ecosystemmanagement.3 Water and sanitation solutions for these areasare complex; for example, dry sanitation technologies such ascomposting latrines have been promoted and provide anappropriate solution for some areas, but will not work in othersfor social and cultural reasons.4

Between 1990 and 2000, 248 million urban dwellers in Asia,Africa, and Latin America made new connections to sewersystems, representing a third of the total urban populationgaining access to improved sanitation during that time.5

Growing populations in small cities of developing countrieswill likely continue to connect to sewer systems; however,without adequate treatment, the discharges from those systemswill degrade surface waters in areas that already have poor waterquality, leading to increased health risks and decreasedeconomic opportunities for those who depend on water qualityfor their livelihood.6

In larger industrialized cities, wastewater is often treated viamechanized processes that require energy inputs, only afraction of which can be recovered by harvesting biogas fromthe anaerobic digestion of sludge. While anaerobic wastewatertreatment processes can potentially increase overall energyrecovery yields,7 wastewater reuse also provides significantenergy and carbon emission savings by offsetting energy neededfor manufacturing and distributing fertilizers and supplyingirrigation water.8 Wastewater reuse is also one solution toprovide global food security amidst the looming phosphoruscrisis.9

In developing countries, community-managed infrastructureoften fails prematurely due to maintenance deficiencies thatresult from decreasing financial durability and communityactivity as the system ages.10 Small cities in developingcountries tend to fall into what has been termed aninfrastructure management gap11they are large and compactenough to have centralized utilities (such as sewer collectionsystems), but they are too small to have the resources withinthe community to manage highly mechanized infrastructure.

Received: December 12, 2012Revised: March 7, 2013Accepted: March 8, 2013Published: March 8, 2013

Policy Analysis

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Wastewater treatment systems in developing countries areoften overloaded or abandoned altogether due to energydemands, lack of skilled operators, and inadequate sludgemanagement.12 In fact, it is estimated that 1.5 billion people usesewerage facilities with no treatment13 and global estimates ofthe total area irrigated with untreated wastewater range from 3million14 to 20 million hectares.15 This places farmers, vendors,and consumers at a greater risk for excreta-related diseases,which account for one-tenth of the global disease burden.16

When determining the most appropriate way to sustainablymanage wastewater in small cities of developing countries,policy-makers, development agencies, and local stakeholdergroups face a continuum of alternatives and trade-offs.Wastewater contains water, nutrients, and energy resources,which can each be recovered for reuse. Alternatively, treatedeffluents can be discharged if nutrients are removed to limitsthat protect receiving waters from nutrient imbalances. Yet, thetrade-off for this may be the need for additional complexity, aswell as energy and chemical inputs for retrofitting or expandingtreatment plants to include tertiary nutrient removal, and foroperation, maintenance, laboratory monitoring, and evaluationtasks.17 However, if treated wastewater is used to irrigate crops,nutrient limits do not need to be monitored, and farmers mayeven be able to expand operations, increase productivity, oroffset costs associated with commercial fertilizers. The publichealth impact of wastewater irrigation, if pathogens are notremoved or inactivated, is yet another trade-off. The removal ofhelminth eggs is especially critical if wastewater is to be reusedfor irrigation in developing communities, where incidence ratesof helminthiasis are high.Given the need to make informed decisions about waste-

water management in urbanizing developing countries amidstthis continuum of alternatives and trade-offs, priorities shouldbe determined regarding the recovery of water, nutrient, andenergy resources. Furthermore, it is important to evaluateresource recovery in systems with appropriate technologies thatfill the infrastructure management gap in small developingcountry cities, in a way that links sanitation goals with urbanwater management and food production. Can water, nutrients,and energy all be recovered, while meeting appropriate healthtargets and protecting the environment?

