Bioresource Technology 100 (2009) 5392–5394

Contents lists available at ScienceDirect

Bioresource Technology
journal homepage: www.elsevier.com/locate/biortech

Disinfection of animal manures, food safety and policy

Dean O. Cliver *
University of California, VM:PHR, 1 Shields Ave., Davis, CA 95616-8743, USA

a r t i c l e i n f o a b s t r a c t

Article history: Manure is a resource, but sometimes also a nuisance. Manure management strategies have traditionally
Received 5 June 2008 focused on soil nutrients (N, P, K), COD, and more recently biological substances (antibiotics, hormones,
Received in revised form 17 April 2009 etc.), with disinfection being a relative afterthought. Zoonotic pathogens (Salmonella and other bacteria,
Accepted 20 April 2009
protozoa, etc.) may be present in manure, but only occasionally cause foodborne disease. In countries
Available online 17 May 2009
where food is relatively safe, requiring heroic manure disinfection measures may be a net detriment to
public health. Decisions that a new, elegant disinfection technology can, should, or must be done may
Keywords:
result from invoking the ‘‘precautionary principle.” Additional capital and operating costs must be passed
Biodegradation
Disinfection
to the consumer. Since such measures are likely to prevent very few human illnesses, policymakers
Foodborne disease should also consider the effect of increased prices on human nutrition and hunger. In most situations,
Manure not eating is more dangerous than eating.
Zoonotic pathogens Ó 2009 Elsevier Ltd. All rights reserved.

1. Introduction lamblia, are sometimes mentioned (Dubey et al., 2006; Fayer,

This review will consider the risks of manure-borne zoonoses to
public health via the food supply and address policy-based strate-
gies for mitigating threats to food safety. It does not undertake to
define ‘‘manure” rigorously, to select the zoonotic pathogens of
concern, nor specifically to review potentially pertinent disinfec-
tion technologies. Finding scientific bases for policies in this domain
represents a considerable challenge in itself.
2. Manure and pathogens
Excrement from any farm animal may be called ‘‘manure.”
How it is handled after it leaves the animal can vary widely
(admixture of bedding, dilution with water, drying, composting,
lagooning, etc.) and will greatly affect what can be done to disin-
fect it. The zoonotic pathogens associated with manure vary with
the source-animal species. Most of the pathogens of concern are
bacteria: Salmonella presents the broadest-spectrum risk, but
enterohemorrhagic E. coli (EHEC) (Fratamico and Smith, 2006),
Campylobacter (Altekruse and Perez-Perez, 2006), Leptospira (Haj-
meer and Fung, 2006), and Yersinia (Niesbakken, 2006) are also
significant threats associated with the waste of certain food ani-
mals. In less-developed countries, Mycobacterium and Brucella
spp. have also to be considered (Hajmeer and Fung, 2006).
Threats from the protozoa, Cryptosporidium spp. and Giardia
* Tel.: +1 530 759 9459; fax: +1 530 752 5845.
E-mail address: docliver@ucdavis.edu
2004). Although livestock harbor a wide variety of viruses, few
of these are apparently transmissible to humans (Cliver and
Moe, 2004).
3. Impacts on food safety
It is possible that EHEC present in manure matted in the hair of
cattle going to slaughter is as likely a source of contamination as
their intestinal contents (Elder et al., 2000). However, zoonoses
are most likely to contaminate food when manure is used as a soil
amendment or when manure contaminates water that is later used
for irrigation or comes in contact with food (Cotruvo et al., 2004).
The soil amendment and irrigation routes are of particular concern
in the production of leafy vegetables eaten raw. Water used in
washing such vegetables, as well as other foods, can also present
a risk.
