Previous Article | Next Article 
Applied and Environmental Microbiology, September 2001, p. 4036-4040, Vol. 67, No. 9
0099-2240/01/$04.00+0 DOI: 10.1128/AEM.67.9.4036-4040.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.
Survival of Fecal Coliforms in Dry-Composting
Toilets
Thomas
Redlinger,1,*
Jay
Graham,2
Verónica
Corella-Barud,2 and
Raquel
Avitia2
Department of Biological
Sciences1 and Center for Environmental
Resource Management,2 The University of
Texas at El Paso, El Paso, Texas 79968
Received 2 April 2001/Accepted 15 June 2001
 |
ABSTRACT |
The dry-composting toilet, which uses neither water nor
sewage infrastructure, is a practical solution in areas with inadequate sewage disposal and where water is limited. These systems are becoming
increasingly popular and are promoted to sanitize human excreta and to
recycle them into fertilizer for nonedible plants, yet there are few
data on the safety of this technology. This study analyzed fecal
coliform reduction in approximately 90 prefabricated, dry-composting
toilets (Sistema Integral de Reciclamiento de Desechos Orgánicos
[SIRDOs]) that were installed on the U.S.-Mexico border in Ciudad
Juárez, Chihuahua, Mexico. The purpose of this study was to
determine fecal coliform reduction over time and the most probable
method of this reduction. Biosolid waste samples were collected and
analyzed at approximately 3 and 6 months and were classified based on
U.S. Environmental Protection Agency standards. Results showed that
class A compost (high grade) was present in only 35.8% of SIRDOs after
6 months. The primary mechanism for fecal coliform reduction was found
to be desiccation rather than biodegradation. There was a significant
correlation (P = 0.008) between classification rating
and percent moisture categories of the biosolid samples: drier samples
had a greater proportion of class A samples. Solar exposure was
critical for maximal class A biosolid end products (P = 0.001). This study only addressed fecal coliforms as an indicator
organism, and further research is necessary to determine the safety of
composting toilets with respect to other pathogenic microorganisms,
some of which are more resistant to desiccation.
 |
INTRODUCTION |
Urban and periurban areas in
developing countries often lack adequate sanitation services for
their rapidly growing populations (11). Lack of the
following accounts for this: financial resources, available water and
space, and institutional infrastructure. Many cities are experiencing
or by the year 2010 will encounter water shortages, which are a major
threat to public health (1, 14, 15).
Urban growth taking place in informal settlements is often overlooked
by municipal governments, which are unable or unwilling to provide
piped water and sewage infrastructure. As a result, many low-income
households must rely on pit latrines or cesspools. This solution is
often not practical because of space requirements for pits, rocky soil
conditions, and well water contamination. Pathogens escaping from
poorly constructed pit latrines and septic tanks have been shown to
contaminate groundwater and surface waters (12).
One approach to safe and sustainable sanitation is the use of dry
sanitation toilets (5). These systems promote recycling of
human excreta, which can be returned to the soil as fertilizer after
pathogen reduction. Pathogen reduction can occur by either dehydration
or biodegradation (10).
Dry sanitation systems require neither water nor sewage infrastructure
for their operation (8). They replace the pit latrine and
have two advantages: they do not pollute the environment and biosolid
waste is sanitized. These systems have the potential to improve public
health by reducing illnesses caused by fecal-oral transmission of pathogens.
In 1999, approximately 300 prefabricated, dry-composting toilets (Grupo
de Tecnología Alternativa) (Naucalpan, Mexico) were installed on the U.S.-Mexico border in three Ciudad Juárez
communities in the state of Chihuahua, Mexico. These units, called
Sistema Integral de Reciclamiento de Desechos Orgánicos (SIRDOs),
are single-vault, solar composting systems. SIRDOs are self-contained fiberglass and plastic structures that stand apart from a home and
usually serve a single family.
This study tested 90 SIRDOs to classify biosolid waste end products as
class A or B based on U.S. Environmental Protection Agency (EPA)
standards with respect to fecal coliform counts. Fecal coliforms are
bacteria meeting these criteria: aerobic and facultative anaerobic,
gram-negative, non-spore forming, and rod-shaped (4, 7).
