Published online 31 August 2007
Published in J Environ Qual 36:1528-1533 (2007)
DOI: 10.2134/jeq2006.0523
© 2007 American Society of Agronomy, Crop Science Society of America, and Soil Science Society of America
677 S. Segoe Rd., Madison, WI 53711 USA
TECHNICAL REPORTS
Waste Management
Inactivation of Ascaris suum in a Biodrying Compost System
Amy S. Collicka,
Scott Inglisa,
Peter Wrightb,
Tammo S. Steenhuisa,* and
Dwight D. Bowmanc
a Biological and Environmental Engineering Dep., Cornell Univ., Ithaca, NY 14853
b USDA-Natural Resource Conservation Service, Syracuse State Office, Syracuse, NY
c Microbiology and Immunology, School of Veterinary Medicine, Cornell Univ., Ithaca, NY 14853
* Corresponding author (tss1{at}cornell.edu).
Received for publication December 2, 2006.
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ABSTRACT
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Pathogen contamination of waterways is a serious concern in dairy farming areas where livestock waste is applied to agricultural fields. As an alternative, a biodrying composting system dries collected livestock waste, reduces the strong odors, and has been proposed as a means of reducing, and even eliminating pathogens present in the waste. Therefore, the survival of pathogens in a biodrying composting system was investigated. Dairy farm livestock waste was piled in a biodrying storage shed where forced aeration and natural decomposition processes heated a major portion of the waste pile to temperatures exceeding 55°C. Ascaris suum eggs were used as the surrogate species and inoculated into special chambers and placed at three different elevations at different intervals along the length of the pile. Control chambers were stored in water at 4°C in the laboratory. Both compost and control chambers were removed at Day 4, 8, 12, 16, and 20. The eggs were extracted from the chamber medium and analyzed for viability. No viable eggs were recovered from any of the chambers removed from the compost pile, while 
90% viability was observed in the control chambers. High temperatures and continued drying were the major contributing factors to the inactivation of the helminth eggs. The complete inactivation of A. suum eggs by the biodrying process encourages the storage and treatment of manure to high temperatures and reduced moisture conditions before field spreading to reduce the risk of harmful pathogens contaminating waterways and potential drinking water supplies.
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INTRODUCTION
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FIELD APPLICATION of livestock waste is a common practice in dairy farming areas. The contamination of waterways with excessive phosphorous and nitrogen has been commonly associated with traditional manure application practices. Furthermore, the presence of pathogens in manure and consequent transport to waterways is a serious concern because various pathogens can be transmitted from livestock to humans. In an attempt to reduce contamination, environmental regulations restrict field application to drier periods of the year (late spring and summer in northeastern US) and to fields away from waterways and other pollutant sensitive areas. In addition, the treatment of manure before field application and alternatives to direct field application have been investigated and implemented to decrease manure handling difficulty, control offensive odors, prevent pathogen contamination, and reduce the impact on environmental quality. In the case of pathogens, farm management practices must further consider the health of the animals and the potential for spreading of disease within the herd. Therefore, the primary line of defense would be to prevent initial pathogen contamination. However, on herd infection, the intent of a management practice would be to remove potentially contaminated manure from animal housing, provide a means for its storage, and offer a mechanism for treatment to either reduce or eliminate the presence of pathogens in the bedding mix before it is spread on fields.
As an alternative to direct field spreading, composting has been effective in providing a drier end product, which can be stored, transported, and field applied without strong odors. High in organic matter, composted material may also be sold for profit off the farm (Wright and Inglis, 2002). A form of composting, biodrying uses forced aeration along with the heat generated by natural aerobic decomposition to dry the manure mix. Furthermore, biodrying has been proposed as an effective means of eliminating pathogens (Wright and Inglis, 2002).
The objective of this study was to investigate the survival of pathogens in a biodrying composting pile. We used Ascaris suum eggs as the surrogate species. Ascaris suum, a parasitic helminth of pigs (Pawlowski, 1982; Feachem et al., 1983; Gaasenbeck and Borgsteede, 1998), occasionally infects cattle (Gaasenbeck and Borgsteede, 1998), and is capable, on rare occasions, of infecting people (Pawlowski, 1982). Considered one of the hardiest of known helminths, the eggs of A. suum, a close relative of the very similar human infecting species Ascaris lumbricoides, have been used as surrogate species in examining the effects of various waste treatment processes (USEPA, 1999), such as aerobic (Kato et al., 2003) and thermophilic anaerobic digestion (Aitken et al., 2005a, 2005b), stabilization ponds (Nelson and Darby, 2002), ensiled feces (Caballero-Hernandez et al., 2004), ammonia-treated wastewater (Ghiglietti et al., 1997), and composting sewage sludge (Paluszak et al., 2003). Furthermore, these helminth eggs are regarded as the most resistant to high temperatures (USEPA, 1999), often the major factor in successful composting. Although enteroviruses may be more resistant to high temperatures during short retention times (<10 min), Ascaris eggs have proven to be better indicators of composting processes because viruses are more difficult to recover and enumerate from compost samples (Feachem et al., 1983).