Leafy green vegetables have attracted a great deal of attention
of late, due to some spectacular outbreaks in which they served
as vehicles (Cooley et al., 2007). When the agent in the outbreak
is EHEC or Salmonella, it is reasonable to suppose that manure
has had a role in contamination; however, a report given at a re-
cent Centers for Disease Control and Prevention (CDC) conference
states that 58.3% of leafy-greens outbreaks reported in the US,
1973–2006, were solely caused by noroviruses (Herman et al.,
2008). In norovirus outbreaks, it is most likely that the source of
contamination is human, rather than animal (Cliver et al., 2006).
EHEC (Fratamico and Smith, 2006) and Salmonella (Mølbak et al.,
2006) may sometimes be of human, rather than animal, origin;

0960-8524/$ - see front matter Ó 2009 Elsevier Ltd. All rights reserved.
doi:10.1016/j.biortech.2009.04.038
 D.O. Cliver / Bioresource Technology 100 (2009) 5392–5394
and a recent publication states that strains of Salmonella isolated
from ill humans often differ from those associated with animals
(Heithoff et al., 2008). Application of genetic ‘‘fingerprinting” tech-
niques has had a great impact on attributions in foodborne disease,
in that it helps identify remote sources of contamination (Tauxe,
2006).
Clearly, the proportion of foodborne or waterborne disease that
results from contamination with farm animal manure is not well
established (Reilly and Browning, 2004). Outbreaks from this al-
leged source receive a great deal of publicity, but risk assessments
needed to provide an accurate perspective have still to be done
(Lammerding and Todd, 2006; McBride, 2004). The infamous
Walkerton, Canada outbreak of EHEC transmitted via drinking
water clearly derived from cattle, but could hardly have been
blamed primarily on a need for manure disinfection (Mølbak and
Scheutz, 2004).
4. Prevention
The obvious approach to preventing pathogens in manure from
contaminating food or water is to eliminate the pathogens from
their animal reservoirs. Means to this end are, unfortunately, not
yet in hand (Gannon, 2004), though considerable progress has been
made in the elimination of Salmonella in on-farm poultry and
swine in some parts of Europe. The levels of organization and ded-
ication required for this are unlikely to be found in the US.
Methods of treating manure to kill pathogens (disinfection) are
available – most prominently, composting of solid waste and lago-
oning of liquid waste. These and other methods are certainly use-
ful, but are subject to variable outcomes and may be costly
(Gannon et al., 2004; Hill, 2003); however, our studies have shown
that bacteria in swine and dairy-cattle waste are able to attack
viruses (Deng and Cliver, 1992a, 1995a) and protozoan cysts (Deng
and Cliver, 1992b, 1994a,b) and oocysts (Deng et al., 2001); such
bacteria were not found in septic tank effluent containing human
waste (Deng and Cliver, 1995a,b). The persistence of bacterial
pathogens in manure or manure slurries is a function of time and
temperature; aeration encourages the action of other microbes
that adversely affect the pathogens (Derbyshire and Brown,
1979). Chemical and physical disinfection treatments tend to be
more costly. Some of the non-microbial residues in manure may
present greater threats to the environment than microbial patho-
gens, in that they resist biodegradation (Tarver, 2008).
5. Public health perspective
The public perceives food safety as absolute, but there are de-
grees of safety (Applebaum et al., 2002), which is why the food
industry prefers the word ‘‘quality.” Activists in the US demand a
zero-risk food supply and claim that cost should not be a consider-
ation. However, costs and availability of food are a significant con-
sideration in the US, as in the rest of the world. A frequently cited
overview from CDC estimates that foodborne diseases cause 5000
deaths in the US each year (Mead et al., 1999); however, reported
annual numbers of deaths from foodborne disease have not ex-
ceeded 100 (CDC, 2006). In contrast, CDC statistics for US deaths
from malnutrition in 2003 gave a total >3000 [National Center
for Health Statistics Data Warehouse <http://www.cdc.gov/nchs/
data/dvs/mortfinal2003_workipt1.pdf>]. At a time when many
people are inadequately fed, insistence on absolute food safety is
likely to be a net detriment to public health. As one looks at the
world, it is clear that not eating is more dangerous than eating.