In addition, they grow and ferment lactose with the production of gas
and acid at 44.5°C, which is the property that permits their
enumeration in the multiple-tube technique (6). This study
not only measured the reduction of these bacteria but also determined
the primary mechanism (biodegradation or dehydration) for reducing
fecal coliforms. Both of these goals were important so that user
maintenance can be optimized to yield a safer end product and so that
user disposal methods can be determined.
 |
MATERIALS AND METHODS |
The study area was located on the outskirts of Ciudad
Juárez, Chihuahua, Mexico, and included the three colonias of
Nueva Galeana, Plutarco Elias Calles, and Felipe
Ángeles. These communities lacked municipal sanitation
services, and most did not have piped water to their homes. Before the
introduction of SIRDOs into the communities, most participants had pit
latrines or an indoor flush toilet that emptied into a pit outside the
home. Study participants were of low socioeconomic status, with an
average yearly income of $3,300.
Dry-composting toilets.
A local foundation provided 300 SIRDOs, and lay health promoters coordinated ecological-theatre events
where participants learned SIRDO operation and management. Families
were assigned a community health promoter who visited them on a regular
basis to assist with SIRDO maintenance. Study participants also
received an instruction booklet for SIRDO operation and a calendar to
remind them of the recommended SIRDO maintenance schedule. Since study participants were new to the concept of dry sanitation and composting, training and support were an integral part of the program.
A cohort design was used to follow a random sample of 90 families using
SIRDOs. The quality of biosolids from the SIRDOs was measured at two
intervals: 3 and 6 months after installation. Study variables included
fecal coliform quantification and moisture content of biosolid waste
samples, stirring the compost heap (aeration), solar exposure,
temperature of composting material, and user maintenance. For the
3-month sampling, the accumulated pile had just been pulled down into
the secondary processing area, which separates it from new waste
additions (Fig. 1). This is the beginning
of a 3-month period during which the composting pile must be aerated by
stirring one or two times per week. The recommended period for
composting the heap is 3 months after pulldown (SIRDO instruction
manual). After this 3-month period in the secondary processing area,
the biosolid waste is removed for disposal. The cycle is repeated by
pulling down the forming pile to begin the composting phase. Consequently, the 3-month sample is collected at the time of pulldown, and the 6-month sample is collected just before biosolid removal for
disposal.

View larger version (34K):
[in this window]
[in a new window]
|
FIG. 1.
Diagram of a single-vault SIRDO showing the forming
pile, which is pulled down after 3 months to produce the composting
pile. The composting pile is located in a secondary processing area
where composting continues without the addition of new waste. The solar
collector is positioned directly over the composting pile and
helps maintain elevated temperatures required for biodegradation or
desiccation. Urine is contained in the secondary processing area and is
not allowed to contaminate the environment.
|
|
Sample collection and analyses.
Samples were taken from five
different sites in the composting heap, combined, and mixed into one
homogeneous sample consisting of 100 to 200 g (fresh weight).
Samples were transported to the laboratory in an ice chest within 2 hours of collection and were analyzed for fecal coliforms on the same
day. After analysis, samples were disinfected or autoclaved.
Five grams of the biosolid waste sample was desiccated in a drying oven
for 24 h, after which the sample was immediately weighed
and dry
weight measurements were calculated as a percentage of
wet weight.
Fecal coliform concentrations were estimated using
the multiple-tube
fermentation direct test (A-1 medium [
13])
as described
previously for the EPA Standard Method 9221 E (
2).
Eleven
grams of the biosolid waste sample was mixed with 99 ml
of sterile
water and was blended for 40 s in a sterile, stainless-steel
Waring blender at low speed. Serial dilutions of the slurry were
made,
and 10 ml of the 10
4, 10
5, and
10
6 dilutions was added to 1 ml of A-1 medium (Hach,
Loveland, Colo.).
The concentration of the A-1 medium was adjusted to
conform to
the standard medium described for the EPA Standard Method
9221
E (
2). Tube contents were incubated at 37°C for
3 h, small
bubbles were removed, and the materials were again
incubated at
44.5°C for 21 h before results were recorded. Gas
in the inverted
Durham tube and turbidity of the medium indicated
positive results,
and the most probable number (MPN) was estimated by
using an MPN
table.