The only similar ascaridoid of cattle is Toxocara vitulorum, which is now quite rare in most of the developed countries of the world although it remains an important parasite of cattle in some parts of the world (Bowman, 2003). The other cattle parasites, e.g., Ostertagia ostertagi, Trichostrongylus spp., Nematodirus spp., Cooperia spp., and the other strongyloid parasites, are not as resistant to environmental extremes as are the eggs of Ascaris (Mentz et al., 2004). Also, although the protozoan pathogens of the genus Eimeria are fairly resistant to environmental extremes, it is believed that they will die in most systems faster than the eggs of ascaridoid nematodes (Farquhar et al., 1979). Also, it has been shown that in most systems the oocysts of Cryptosporidium parvum are less resistant than the eggs of A. suum (Kato et al., 2003). Therefore, A. suum eggs were used in this study to investigate the effectiveness of the biodrying compost system with the belief that if they are destroyed that most other parasite transmission stages and other pathogens of similar or greater vulnerability would also be inactivated. It was felt that the death of all eggs would provide evidence of substantial inactivation that would indicate whether or not the biodrying process was an effective means of pathogen control.
In this biodrying study Sentinel Chambers were used. These chambers have the advantage that they securely contain the pathogen and allow for the eggs to be exposed and equilibrate to external conditions through permeable mesh. The chambers were initially developed to monitor Cryptosporidium parvum survival (Jenkins et al., 1999) and modified to securely contain Ascaris suum eggs inoculated into the chamber medium (usually sludge, soil, or mixed animal waste solids).
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Materials and Methods
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Special chambers containing an animal waste and bedding mix were inoculated with Ascaris suum eggs and situated in a biodrying compost pile located on a small dairy farm. The biodrying system ran for 21 d, and pairs of chambers were sampled at 4-d intervals throughout the process. The eggs from the chambers and from controls stored in the laboratory were recovered and examined for viability.
Egg Collection
Ascaris suum eggs were extracted from pig intestines and feces collected from a slaughterhouse. The feces were washed through a series of sieves ranging from 425 to 38 µm. Eggs were finally collected on the 38-µm sieve. The eggs were stored in a 4°C refrigerator in reverse osmosis (RO) water and 10% formaldehyde to prevent mold growth. Upon use, a portion of the solution was collected and the eggs enumerated.
Chambers
Sentinel Chambers were utilized to monitor the survival of A. suum eggs exposed to the biodrying compost system. The chambers were provided fully assembled (Excelsior Sentinel, Inc., Newfield, NY) and consisted of a 2.5 cm long, 2.5 cm diameter polycarbonate tube enclosed on both ends by stainless steel mesh. The mesh securely contained the eggs within the chamber and allowed for external environment exposure and equilibration.
Chamber Preparation
Animal waste mixed with bedding material was collected from the gutters of the milking barn facility, and then air-dried for 3 d to decrease moisture content. The air-dried waste was dried at 55°C for >24 h, ground, sieved (2 mm diameter openings), and stored at 4°C for use in the chambers. Chambers were filled with the prepared waste material and saturated with RO water. Ten thousand A. suum eggs in solution were pipetted into the saturated chamber medium. The chambers, soaking in 4°C water, were transported to the farm for installment.
A total of 130 chambers were prepared and inoculated with eggs. However, ten chambers were stored in RO water at 4°C in the laboratory refrigerator and served as control chambers throughout the duration of the study.
Compost Preparation
The biodrying compost system is located on an 85 milking cow dairy farm in Delaware County in southeastern New York. The system consisted of a three-sided storage shed equipped with a forced aeration system in the floor and has the capacity to store compost manure mix piled 2 m high for a 21-d cycle (Wright et al., 2001). On the day before chamber installation, manure and bedding was collected from the floor and gutters of the milking barn facility, mixed with alfalfa hay in the compost storage shed, and blown from a side-delivery manure spreader into a storage block at a depth of 0.75 m. Each block consists of three floor aeration channels running the width of the storage facility and length of the pile. After the first layer of chambers was installed, the manure and bedding mix collected from the current day was blown on top of the pile. The final pile was approximately 11.5 m long, 2.2 m wide and had an average depth of 1.2 m (Fig. 1
).