Accordingly, the purpose of this study is to evaluate theresource recovery potential of wastewater from two treatmentsystems serving small (and growing) cities in the Yungas regionof Bolivia: one consisting of three stabilization ponds in series(three-pond system), and the other consisting of an upflowanaerobic sludge blanket (UASB) reactor followed by twopolishing ponds in series (UASB−pond system). Specifically,the two systems are compared with respect to their removal ofconventional wastewater quality parameters, nutrients, patho-gens (helminth eggs, Giardia cysts, Cryptosporidium oocysts),and bacterial pathogen indicators, using the 2006 World HealthOrganization (WHO) guidelines19 as a benchmark. Nitrogenand phosphorus concentrations in the effluent are measured todetermine their potential fertilizer value for agricultural reuse.Assessing the wastewater reuse potential in geographicalsettings like this is particularly important since a recent studyof the watersheds in this agriculturally productive regionconcluded that they exhibit water stress due to climatechange.20

Stabilization ponds have been used globally to treatwastewater for over 100 years, and are especially common indeveloping country cities of all sizes. The UASB reactor is anadvanced anaerobic wastewater treatment technology thatallows for the recovery of biogas. Originally developed totreat industrial wastewater, these reactors were successfullydemonstrated at a pilot scale for the treatment of domesticwastewater in the 1980s, and thousands of full-scale systemshave since been implemented worldwide, especially in LatinAmerica and South Asia.21

2. MATERIALS AND METHODS

The two systems in this study are located within 20 km fromeach other, at elevations of 400 and 460 m above sea level, in atropical region with an average annual ambient temperature ofapproximately 25 °C.22 The three-pond system started outserving a population of approximately 420 people in 2006, andby 2012 the population connected to the system had grown to780 people. Twenty-four-hour flow measurements taken in thissystem during the month of June between 2007 and 2012resulted in average daily flow rates that ranged from 52 m3/day(in 2007) to 121 m3/day (in 2012). The average per capita flowin this community was 120 ± 32 L/person/day. The UASB−

Figure 1. Schematic diagram of the upflow anaerobic sludge blanket (UASB)−pond system (top); and the three-pond system (bottom).

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pond system started out serving a population of approximately780 people in 2006, but has since increased coverage to nowserve approximately 1310 people. Twenty-four-hour flowmeasurements taken during the month of June between 2007and 2012 show that the average daily flow rate in this systemhas ranged from 43 m3/day (in 2007) to 124 m3/day (in 2012).The average per capita flow between 2007 and 2012 in thissystem is only 63 ± 21 L/person/day. The apparent differencein the observed per capita flow rates may be explain by the factthat water supply in the UASB−pond community is metered(customers pay a rate that is based on consumption), whereascustomers in the three-pond community pay a flat monthly rateregardless of use.Figure 1 depicts a schematic of both systems, showing the

sampling locations. All wastewater samples were collected inJune (during the dry season). Grab samples were collectedfrom 2007 to 2011 during the hours of peak daily flow(between 7:00 a.m. and 10:00 a.m.) and analyzed forthermotolerant coliforms, in accordance with either the most

probable number method or the membrane filtration method.23

The maximum holding time for grab samples was 24 h.Composite samples were generally collected in one or more 10-L plastic containers in the field at hourly intervals over thecourse of 24 h, such that the volume collected each hour wasproportional to the flow rate measured during that hour.Composite samples were analyzed annually from 2007 to 2011for five-day biochemical oxygen demand (BOD5), totalsuspended solids (TSS), total nitrogen (TN), and totalphosphorus (TP) in accordance with Standard Methods.23

Composite samples were also analyzed for helminth eggs (in2011 and 2012) and for Giardia and Cryptosporidium (in 2012).The sample volumes for physical−chemical parameters were2.0 L each; sample volumes for helminth egg analysis rangedfrom 2.0 to 32.1 L; and sample volumes for Giardia andCryptosporidium analysis were 4.0 L each. The maximumholding time for composite samples was 48 h. All samples wereeither stored on ice in a cooler, or in a refrigerator, until thetime of analysis in the laboratory.

Figure 2. Observed mass balance removal of total nitrogen, total phosphorus, and thermotolerant coliforms (a) in the three-pond system (□) and inthe UASB−pond system (■); also, (b) in the facultative pond from the three-pond system (□) and in the UASB reactor (■).