Biosolid waste classifications.
MPN data was categorized
into EPA standards of class A and class B compost. Based on these
classifications (16), class A compost contains safe and
acceptable levels of pathogens and is a safe soil amendment for food
and nonfood plants. It must contain <1,000 MPN fecal coliforms per g.
Class B compost is a safe soil amendment for ornamental plants and must
contain <2 × 106 MPN fecal coliforms per g. In this
study, we followed the above EPA recommended values for class A and
class B compost with respect to the MPN of fecal coliforms. Those
samples with an MPN greater than 2 × 106 fecal
coliforms per g did not fit in either class A or B, so they were placed
in a separate division, class C. The moisture content of biosolid
samples was divided into three groups: <40, 40 to 60, and >60%.
These groups were established for this study based on reported moisture
content considered optimum for aerobic biodegradation (3, 5,
8).
Statistical analysis.
All data were analyzed utilizing
Statistical Package for the Social Sciences (SPSS) statistical
software, and chi-square tests were employed to determine significant
correlations. Logistic regression was used to identify the relationship
of environmental and household factors with the quality of biosolid
waste while controlling for the effect of other variables. The fit of
the model was evaluated using the Hosmer-Lemeshow goodness-of-fit test
(9).
 |
RESULTS |
Biosolid fecal coliforms.
To evaluate the best approach to
analyzing biosolid fecal coliforms, we first looked at the relationship
between the MPN and moisture levels as one of the continuous variables
(Fig. 2). There was a wide distribution
of points at all moisture levels with high standard deviations; thus,
our ability to detect valid relationships among study variables was
limited. Therefore, categorical variables were used to represent fecal
coliforms and percent moisture, using biologically relevant groups as
defined in Materials and Methods.

View larger version (18K):
[in this window]
[in a new window]
|
FIG. 2.
Scatter plots showing distribution of MPN and percent
moisture for 6-month (upper graph) and 3-month (lower graph) samples.
Horizontal dashed lines separate the MPN categories based on fecal
coliform counts: class A, class B, and class C.
|
|
Biosolids were measured at 3 and 6 months. For both the 3- and 6-month
samples, class B was the most abundant classification
at 70.6 and
60.5%, respectively, with the greatest percentage
occurring at 3 months (Table
1). On the other hand,
class A samples,
although not the dominant class, significantly
(
P = 0.043) increased
at 6 months (35.8%) from the
3-month period (19.4%). This demonstrated
that with respect to fecal
coliform reduction, one-third of SIRDOs
produced a high-grade end
product. Also, by 6 months there were
no samples with extremely high
fecal coliform counts (class C).
Missing data reflected in the totals
resulted from inability to
collect samples because study participants
were not at home.
Moisture content.
Moisture content in the compost pile is
related to the amount of soak materials that are added after using the
facilities. Almost all SIRDO users deposited toilet paper (89%) and
sawdust (96%) into the forming pile. As a result, it was difficult to determine the effect of depositing these soak materials in the compost
pile with respect to moisture content and compost classification rating. The high content of soak materials in samples indicated that
SIRDO users were following required protocol for managing their SIRDO units.
Odor associated with toilets is a primary concern of users. In general,
when the moisture content of the heap was low (<40%),
unpleasant
odors were significantly less noticeable (
P < 0.003).
Smell was a subjective measure and was determined by the sampler
at the
time that the biosolid waste sample was taken. Results
from this study
showed that 64.5% of the units did not have a
detectable
odor.
At the ideal moisture content for aerobic biodegradation (40 to 60%),
only four samples met the class A requirements (Table
2). In fact, only 18.0% of all samples
fit into the ideal moisture
content range for aerobic biodegradation.
On the other hand, more
than half (54.0%) had a moisture content of
<40% and this group
also had the highest percentage (73.8%) of class
A compost. The
relationship between biosolid classification rating at 6 months
and moisture content showed that there was a significant
correlation
(
P = 0.008) between the classification
rating and the percent
moisture categories of the biosolid samples.
These findings, taken
together, indicated that the reduction of fecal
coliforms was
primarily the result of desiccation and not of aerobic
biodegradation.