Manure is a byproduct of food production that can be used to
produce more food. As such, its resource value should not be
underestimated. In much of the world, manure is an essential fac-
5393
tor in agricultural production. It may be applied to land at exces-
sive rates, but the consequences of this are seldom as dire as of
the application of excessive amounts of chemical fertilizers. How-
ever, the major plant nutrients – N, P, and K – are pollutants if
excessive levels contaminate water. N seems more likely to be a
problem in groundwater, whereas P is most problematic in surface
water. ‘‘Manure handling” recommendations and regulations tend
to focus on these elements (CAST, 1995); but the other, biological
products (antibiotics, hormones, etc.) of animal agriculture are
increasingly being recognized as water contaminants (Tarver,
2008). Neither N, P, nor biologicals are likely to be controlled by
disinfection methods; but rigorous containment or removal of N,
P, or biologicals may contribute to pathogen reduction. In most re-
spects, disinfection is apparently an afterthought.
In a time when the world’s population is growing and an increas-
ing proportion of humanity is living in cities with no option of pro-
ducing their own food, the challenge of feeding these multitudes
has fallen on a smaller portion of the population, who are obliged
to apply economies of scale to produce needed food at affordable
prices. This is being accomplished; the quantities of food produced
worldwide are said to be adequate, but problems of distributing
food to the hungriest people have yet to be solved (Ehrlich and Ehr-
lich, 1990). Intensive food production practices, such as concen-
trated animal feeding operations (CAFOs), have enabled
economical production of large quantities of animal protein. The
distribution problem is exacerbated, however, in that the vast quan-
tities of product do not lend themselves to sale to consumers at the
farm gate. The other drawback of CAFOs is that their areas are too
small to absorb the large quantities of animal waste they yield.
However, if disinfection is to be applied, the large quantity of waste
to be treated will partly mitigate the capital cost of the necessary
treatment facilities. Both the capital cost and operating expenses
will need to be passed on to the consumer, thus somewhat dimin-
ishing the erstwhile economies of scale. The extent to which these
added expenses enhance food safety is, or should be, a key question.
In the infamous 2006 outbreak of EHEC infections from baby
spinach, there were, clearly, cattle in the area, shedding the out-
break strain (Cooley et al., 2007). However, the manner in which
the EHEC got from cattle to the spinach field could not be deter-
mined, in spite of intensive investigation. Water was a possible
means of conveyance, as were the numerous feral swine in the
area, which were shown to be shedding the agent (Jay et al.,
2007). The swine forced access to the cattle area and to the spin-
ach-growing field; they may not merit the term ‘‘wildlife,” but they
are clearly free-ranging and have successfully colonized much of
the state of California. Methods for keeping these swine completely
out of cattle pens and pastures and of fields growing leafy green
vegetables are being sought that have not yet been identified. This
may seem a special case, but California produces one-third of the
US food supply, and programs that focus entirely on food-animal
waste without regard to feral swine droppings may well fall short
in protecting public health.
6. Policy
An official of the US EPA has pointed out that there is regulatory
parity in the perceived threat of human and animal waste in water;
this results from a lack of data to feed quantitative risk assess-
ments (Schaub, 2004). If needed data were in hand, the risk assess-
ment methods with which to apply them are reasonably well
established (Lammerding and Todd, 2006; McBride, 2004). Unfor-
tunately, formal, full-scale risk assessments consume much time
and resources, so it becomes expedient to apply the so-called pre-
cautionary principle. This entails generating a politically viable and
expedient course of action that does not depend strongly on estab-
5394 D.O. Cliver / Bioresource Technology 100 (2009) 5392–5394
lished fact. Options as to what can, should, or must be done are
weighed by the executive, and perhaps legislative, branches of gov-
ernment. The electorate may be consulted, and the electorate may
even demand priority in the decision-making process. Often, the
judicial branch is obliged to arbitrate. In the US, the federal and
state governments are confronted by a broad spectrum of political
and technical orientations and priorities, further complicated by an
antipathy for rules in general, in such cases. Many other govern-
ments seem to have an easier time making rules, but the rules
do not necessarily have a more valid scientific basis. Where inter-
national rule-making is involved, the European Union appears to
have evolved a relatively orderly mechanism, though the outcome
may not be any more favorable. One might wish that agencies of
the United Nations were empowered in similar fashion.