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Helminth egg samples that were larger than 4.0 L in volumewere concentrated in the field as follows: samples weretransferred to buckets and placed on a flat surface for at least 4h to allow eggs to settle, after which time the supernatant wasdecanted using a siphon and the remaining sediments weretransferred into prerinsed 2-L plastic bottles and transportedwithin 48 h on ice to the Centro de Aguas y SaneamientoAmbiental (CASA) laboratory (Cochabamba) for furtherprocessing and analysis. Samples for conventional water qualityparameters and for Giardia and Cryptosporidium analysis werenot concentrated in the field, but were transferred directly intoprerinsed 2-L plastic bottles for delivery to the laboratory.Sludge core samples were also collected from the first pond inthe three-pond system (in 2011 and 2012) and from the UASBreactor (in 2012), and were transferred directly into opaqueplastic containers, placed on ice, and transported within 48 h tothe laboratory.In the laboratory, helminth egg samples were further

concentrated using CASA’s standard protocol, which hasbeen described in detail elsewhere.24 Briefly, eggs were isolatedfrom samples using sedimentation, flotation, and two-phaseseparation, as described by the Mexican Test Method for theDetermination of Helminth Eggs in Water Samples,25 with theexception that magnesium sulfate was used for flotation insteadof zinc sulfate. Representative portions of the concentratedsamples were transferred to 0.1-mm-deep Neubauer countingslides. Concentrated samples were gently mixed by turning thecentrifuge tube over several times before removing the aliquotwith a micropipet for observation under the microscope.Observations were made (2−4 repetitions) on an area of 18mm2 of the slides under a microscope (Eclipse E600, Nikon) ateither 400× or 1000× magnification, where helminth eggs wereidentified and enumerated. The average count was used tocalculate the concentration of helminth eggs in the originalsample. Minimum levels of detection varied depending on thevolume of sample collected, and the final concentrated volumeof each sample (which ranged from 1.1 to 5.0 mL per sample).The number of viable helminth eggs was judged by adding

0.1 mL of 0.4% Trypan Blue solution to a portion of theconcentrated sample containing eggs. Trypan Blue, which stainsnonviable cells, leaving living cells unstained, may overpredictthe number of nonviable eggs, since the amount of stained eggsincreases with respect to time.26 To minimize these effects,samples were read within 5 min of adding the stain. Eggs thatwere unstained within the first 5 min were judged as viable. It isalso important to note that some of the eggs may have been

inactivated or destroyed by the ether used in the final step ofthe concentration process.27

Samples were analyzed for Giardia and Cryptosporidium ingeneral accordance with EPA Method 1623.28 Briefly, sampleswere concentrated as described for the helminth egg analyses,with the exception that the flotation steps were omitted.Giardia cysts and Cryptosporidium oocysts were isolated fromthe concentrated samples using immunomagnetic separationwith Dynabeads (Life Technologies). The entire volume ofeach concentrated sample (two repetitions per sample) wasadded to slide wells. Slide wells were prepared for differentialinterference contrast microscopic evaluation by addingmounting medium, a fluorescein-labeled monoclonal antibodyreagent, and DAPI stain, yielding two final volumes of 100 μLin each well (100 μL per repetition). The number of cysts andoocysts were counted under the microscope, and the averagecount from the two repetitions is reported with the standarddeviation.

3. RESULTS

To compensate for the different per capita water usage rates inthe two communities, a mass balance was performed on eachsystem, and the removal of water quality parameters arecompared as the percent of mass that was removed between theinfluent and effluent points (Figure 2). The observed removalof BOD5, TSS, TN, and TP was similar in both systems.Removal of BOD5 was 91.2 ± 5.4% for the three-pond systemand 86.9 ± 9.8% for the UASB−pond system, which is near thehigher range of expected removal for systems using thesetechnologies.24 Removal of TSS was 84.8 ± 8.9% for the three-pond system and 91.3 ± 3.8% for UASB−pond system. Theremoval of TN and TP in the three-pond system was only 43.2± 30.5% and 40.7 ± 32.4%, respectively; and in the UASB−pond system, only 28.7 ± 33.8% and 22.8 ± 27.1%,respectively.The removal of pathogens and pathogen indicators varied in

both systems. The three-pond system provided a 3.4-log10reduction of thermotolerant coliforms on average (n = 6),which may be higher than the 2.3-log10 reduction (n = 5) thatwas provided in the UASB−pond system (p = 0.1261). Theconcentrations of parasites detected in samples from bothsystems are shown in Figure 3. In the three-pond system,Giardia cysts were detected at a concentration of 159.5 ± 2.8cysts/L at the influent and 22.8 ± 3.9 cysts/L at the effluent.Cryptosporidium oocysts were detected at 6.0 ± 1.4 oocysts/Lat the influent and 4.0 ± 1.4 oocysts/L at the effluent. The

Figure 3. Observed removal of (a) helminth eggs, and (b) Giardia cysts, Cryptosporidium oocysts in both systems. Bar graph represents averageconcentration; all “non-detect” samples were replaced with a value equal to half of the limit of detection. Whiskers represent standard deviations.