Since desiccation was the primary method of disinfection, moisture
categories were combined to focus on reduced moisture (one
group of
<40% and another of 40 to 100%). Using these new categories,
moisture content was evaluated for 3 versus 6 months, but no
significant
difference was found, although there was a trend in the
direction
of lower moisture content at 6 months (data not shown). These
results indicated that by 3 months, half of the samples already
had
reduced moisture content (<40%) and that this did not change
significantly during the ensuing 3
months.
There was a small number of class A cases (16.7%) that had a moisture
content of >60% (Table
2). These cases were not the
result of
desiccation and not likely the result of aerobic biodegradation,
since
high moisture content excludes oxygen. The most probable
cause of this
reduction in fecal coliform was anaerobic biodegradation.
This was
confirmed by a significant correlation (
P = 0.003) for
moisture content of >60% and associated unpleasant odors which
are
produced during anaerobic biodegradation. The increase in
class A
samples at a moisture content of >60% was not significant,
but there
was a trend (Fishers exact test,
P = 0.168) to more
class A at 6 months (24.0%) than at 3 months (7.1%).
Composting heap temperature.
A characteristic of thermophilic
aerobic biodegradation is a rise in temperature almost immediately
after pulldown and stirring to aerate the pile. Pile temperatures
should rise due to microbiotic aerobic metabolism and may reach 70°C
(3). In this study, the temperature of the heap was
measured by placing a thermometer in the middle of the heap. In
general, temperatures of the compost heaps were usually equal to or
similar to the ambient temperature. There was only one case where there
was a significant difference between the ambient and pile temperatures
(28 and 40°C, respectively), and this pile temperature still did not
fall within the optimum range for thermophilic bacteria. Therefore,
pile temperature data indicated that composting heaps were not
generating heat by aerobic thermophilic microorganisms.
Composting heap aeration.
When there are high moisture content
and insufficient soak material such as sawdust to increase pore space,
oxygen is restricted to the outer surface of the heap. Thus, stirring
or turning over the compost heap is important to encourage growth of
aerobic biodegradation microbes. To determine if the composting heap
had been properly stirred, we employed a subjective estimate by the
sample collector as to the condition of the heap. This was based on
observations of the presence of spiderwebs, large lumps of fecal
material, and in general, a lack of smooth consistency. The condition
of the heap was classified into two groups: mixed and not mixed. This
variable was a reflection of user maintenance of their SIRDO.
In the 6-month sampling, 37.3% of SIRDOs appeared not to have been
mixed, while 62.5% were mixed. The correlation between
classification
of the biosolids and whether they were stirred
was not statistically
significant (
P = 0.200). This result was
not
surprising, since aerobic biodegradation did not appear to
be the
primary method for fecal coliform reduction as noted
above.
Solar exposure.
Solar exposure is important for two reasons.
First, it heats the composting vault and promotes active biodegradation
by thermophilic aerobic microorganisms. Second, it lowers moisture of
the pile and prevents flooding due to excessive urine content.
Seventy-eight percent of the SIRDO units had solar exposure, which is
defined by southern orientation of the passive solar panel on the SIRDO unit and no blockage of the panel to solar irradiation. There was no
significant correlation between solar exposure and moisture content, although there was more dehydration with solar exposure (53 versus 47%). This result reflects the earlier finding that by
3 months, half of biosolid samples already had low moisture content. On the other hand, there was a significant correlation between
solar exposure and compost classification ratings (P = 0.001). Ninety-five percent of the composted samples with class A
ratings were from SIRDOs with solar exposure. This illustrates the
importance of solar exposure and SIRDO directional orientation to
achieve a high-quality end product.
Multivariate analysis. A logistic regression analysis was
conducted to estimate the effects of environmental factors
and user
maintenance on class A biosolids (Table
3). Solar exposure
of SIRDOs remained
highly correlated to class A production. The
odds ratio showed that
class A biosolids were 10.2 times likelier
to occur with solar
exposure. Low moisture was another influential
indicator of class A
biosolids, with an odds ratio of 3.6. As
indicated above and in this
model, neither temperature nor aeration
of the heap showed a
significant correlation with class A biosolids.