7. Conclusions
Food in the developed world seldom injures the consumer.
Heroic measures to achieve small further increments of safety
are likely to increase food insecurity and malnutrition, to the net
detriment of public health. Manure is a resource to be treated with
respect. Pathogens from manure are responsible for only a small
proportion of foodborne disease, and some other contaminants
may be more difficult to eliminate. Preventive measures should
be implemented based on quantitative risk assessments comparing
the impacts of alternate courses of action, both on those who eat
the impacted food and on those who may not get to eat.
References
Altekruse, S.F., Perez-Perez, G.I., 2006. Campylobacter jejuni and related pathogens.
In: Riemann, H.P., Cliver, D.O. (Eds.), Foodborne Infections and Intoxications,
third ed. Academic Press (Elsevier), London, Amsterdam, pp. 259–287.
Applebaum, R., Bernard, D.T., Scott, V.N., 2002. Organizing a safe food supply
system. In: Cliver, D.O., Riemann, H.P. (Eds.), Foodborne Diseases, second ed.
Academic Press, London, pp. 353–374.
CAST, 1995. Waste Management and Utilization in Food Production and Processing.
Council for Agricultural Science and Technology, Ames, Iowa.
CDC, 2006. Surveillance for Foodborne-Disease Outbreaks – United States, 1998–
2002. Surveillance Summaries 55.
Cliver, D.O., Moe, C.L., 2004. Prospects of waterborne viral zoonoses. In: Cotruvo,
J.A., Dufour, A., Rees, G., Bartram, J., Carr, R., Cliver, D.O., Craun, G.F., Fayer, R.,
Gannon, V.P.J. (Eds.), Waterborne Zoonoses: Identification, Causes and Control.
IWA (International Water Association) Publishing, London, pp. 242–254.
Cliver, D.O., Matsui, S.M., Casteel, M., 2006. Infections with viruses and prions. In:
Riemann, H.P., Cliver, D.O. (Eds.), Foodborne Infections and Intoxications, third
ed. Academic Press (Elsevier), London, Amsterdam, pp. 367–448.
Cooley, M., Carychao, D., Crawford-Miksza, L., Jay, M.T., Myers, C., Rose, C., Keys, C.,
Farrar, J., Mandrell, R.E., 2007. Incidence and tracking of Escherichia coli
O157:H7 in a major produce production region in California. PLoS ONE 2, e1159.
Cotruvo, J.A., Dufour, A., Rees, G., Bartram, J., Carr, R., Cliver, D.O., Craun, G.F., Fayer,
R., Gannon, V.P.J. (Eds.), 2004. Waterborne Zoonoses: Identification, Causes and
Control. IWA (International Water Association) Publishing, London.
Deng, M.Y., Cliver, D.O., 1992a. Inactivation of poliovirus type 1 in mixed human
and swine wastes and by bacteria from swine manure. Appl. Environ. Microbiol.
58, 2016–2021.
Deng, M.Y., Cliver, D.O., 1992b. Degradation of Giardia lamblia cysts in mixed human
and swine wastes. Appl. Environ. Microbiol. 58, 2368–2674.
Deng, M.Y., Cliver, D.O., 1994a. LVSEM morphology of Giardia lamblia cysts as
related to viability determined by fluorogenic dye staining. Midwest
Microscopy 23, 24–32.
Deng, M.Y., Cliver, D.O., 1994b. Mixed waste studies with viruses and Giardia, in:
Collins, E.E. (Ed.), On-Site Wastewater Treatment. Proceedings of the Seventh
International Symposium on Individual and Small Community Sewage Systems.