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UASB-pond system appeared to provide similar removal:Giardia cysts were detected at 242.3 ± 42.8 and 73.3 ± 13.8cysts/L at the influent and effluent, respectively. Cryptospori-dium oocysts were detected at 9.5 ± 6.4 and 6.5 ± 1.4 at theinfluent and effluent, respectively.Helminth eggs were detected in the raw wastewater of the

three-pond system (1605 ± 1242 eggs/L, n = 3) and theUASB−pond system (average concentration of 1809 ± 1129eggs/L, n = 3). The most common species detected in the rawwastewater samples were Taenia (78.9%), Ascaris (19.1%),Trichuris (1.7%), and Hookworm (0.3%). The only speciesdetected in the treated effluent of the three-pond system wasTaenia, but both Taenia and Ascaris eggs were detected in onesample from the effluent of the UASB−pond system. WhileTaenia is not one of the four helminth genera referred to in theWHO Guidelines for wastewater reuse,29 Taenia eggs havebeen detected in the effluents of a waste stabilization pondsystem in Tunisia with a theoretical HRT of 20 days,30 and in6−10-month-old composted feces from toilets in Panama.31

The ingestion of eggs from the swine species (Taenia solium)can cause cysticercosis in humans, which is an emerging,neglected disease32,33 and the leading cause of acquired epilepsyin the world.34

The three-pond system provided an average overall removalof 97% of all species of soil-transmitted helminth eggs(including Taenia), and Taenia was the only species detectedin the system effluent. Conversely, a large number of helmintheggs (including both Taenia and Ascaris species) was detectedin one of the two composite samples collected at the effluent ofthe UASB−pond system. Sludge samples from the UASBreactor also had a lower average concentration of helminth eggs(236 ± 225 eggs/g TS) than sediment samples collected nearthe inlet of the facultative pond in the three-pond system (841± 606 eggs/g TS) (p = 0.0951).Parasites pose a risk to human health only if they are viable

and infective to humans at the time of exposure. Therefore, it isimportant to understand not only how many parasites arepresent, but also what percentage are still viable. In this study,one out of six helminth eggs isolated from raw wastewatersamples entering the three-pond system, and one out of eighthelminth eggs from raw wastewater samples entering theUASB−pond system were judged to be viable. And while noneof the eggs isolated from pond effluents in either system (n =18 eggs) were judged to be viable, one-third of the eggs isolatedfrom the UASB reactor effluent samples (n = 9 eggs) werejudged to be viable. Sludge samples also showed greater eggviability: one-third of eggs isolated from UASB reactor sludge(n = 15 eggs), and 9 of 24 eggs from the facultative pond sludgewere judged to be viable.

4. DISCUSSIONThere is not much difference between the two wastewatertreatment systems in terms of their ability to remove BOD5 andTSS. While the average removal of BOD5 was higher in thefacultative pond (of the three-pond system) (81 ± 8.6%) thanit was for the UASB reactor (48 ± 39%), the average removal ofTSS was similar in both technologies (74 ± 19% for thefacultative pond and 77 ± 18% for the UASB reactor). Basedon the standard deviations, the facultative pond in this settinghas provided a more consistent removal of BOD5 than theUASB reactor over the lifespan of the project. While thisapparent difference in consistency may be a result of thedifferent per capita flow rates (and wastewater strengths)

between the two communities, it ultimately does not affect theperformance of the entire systems. Removal of BOD5 and TSSwas quite good in both systems, ranging from 85 to 91%.Both systems rely on treatment mechanisms that produce

methane and carbon dioxide emissions, but only the UASBreactor is designed for the collection of biogas, which contains56−77% methane.35 On average, 22 kg of COD was removedfrom the wastewater in the reactor per day. Theoretically,assuming that one-fifth of the COD removed from thewastewater is converted to biomass,36 and that the remainingfraction is converted to biogas, in 1 day, the UASB reactorwould produce biogas with 10−13 kg CH4, and an equivalentharvestable energy content of 500−650 MJ. Measurementsfrom the UASB reactor’s biogas chamber in 200937 support thisresult and suggest that the harvestable energy content of thisreactor may even be slightly higher.If the energy footprint of wastewater management is a