The variable
"time" (3 months and 6 months), although not significant,
was in
this model to control for any potential differences between
the 3- and
6-month samples. The Hosmer Lemeshow test showed a
good fit for the
model (Hosmer-Lemeshow goodness of fit,
2 = 3.98;
P = 0.86).
 |
DISCUSSION |
In this study, we investigated fecal coliforms only as indicator
organisms. Other pathogens, especially those forming spores or eggs,
may be less affected by biodegradation and desiccation and can survive
for much longer times. Thus, the reduction of fecal coliforms does not
necessary predict reduction of other, more resistant pathogens, which
also must be considered with respect to handling safety and disposal of
composted biosolid waste.
In dry-sanitation systems, pathogenic microorganisms can be reduced
through biodegradation, desiccation, or a combination of the two
(5). In this study, desiccation was found to be the
principal method for fecal coliform reduction for two reasons. First,
the greatest number of samples (54%) had low moisture content, which
was suboptimum for biodegradation, and of these, 73.8% were class A. Second, only a few samples with optimum moisture for aerobic
biodegradation were class A (<10%).
Desiccation occurs when moisture content is too low for microorganism
survival and when cells die due to lack of water to drive cellular
metabolic processes. On the other hand, aerobic biodegradation occurs
when microorganisms have sufficient water for metabolic processes but
is inhibited when too much water excludes oxygen. When oxygen levels
are too low, anaerobic biodegradation takes over. Thus, a critical
variable in this study was moisture content, which regulated the
primary method (desiccation, aerobic biodegradation, or anaerobic
biodegradation) responsible for fecal coliform reduction.
In this study, there was a highly significant correlation between the
orientation of the SIRDO unit's solar panel (solar exposure) and
higher compost classification (lower fecal coliform counts). The solar
panel was in an optimal position if it faced south and was not shaded
by trees and buildings. The most probable reason for the strong
relationship between solar exposure and lower fecal coliform counts was
that solar exposure heated the SIRDO chamber, promoting fecal coliform
reduction by desiccation. With a lower percentage of water, cells were
killed and biosolid classification was higher. Thus, rather than solar
exposure promoting aerobic biodegradation by raising the pile
temperature, the main effect was drying. Results showed that already by
3 months, more than half of the biosolid piles had less than 40% moisture.
The environmental setting of this study area was a key variable related
to moisture levels of composting heaps. Summer months are hot and dry,
while winter months are sunny, dry, and cool. With a year-round dry
climate, moisture levels in the compost heap are lower than would be
expected in humid, tropical environments. Maintaining sufficient
moisture levels for aerobic biodegradation required that SIRDO managers
(usually the women of the households) be able to judge moisture levels
of the compost heap and adjust with water. This was usually beyond the
expertise of these first-time users and may be a barrier to adequate
maintenance for optimal biodegradation. As a result, at both 3 and 6 months, the moisture content of more than half the SIRDOs was <40%.
Aerobic biodegradation has the advantage of achieving high
temperatures, which will destroy many pathogens that desiccation cannot
(3). In this study, aerobic biodegradation was rarely (if
ever) achieved for several reasons: (i) the heap's small mass was not
large enough to trap sufficient heat (heat buildup) to maintain the
high temperatures (40 to 60°C) required for aerobic thermophilic
bacterial growth, (ii) users did not regularly adjust the moisture
levels of the compost pile with water or soak materials (sawdust), and
(iii) users did not regularly adjust pile oxygen content by stirring or
turning over the pile.
The ideal C:N ratio for composting toilets is between 15:1 and 30:1
(5). Human excreta generally have a C:N ratio of 5:1 (8); therefore, a carbonaceous material (bulking agent or
soak material) must be added after each use to raise the carbon level. The C:N ratio was not problematic in this study, as participants faithfully added sawdust (perhaps too much) after using the facilities. Undoubtedly, they were motivated to do this as the carbonaceous material covered the waste, reduced odors, and lowered the prevalence of insects. The addition of soak material also aided in aerating the
compost heap by creating a coarse matrix, which allows for small air
pockets. On the other hand, too much soak will lower moisture content
below the optimum for aerobic biodegradation.