Dec. 11–13, 1994. Atlanta, GA, pp. 573–578.
Deng, M.Y., Cliver, D.O., 1995a. Antiviral effects of bacteria isolated from manure.
Microb. Ecol. 30, 43–45.
Deng, M.Y., Cliver, D.O., 1995b. Persistence of inoculated hepatitis A virus in mixed
human and human wastes. Appl. Environ. Microbiol. 61, 87–91.
Deng, M., Nuanualsuwan, S., Cliver, D.O., 2001. Inactivation of Cryptosporidium
parvum oocysts by bacterial strains. J. Eukary. Microbiol. (Suppl.), 37S–39S.
Derbyshire, J.B., Brown, E.G., 1979. The inactivation of viruses in cattle and pig
slurry by aeration or treatment with calcium hydroxide. J. Hyg. (London) 82,
293–299.
Dubey, J.P., Murrell, K.D., Cross, J.H., 2006. Foodborne parasites. In: Riemann, H.P.,
Cliver, D.O. (Eds.), Foodborne Infections and Intoxications, third ed. Academic
Press (Elsevier), London, Amsterdam, pp. 449–481.
Ehrlich, P.R., Ehrlich, A.H., 1990. The population explosion. Why isn’t everyone as
scared as we are? Amic. J. 12, 22–29.
Elder, R.O., Keen, J.E., Siragusa, G.R., Barkocy-Gallagher, G.A., Koohmaraie, M.,
Laegreid, W.W., 2000. Correlation of enterohemorrhagic Escherichia coli O157
prevalence in feces, hides, and carcasses of beef cattle during processing. Proc.
Natl. Acad. Sci. USA 97, 2999–3003.
Fayer, R., 2004. Waterborne zoonotic protozoa. In: Cotruvo, J.A., Dufour, A., Rees, G.,
Bartram, J., Carr, R., Cliver, D.O., Craun, G.F., Fayer, R., Gannon, V.P.J. (Eds.),
Waterborne Zoonoses: Identification, Causes and Control. IWA (International
Water Association) Publishing, London, pp. 255–282.
Fratamico, P.M., Smith, J.L., 2006. Escherichia coli. In: Riemann, H.P., Cliver, D.O.
(Eds.), Foodborne Infections and Intoxications, third ed. Academic Press
(Elsevier), London, Amsterdam, pp. 205–258.
Gannon, V.P.J., 2004. Control of zoonotic waterborne pathogens in animal
reservoirs. In: Cotruvo, J.A., Dufour, A., Rees, G., Bartram, J., Carr, R., Cliver,
D.O., Craun, G.F., Fayer, R., Gannon, V.P.J. (Eds.), Waterborne Zoonoses:
Identification, Causes and Control. IWA (International Water Association)
Publishing, London, pp. 380–408.
Gannon, V.P., Humenik, F., Rice, M., Cicmanec, J.L., Smith Jr., J.E., Carr, R., 2004.
Control of zoonotic pathogens in animal wastes. In: Cotruvo, J.A., Dufour, A.,
Rees, G., Bartram, J., Carr, R., Cliver, D.O., Craun, G.F., Fayer, R., Gannon, V.P.J.
(Eds.), Waterborne Zoonoses: Identification, Causes and Control. IWA
(International Water Association) Publishing, London, pp. 409–425.
Hajmeer, M.N., Fung, D.Y.C., 2006. Infections with other bacteria. In: Riemann, H.P.,
Cliver, D.O. (Eds.), Foodborne Infections and Intoxications, third ed. Academic
Press (Elsevier), London, Amsterdam, pp. 341–365.
Heithoff, D.M., Shimp, W.R., Lau, P.W., Badie, G., Enioutina, E.Y., Daynes, R.A., Byrne,
B.A., House, J.K., Mahan, M.J., 2008. Human Salmonella clinical isolates distinct
from those of animal origin. Appl. Environ. Microbiol. 74, 1757–1766.