primary concern, wastewater reuse may provide a greaterenergy savings than biogas recovery alone. For example, onerecent study found that water reuse had a higher potential foroffsetting carbon footprint and embodied energy than on-siteenergy generation and nutrient recycling via land application ofbiosolids.8 Eutrophication potential is also an important factorfor wastewater management in developing countries, and in thisstudy, wastewater reuse would decrease eutrophicationpotential by discharging high nutrient loads directly to land.The UASB−pond system discharges high concentrations oftotal nitrogen (51.8 ± 28.1 mg N/L) and phosphorus (9.4 ±4.4 mg P/L) to a receiving water body that is a tributary of theBeni River, which is part of the Amazon basin and a localsource for fishing. The concentrations discharged by the three-pond system are slightly less (34.7 ± 14.1 mg N/L and 6.4 ±2.2 mg P/L), but are still high. Limited nutrient removal is notuncommon in UASB reactors38 and stabilization ponds. Forexample, in a study of 178 different ponds, Racault et al.39

reported removals of only 72% and 68% for total Kjeldahlnitrogen (TKN) and total phosphorus (TP), respectively, with22 mg/L TKN and 8.5 mg/L TP detected on average in thesystem effluents. For a compliance-based approach toeffectively manage the discharge of nutrients to receivingwaters, communities in developing countries with these existingtechnologies would have to retrofit their systems to addadditional nutrient removal components, which would requireadditional financial, complexity, energy, and material inputs.However, if effluents are applied to land, reclaimed nutrientscan offset farmer’s costs for fertilizer or may even augmentproduction capacity. In fact, the phosphorus in human wastealone accounts for one-fifth of the global demand.40

Despite the observed difference in effluent concentrations,the mass discharge rate of nutrients per capita in the effluent ofboth systems is not significantly different, and was found to be3.06 ± 1.39 g/capita/day (total nitrogen) and 0.50 ± 0.22 g/capita/day (total phosphorus). Based on published nutrientapplication rates and crop yields for wheat, maize, and rice inLatin America,41 the volume of treated wastewater dischargedfrom these systems over a period of 6 months is estimated tocontain the same mass of phosphorus as commercial fertilizerthat is used to support the production of 9.8 ± 3.9 kg of wheat,18.9 ± 7.5 kg of maize, or 14.5 ± 5.8 kg of rice per person thatdischarges wastewater to the treatment system. This representsapproximately 100−400 MJ of food energy,42 which isequivalent to 10−75 days’ worth of the recommended dailyfood energy intake for one human.43 While agricultural yield

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will certainly vary based on a variety of regional and site-specificfactors, the calculation shows the potential for integrating urbanwater infrastructure with food security efforts. From a regionalmanagement standpoint, it makes little sense to expendadditional resources to remove nutrients from wastewater sothat it may be discharged without impairing receiving waters.If pathogens are present in the system effluents, the

advantages of nutrient, water, and biogas recovery may becountered by public health risks. Assessing the potential healthrisks from helminth eggs is particularly important in thesesettings due to high incidence rates and because of the fact thatthe infectious dose is low. The infectious dose for helminthscan be as low as one egg, and the eggs of some species, such asAscaris lumbricoides, can survive for months or even years insoil, sediments, or sludge (see review in ref 24). In addition,helminthiasis can impact the nutritional status of children:Ascariasis alone may put as many as 1.5 million children underthe age of 15 at risk for permanent growth retardation.18

The 2006 WHO Guidelines for wastewater reuse,19 whichare designed for a tolerable additional disease burden of 10−6