In the dry atmosphere of north-central Mexico, perhaps desiccation is
the best mechanism for dry sanitation. The alternative of maintaining
sufficient moisture content for biodegradation may not be practical and
achievable for the targeted population of dry-sanitation users. Study
limitations included missing cases due to the inability of
researchers to collect samples; thus, there were fewer 3-month
samples. Since SIRDO biosolid waste will not be tested on a
regular basis before disposal, it will not be possible to
determine classifications. Therefore, the recommendation for users is
that compost not be used before 6 months and that no 6-month compost
should be disposed on edible plants or in areas where persons could be
exposed via dust or direct contact.
 |
ACKNOWLEDGMENTS |
This work was supported by Center for Environmental Resource
Management grant ERC2K-R6 from the EPA and by a Border Biomedical Research Center grant from the National Institutes of Health.
 |
FOOTNOTES |
*
Corresponding author. Mailing address: Department of
Biological Sciences, University of Texas, El Paso, TX 79968. Phone:
(915) 747-6995. Fax: (915) 747-5808. E-mail:
thomasr{at}utep.edu.
 |
REFERENCES |
| 1.
|
Brown, L.
1997.
Who will feed China: wake-up call for a small planet. W. W.
Norton & Co., New York, N.Y.
|
| 2.
|
Clesceri, L. S.,
A. E. Greenberg, and A. Eaton (ed.).
1998.
Standard methods for the examination of water and wastewater, 20th ed.
American Public Health Association, Washington, D.C.
|
| 3.
|
del Porto, D., and C. Steinffeld.
1998.
The composting toilet system book.
Center for Ecological Pollution Prevention, Concord, N.H.
|
| 4.
|
Dutka, B.,
A. Chau, and J. Coburn.
1974.
Relationship between bacterial indicators of water pollution and fecal sterols.
Water Res.
8:1047-1055[CrossRef].
|
| 5.
|
Esrey, S.,
J. Gough,
D. Rapaport,
R. Sawyer,
M. Simpson-Hebert,
J. Vargas, and U. Windlad.
1998.
Ecological sanitation
Sida, Stockholm, Sweden.
|
| 6.
|
Geldreich, E.
1977.
Microbiology of water.
Water Pollut. Control Fed.
49:1222-1244.
|
| 7.
|
Geldreich, E.
1967.
Fecal coliform concepts in stream pollution.
Water Sewage Works
114:98-110.
|
| 8.
|
Harper, P., and L. Halestrap.
1999.
Lifting the lid.
Biddles, Ltd., London, England.
|
| 9.
|
Hosmer, D., and S. Lemeshow.
1989.
Applied logistic regression.
John Wiley & Sons, New York, N.Y.
|
| 10.
|
Jenkins, J.
1999.
The Humanure, 2nd ed.
Jenkins Publishing, Grove City, Pa.
|
| 11.
|
Stauffer, J.
1998.
The water crisis.
Earthscan Publications, Ltd., London, England.
|
| 12.
|
Stenstrom, T.
1996.
Water microbiology for the 21st century.
Stockholm Water Symposium, Stockholm, Sweden.
|
| 13.
|
Strandridge, J. H., and J. J. Delfino.
1981.
A-1 medium: alternative technique for fecal coliform organism enumeration in chlorinated wastewaters.
Appl. Environ. Microbiol.
42:918-920[Abstract/Free Full Text].
|
| 14.
|
United Nations Conference on Human Settlements.
1996.
Habitat II, dialogue III: water for thirsty cities.
United Nations Conference on Human Settlements, Istanbul, Turkey.
|
| 15.
|
United Nations Conference on Human Settlements.
1996.
Water crisis to strike most developing world cities by 2010. Habitat press release
United Nations Conference on Human Settlements, Nairobi, Kenya.
|
| 16.
|
U.S. Environmental Protection Agency.
1994.
A plain English guide to the EPA part 503 biosolids rule.
Office of Wastewater Management, U.S. Environmental Protection Agency, Washington, D.C.
|
Applied and Environmental Microbiology, September 2001, p. 4036-4040, Vol. 67, No. 9
0099-2240/01/$04.00+0 DOI: 10.1128/AEM.67.9.4036-4040.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.