Herman, K.M., Ayers, T.L., Lynch, M. 2008. Foodborne disease outbreaks associated
with leafy greens, 1973–2006. Presented at the International Conference on
Emerging Infectious Diseases 2008, Atlanta, Georgia.
Hill, V.R., 2003. Prospects for pathogen reductions in livestock wastewaters: a
review. Crit. Rev. Environ. Sci. Technol. 33, 187–235.
Jay, M.T., Cooley, M., Carychao, D., Wiscomb, G.W., Sweitzer, R.A., Crawford-Miksza,
L., Farrar, J.A., Lau, D.K., O’Connell, J., Millington, A., Asmundson, R.V., Atwill, E.R.,
Mandrell, R.E., 2007. Escherichia coli O157:H7 in feral swine near spinach fields
and cattle, central California coast. Emerg. Infect. Dis. 13, 1908–1911.
Lammerding, A.M., Todd, E.C.D., 2006. Microbial food safety risk assessment. In:
Riemann, H.P., Cliver, D.O. (Eds.), Foodborne Infections and Intoxications, third
ed. Academic Press (Elsevier), London, Amsterdam, pp. 27–53.
McBride, G.B., 2004. Quantitative microbial risk assessment issues. In: Cotruvo, J.A.,
Dufour, A., Rees, G., Bartram, J., Carr, R., Cliver, D.O., Craun, G.F., Fayer, R.,
Gannon, V.P.J. (Eds.), Waterborne Zoonoses: Identification, Causes and Control.
IWA (International Water Association) Publishing, London, pp. 460–
470.
Mead, P.S., Slutsker, L., Dietz, V., McCaig, L.F., Bresee, J.S., Shapiro, C., Griffin, P.M.,
Tauxe, R.V., 1999. Food-related illness and death in the United States. Emerg.
Infect. Dis. 5, 607–625.
Mølbak, K., Scheutz, F., 2004. Verocytotoxin-producing Escherichia coli and other
diarrhoeagenic E. coli. In: Cotruvo, J.A., Dufour, A., Rees, G., Bartram, J., Carr, R.,
Cliver, D.O., Craun, G.F., Fayer, R., Gannon, V.P.J. (Eds.), Waterborne Zoonoses:
Identification, Causes and Control. IWA (International Water Association)
Publishing, London, pp. 213–227.
Mølbak, K., Olsen, J.E., Wegener, H.C., 2006. Salmonella infections. In: Riemann, H.P.,
Cliver, D.O. (Eds.), Foodborne Infections and Intoxications, third ed. Academic
Press (Elsevier), London, Amsterdam, pp. 57–136.
Niesbakken, T., 2006. Yersinia infections. In: Riemann, H.P., Cliver, D.O. (Eds.),
Foodborne Infections and Intoxications, third ed. Academic Press (Elsevier),
London, Amsterdam, pp. 289–312.
Reilly, W.J., Browning, L.M., 2004. Zoonoses in Scotland — food, water, or contact?
In: Cotruvo, J.A., Dufour, A., Rees, G., Bartram, J., Carr, R., Cliver, D.O., Craun, G.F.,
Fayer, R., Gannon, V.P.J. (Eds.), Waterborne Zoonoses: Identification, Causes and
Control. IWA (International Water Association) Publishing, London, pp. 167–
190.
Schaub, S.A., 2004. A regulatory perspective on zoonotic pathogens in water. In:
Cotruvo, J.A., Dufour, A., Rees, G., Bartram, J., Carr, R., Cliver, D.O., Craun, G.F.,
Fayer, R., Gannon, V.P.J. (Eds.), Waterborne Zoonoses: Identification, Causes and
Control. IWA (International Water Association) Publishing, London, pp. 439–
451.
Tarver, T., 2008. ‘‘Just add water”: regulating and protecting the most common
ingredient. J. Food Prot. 73, R1–R13.
Tauxe, R.V., 2006. Molecular subtyping and the transformation of public health.
Foodborne Pathog. Dis. 3, 4–8.