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Fig. 1. Cross-sectional view (A): Chamber pairs situated at the three different elevations, labeled A, B, or C, in the biodrying compost pile. The initial depth of the pile was approximately 1.2 m. Top view of compost pile (B): Circles represent a set of three chamber pairs situated vertically through the pile. Twenty sets of three pairs were situated along horizontal distances on either side of the pile. The four thermocouples located at the horizontal distance of 9.5 m (equivalent with sample set #19) had initial elevations of 94, 74, 45, and 16 cm.
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Four Type T thermocouples were inserted at different elevations (94, 74, 45, and 16 cm) at 9.5 m horizontal distance to monitor the temperature of the pile (Fig. 1B). The temperature was automatically inputted into a time/temperature algorithm programmed with LabVIEW software (National Instruments Corporation, Austin, Texas) (Wright et al., 2001). Two other thermocouples were inserted at the back and front of the pile to record the core temperature of the pile and to be used for controlling the composting process utilizing a PC with analog input/output hardware (Wright et al., 2001).
Chamber Installment
Chambers were situated in pairs in two holes punctured into a 3.8 x 10 cm strip of stainless steel. Measured insulated wire was attached to each stainless plate for removal from the compost pile. Twenty chamber pairs were installed at 1-m horizontal intervals on both sides of the initial 1.2-m high pile at approximately 30 cm from the floor. After the second load was added to the pile, 20 chamber pairs were installed similarly 30 cm from the top of the pile. The final 20 chambers were installed similarly at either 5 or 15 cm from the top of the pile. Therefore, three chamber pairs at different elevations in the pile corresponded to one horizontal distance. The different elevations of 5 or 15 cm from the top of the pile, 30 cm from the top, and 30 cm from the floor were labeled A, B, and C, respectively (Fig. 1A). The end portion of the attached insulated wire was exposed outside of the pile and labeled for sample identification.
Composting Process
Forced aeration was used to increase the natural composting processes and to effectively dry the compost mix. The drying process required a calculated airflow of 0.36 m3 per minute of air for each m3 of compost (Wright and Inglis, 2002).
Fluctuations in temperature controlled the operation of the 1.5 kilowatt fans, which delivered the air through channels spaced every 0.8 m in the floor (Wright and Inglis, 2002). Each channel was covered by steel, perforated by 1.3-cm holes at intervals of 30.5 cm longitudinally. At temperatures below 60°C, the fans ran for 5 to 10 min every hour, and at temperatures above 60°C, the fans ran continuously until the temperature decreased below 60°C. From Day 14 to 21, the fans ran continuously to finish drying the compost.
Sampling
The A-, B-, C-labeled chamber pairs from four different horizontal distance locations were collected during each sampling on 4, 8, 12, 16, and 20 d after installation. Therefore, 24 chambers were collected and transported on ice packs at each sampling. In addition, at each sampling, the height, width, and length of the pile and the elevation and lateral depth (depth from side of pile) of each chamber pair were recorded. The lateral depth was determined by measuring the exposed portion of the insulated wire on each pair then subtracting this length from the total length of the attached wire. In addition to the chamber samples from the compost, two control chambers were removed from the laboratory refrigerator (4°C) for processing on each sampling day.
Chamber Processing
Each chamber was dismantled by removing the mesh from one end and emptying the chamber medium into a cup with a tongue depressor. The chamber was then rinsed thoroughly with RO water into the cup and stirred for 30 s. After passing the mix through a #100 sieve (150 µm pore size), the eggs and other debris were collected on to a #400 sieve (38 µm pore size) and carefully rinsed into a 50-mL tube to a volume of 45 mL. These were centrifuged at approximately 800 g for 3 min, and then the supernatant was decanted, replaced with 45 ml of 1.2 specific gravity MgSO4 solution (epsom salt (MgSO4) and RO water), and mixed well. After centrifugation at 800 g for 15 min, the top 15 ml of solution containing the isolated Ascaris eggs was carefully poured through a #400 sieve, rinsed with RO water to remove excess MgSO4 solution, and then rinsed from the sieve into a 30 ml T25 flask (Fisher Scientific, Pittsburgh, PA) to a volume of 10 ml. To each flask, 50 µL of 37% formaldehyde was added to prevent mold growth. Each flask remained for 4 wk in a 28°C incubator to induce the larvation of viable eggs.