DALY per person per year, recommend that wastewater usedfor the irrigation of any crop have an average concentration ofless than one helminth egg per liter. In this study, Ascaris,Trichuris, and Hookworm eggs were not detected in the effluentof the three-pond system, but Ascaris eggs were detected in theeffluents of the UASB−pond system. Taenia eggs, which have alower density than Ascaris, Trichuris, or Hookworm eggs,44

were detected in the effluents of both systems. There was a 97%overall reduction of helminth eggs in the three-pond system(70% of which happened in the first pond), compared withonly 23% overall reduction of helminth eggs in the UASBreactor. Thus, the UASB−pond system appears to be lesseffective at removing helminth eggs than the three-pondsystem, and reuse of the UASB−pond system effluent forirrigation may present higher health risks. Though severalrecent publications suggest that 10−4 or 10−5 DALYs per personper year may be a more appropriate health target for someregions,45,46 and because the WHO recommendation forhelminth eggs is based on a limited number of epidemiologicalstudies, it has been suggested that wastewater with averageconcentrations of greater than one helminth egg per liter maystill be suitable for reuse.47 When treatment provides limitedremoval of pathogens, the 2006 WHO Guidelines suggest thatrisks for consumers can be further reduced by implementingnontreatment public health interventions in fields and on farms.For example, produce can be washed, rinsed, or peeled prior toconsumption,48 irrigation can also be ceased several weeks priorto harvesting,49 or drip irrigation systems can be used tominimize contamination of edible portions of the crop.50

However, these interventions generally do not provideadditional protection for farmers or field workers.The results from the Trypan blue staining indicate that

helminth eggs detected in the raw wastewater from bothsystems, in the effluent of the UASB reactor, and in the sludgefrom both systems were more likely to be viable than eggsdetected in the pond effluents from either system. Sedimenta-tion is one of the main mechanisms responsible for thereduction of parasites in stabilization ponds,36 and largerparasites, such as helminth eggs, may be removed in UASBreactors by getting captured in the sludge bed.38 Therefore,many of the parasites that are removed from wastewater willbecome concentrated in the sludge. Nonviable eggs have alower density than viable eggs, and therefore they may settle at

a slower rate or become resuspended during periods of peakflow and advance toward the pond outlet. Similar results werefound in a study in Mexico, where sludge samples located nearthe pond outlet had a higher percentage of nonviable eggs thansamples located near the pond inlet.51 In the present study,sludge samples collected near the inlet of the first pond in thethree-pond system had a higher concentration of helminth eggsthan sludge samples from the UASB reactor, and sludgesamples from both systems had similar percentages of viableeggs. However, stabilization ponds produce less sludge perkilogram of organic material removed than UASB reactors,36

and the sludge from ponds only needs to be removed onceevery few years. Because operators of UASB reactors mustremove sludge every 2−4 weeks, they have the potential to beexposed to sludge more frequently than operators ofstabilization pond systems. Therefore, health risks associatedwith managing biosolids may be greater for a UASB reactorsystem than they are for a stabilization pond system.The two systems in this study used technologies that are

common in small cities of developing countries and canpotentially fill part of the infrastructure management gap. TheUASB reactor in this study produces 500−650 MJ of biogasenergy which can be recovered daily. Both systems dischargeeffluents with the same mass of nutrients as that used incommercial fertilizers to produce food with an energy contentequivalent to 10−75 days’ worth of the recommended dailyfood energy intake for one human. However, the concentrationof pathogens was reduced to a lesser extent in the UASB−pondsystem than in the three-pond system, and helminth eggsdetected in the effluent of the UASB reactor were more likelyto be viable than those detected in stabilization pond effluents.While wastewater management systems in large cities and indeveloped countries may be designed for the removal ofnutrients and discharge into receiving waters, the technologiesused in developing countries do not provide sufficient nutrientremoval to do this without impairing receiving waters. Thereuse of wastewater nutrients for agriculture can offseteutrophication potential and create synergy between sanitationand food security development goals. Thus, wastewatermanagement in small cities of developing countries shoulduse technologies that remove pathogens so that water andnutrients can be safely reclaimed. Direct energy recovery frombiogas may be a priority that should be subservient to water andnutrient recovery in these settings.

■ AUTHOR INFORMATIONCorresponding Author*E-mail: [email protected] authors declare no competing financial interest.

■ ACKNOWLEDGMENTSThis work is based upon work supported by the NationalScience Foundation under Grants 0966410 and 1243510 and aGraduate Research Fellowship awarded to M.E.V. We alsoacknowledge Mercedes Iriarte from the Centro de Aguas ySaneamiento Ambiental at the Universidad Mayor de SanSimon in Bolivia.

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