Microscopy and Counting
After incubation and before microscopic examination, 0.5 mL of commercial bleach was pipetted into each flask. The addition of bleach removed the outer wall of the A. suum egg, and the zygote, developing morula, or larvae within the eggshell were then easily viewed. The entire flask was thoroughly examined under a Zeiss IM (inverted microscope) (Carl Zeiss, Inc., Germany) with a 16X objective. A minimum of 100 A. suum eggs were counted and categorized as larvated or not larvated (Fig. 2
), and percent viability was determined by dividing the number of larvated eggs by the total number counted.
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Fig. 2. Images produced from microscopic examination of larvated (A) and not larvated (B) A. suum eggs. Both larvated and non-larvated eggs were present in control chambers, but only eggs that had not larvated were present in those chambers removed from the compost pile.
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Results
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The biodrying system ran for 21 d. During this process, the compost pile decreased in size due to the loss of moisture. An overall decrease in pile height of 24% was observed (solid line in Fig. 3
). The width of the pile did not change substantially over the 21 d.
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Fig. 3. Pile height (thick solid line) and chamber [a (black squares), b (empty squares), and c (gray squares)] elevation at Day 1 (a), Day 4 (b), Day 8 (c), Day 12 (d), Day 16 (e), and Day 20 (f) before each day's sampling. The four horizontal lines in each day's graph represent the elevation of the thermocouples situated at the bottom (line with cross), bottom middle (dash line), top middle (line with X), and top (solid line).
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The elevation above the floor of the chamber pairs decreased along with the pile height. Figure 3A–F provides the initial pile height and initial chamber pair elevations (A) along with the pile height and the elevations of the chamber pairs at Day 4 (B), Day 8 (C), Day 12 (D), Day 16 (E), and Day 20 (F). Very little change (0–2%, depending on sample) was observed in the lateral depth of the samples. In addition to the situation of the chambers, the changing elevation of the four thermocouples was also shown by horizontal lines in Fig. 3A–F.
Although not measured directly, moisture changes were reported qualitatively. The top third of the pile remained saturated for the duration of the study, while the bottom two-thirds dried to a mulch-like texture. The inner core of the bottom 25 cm of the pile heated to such a high temperature (almost unbearable to touch) causing the mulch to convert to ash. Above the super heated portion of the pile, approximately 25 to 50 cm above the floor, the compost was able to dry, reducing moisture significantly, but the temperatures were never so great to cause combustion.
The thermocouples provided temperatures in the bottom, bottom middle, top middle, top of the pile, and at two positions in the core of the pile. Within the first day of the composting process, the bottom, top middle, and top attained temperatures of greater than 55°C and maintained these temperatures for the first 14 d (Fig. 4
). However, the bottom middle thermocouple, positioned initially at 45 cm above the floor (Fig. 3A) then after 20 d at 30 cm (Fig. 3F), maintained a temperature of approximately 30°C for the duration of the study. Temperatures remained between 55 and 65°C at the two thermocouples recording the pile's core temperatures and controlling the fans. After the initial 14 d, temperatures at the six thermocouples decreased below 20°C and remained at temperatures within 10°C of outside temperatures for the final 7 d of the cycle. The full 21-d cycle of temperatures is presented in Fig. 4.
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Fig. 4. Full 21-d cycle of outside temperature and temperatures at four thermocouples situated throughout the biodrying compost pile.
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The chamber pairs labeled C were positioned in between the bottom (>55°C for 14 d) and the bottom middle (approx. 30°C for 14 d) thermocouples. Nearly one-third to half of these chamber pairs decreased in elevation with the bottom middle thermocouple for the 20 d, and the remaining chamber pairs were likely affected by the high temperatures recorded by the bottom thermocouple. Those pairs labeled A and B were associated with the temperatures recorded by the top and top middle thermocouples.
The viability of the A. suum eggs in each chamber was presented as a percent viability. For the first sampling at 4 d and any further sampling, no eggs that completed successful larvation were observed (Fig. 5
). Therefore, all 120-chamber samples were reported as not viable. On the other hand, the control chamber samples had 90% viability at all five samplings (Fig. 5).
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Fig. 5. Inactivation of A. suum eggs extracted from chambers in the biodrying compost pile (dashed line with circles) and from control chambers (line with squares).
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Discussion
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The extensive inactivation of Ascaris suum eggs during this study strongly encourages the treatment of manure before field spreading to reduce the risk of pathogen contamination of the environment. Two key factors most likely causing the inactivation of A. suum eggs exposed to the biodrying composting system were high temperatures (>55°C) in much of the pile and the drying out of the bottom half of the pile. The influence of time and temperature on A. suum inactivation has been extensively studied (Feachem et al., 1983; Aitken et al., 2005a, 2005b). According to a compilation of several of these studies, total inactivation of Ascaris eggs occurred in less than 2 h in conditions in which temperatures remained above 55°C (Feachem et al., 1983). Pecson and Nelson (2005) determined total inactivation of A. suum eggs occurred at temperatures of greater than 51°C in 1 h and greater than 48°C in 24 h. Otherwise, eggs subjected to temperatures of 45°C and below in various conditions required more than 1 yr for complete inactivation (Feachem et al., 1983). The inactivation of the top chamber samples (A and B samples) can be explained by the temperatures in excess of 65°C for >1 wk observed in proximity of these samples. A few of the chamber pairs labeled C, which settled substantially <30 cm elevation), were also in proximity of high temperatures (55–60°C for several consecutive days) recorded by the bottom thermocouple, nearest the biodrying fans and air channels. However, the C sample chambers settling to a lesser extent, just below 30 cm from the bottom of the pile, were associated with temperatures near 30°C, and no viable eggs were found in these chambers even at the first sampling on Day 4. This portion of the pile did experience substantially greater drying compared to the top portion of the pile where it remained moist and temperatures were in excess of 60°C. Because it has been shown to be deleterious to Ascaris eggs (Feachem et al., 1983) and the extent of drying that occurred in the bottom portion of the compost pile, dessication was deemed the likely factor in the inactivation of the sample eggs in the C chambers. Gaasenbeck and Borgsteede (1998) investigated the environmental factors which lead to A. suum inactivation and realized that dryness was an important means of increasing inactivation. Eggs exposed to low relative humidity (<47.5%) or dry, sunny conditions experienced greater inactivation in less time (<8 wk) than those in high humidity and wet, shady conditions (Gaasenbeck and Borgsteede, 1998). Other microbial and composting processes besides the dominating factors of high temperature and reduced moisture may also be important factors responsible for inactivating A. suum eggs but were not investigated during this study.
Aerobic composting with the addition of a bulking agent has been effective in eliminating Ascaris eggs in other studies, as well (Feachem et al., 1983). Careful compost process management by the regulation of moisture content, carbon/nitrogen ratio, and pile temperature was necessary to inactivate the eggs. Pile temperature was deemed the crucial factor in the elimination of the eggs (Feachem et al., 1983). The biodrying system provided additional proof to the effectiveness of temperature and moisture regulation on the management and inactivation of pathogens in the composting processes.
Although additional adjustments to the biodrying system may be required to ensure a thoroughly composted product, the complete elimination of A. suum eggs justifies continued research into this system and other alternative composting systems, which produce high temperatures and reduced moisture conditions, as feasible and environmentally sound manure storage and handling practices for small and medium dairy farms. Ongoing research is being conducted to determine the necessary adjustments to improve the biodrying process and provide a useful dry end product (
40% moisture content), which can be effectively handled to decrease negative environmental impact and to even be sold off the farm for profit (Wright and Inglis, 2002).
Sentinel Chambers have proven effective in monitoring the survival of Ascaris suum in the biodrying compost system. The high viability results from the control chambers ensured the initial viability of the A. suum eggs and ascertained the efficacy of the chamber processing and egg extraction (MgSO4 flotation and pouring the resulting supernatant through a 38-µm sieve) and incubation methods. Furthermore, Nelson and Darby (2001) determined the common reagents (MgSO4, ZnSO4, and NaCl) used during flotation of Ascaris eggs did not significantly affect the viability of the eggs, and sieving the resulting supernatant compared to extracting with acid recovered greater numbers of eggs and did not significantly decrease their viability. Therefore, the inactivation observed in the compost chamber samples was caused by the biodrying process and not by laboratory processing.
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ACKNOWLEDGMENTS
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A special thanks to Elizabeth A. Fogarty for the preparation of Ascaris suum eggs and chambers. This research was conducted with the helpful support and financial resources of the Watershed Agricultural Council (WAC) of Walton, New York and the New York State Energy Research & Development Authority (NYSERDA) of Albany, New York.
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NOTES
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All rights reserved. No part of this periodical may be reproduced or transmitted in any form or by any means, electronic or mechanical, including photocopying, recording, or any information storage and retrieval system, without permission in writing from the publisher.
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ABSTRACT
INTRODUCTION
