Journal of Applied Microbiology 2001, 90, 68S±79S
Campylobacters in water, sewage and the environment
K. Jones
Department of Biological Sciences, IENS, Lancaster University, Lancaster, UK
1.
2.
3.
4.
Summary, 68S
Introduction, 68S
Campylobacters in water, 68S
3.1 Fresh water, 69S
3.1.1 Streams, 69S
3.1.2 Rivers, 69S
3.1.3 Canals, 70S
3.1.4 Ponds and ornamental lakes, 70S
3.1.5 Groundwater, 70S
3.1.6 Reservoirs, 70S
3.1.7 Drinking water, 70S
3.2 Marine, 71S
3.2.1 Coastal waters/bathing waters and
sediment, 71S
3.2.2 campylobacters for coastal bathing
waters, 71S
3.2.3 Estuaries, 71S
Campylobacters in sewage, 72S
4.1 Sewage treatment, 72S
4.2 Effects of sewage ef¯uent on receiving surface
waters, 72S
1. SUMMARY
Thermophilic campylobacters are widespread in the environment, where they are a sign of recent contamination with
animal and avian faeces, agricultural run-off and sewage
ef¯uent. Although intestinal carriage of campylobacters is
ubiquitous in livestock, domestic animals, wild animals, wild
birds and poultry, contamination of the environment with
the bacteria in faeces is intermittent and varies seasonally,
depending on factors such as stress and changes in diet.
Wild birds, and not sewage ef¯uent, are the source of
campylobacters in some coastal waters. The density of
Campylobacter spp. in sewage ef¯uent depends on the source
of the sewage and the type of treatment. There is a
qualitative, but not a quantitative, correlation between
campylobacters and faecal indicators in environmental
samples. The marked seasonal pattern of campylobacters
Correspondence to: K. Jones, Department of Biological Sciences, IENS,
Lancaster University, Lancaster, LA1 4YQ, UK
(e-mail: k.jones@lancaster.ac.uk).
4.3
5.
6.
7.
8.
9.
10.
Sewage sludge, 72S
4.3.1 Sewage sludge put to land, 73S
Correlation with faecal indicators, 73S
Miscellaneous aspects of survival, 73S
6.1 Protection in bio®lms, 74S
6.2 Viable but non-culturable Campylobacter, 74S
6.3 Survival of an infective dose, 74S
Environmental loading and seasonality, 74S
7.1 The farm as an environmental reservoir of
infection, 74S
7.2 Shedding of campylobacters in faeces of
livestock, 74S
7.3 Campylobacters in farm waste, 75S
7.4 Wild animals, wild birds and pets, 75S
7.5 Are campylobacter strains found in the environment important?, 75S
Conclusions, 76S
Acknowledgements, 76S
References, 76S
in temperate, aquatic environments is a result of variations
in Campylobacter die-off rates at different times of the
year.
2. INTRODUCTION
The presence of campylobacters in environmental samples
can be taken as a sign of recent faecal contamination, because
not only are campylobacters unable to multiply outside
warm-blooded host animals, they also survive for a shorter
time than the usual indicators, faecal coliforms and faecal
streptococci (Bolton et al. 1987; Korhonen and Martikainen
1991; Wallace et al. 1993; Koenraad et al. 1997; ObiriDanso and Jones 1999a).
3. CAMPYLOBACTERS IN WATER
The incidence of enteritis caused by thermophilic campylobacters has the hallmarks of a waterborne disease, in that
there is a major spring peak followed by a trough in the
summer and a small peak in autumn. However, this is not
backed up by quantitative studies of surface waters, where
ã 2001 The Society for Applied Microbiology
CAMPYLOBACTERS IN THE ENVIRONMENT
1
numbers are higher in the winter than in the summer
(Fig. 1).
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Table 1 Examples of event-led and location-led agricultural contamination of streams with Campylobacter
Number of campylobacters per 100 ml
3.1. Fresh water
3.1.1. Streams. The presence of thermophilic campylobacters in streams varies with location, season and agricultural
practice. Studies of streams in north-west England have
shown that campylobacters are absent from streams running
through upland moors but present in the same streams
running through lowland, grazed pasture (Jones et al. 1990a;
Jones and Hobbs 1996). The composition of the Campylobacter population is dependent on the path of the stream
(Obiri-Danso and Jones 1999a). Streams running through
pasture contain mainly C. jejuni with some C. coli, shed by
grazing cattle (Stanley et al. 1998c) and sheep (Stanley et al.
1998d; Jones et al. 1999b), whereas those draining duck
ponds contained a mixture of C. jejuni, C. lari, C. coli and
urease-positive thermophilic campylobacters (UPTCs),
which are typical of avian sources. A further study showed
that campylobacters occurred intermittently in streams, with
their density correlating with upstream agricultural locations
2 (Table 1), such as farmyards, small-holdings and a slaughterhouse, and agricultural events, such as emptying of slurry
tanks and the spraying of farm slurry onto land (Jones and
Hobbs 1996; Stanley et al. 1998b). These observations
con®rm the generally held view that agricultural slurries,
manure and municipal sewage following land disposal, or
unintentional leakage from sewers, farm stockpiles or slurry
holding pits, are the primary sources of contamination of
streams with microorganisms of public health concern (Goss
and Barry 1995; Watson 1985).
Upstream
Downstream
Small holding
Cattle market
Cleaning slurry tank
Slurry spraying
5
8
4
20
86
36
141
160
A detailed study of the river Conder (north-west England)
showed that the upper, cleaner reaches of the river were free
of Campylobacter but, as the water ¯owed through grazed
farmland, it became progressively more contaminated with
campylobacters, particularly C. jejuni (Fig. 2.) (Jones et al.
1990a; Jones and Hobbs 1996). A 2-year survey of two
inland recreational waters on the river Lune in the same
geographical area (Obiri-Danso and Jones 1999a) con®rmed
the results reported by Bolton et al. (1987) and Jones et al.
(1990a) which showed that campylobacters were present all
year round, but with lower numbers in the summer
corresponding to elevated UV levels and higher temperatures. Sources of Campylobacter contamination for the Lune
included: sewage ef¯uent from a small waste water treatment
works (secondary treatment by trickle ®ltration), streams
containing agricultural run-off, sheep and cattle grazing
meadows bordering the river and an indigenous population
of ducks. C. jejuni was the predominant species isolated;
however, the presence of C. lari, C. coli and UPTCs is
indicative of a range of sources. There was little diurnal
variation (numbers did not decline during the day), which
re¯ects the diverse and continuous nature of the inputs. The
river sediments showed the same distribution of species but
the numbers remained constant throughout the year,
showing no seasonality. A study of rivers and lakes in the
Warsaw region of Poland showed that 70% of water samples
were positive for thermotolerant Campylobacter with C. jejuni
making up 65% of the isolates, C. coli 22% and C. lari 13%.
–1
3.1.2. Rivers. Thermophilic campylobacters are ubiquitous in rivers, especially those exposed to agricultural run-off
and ef¯uent from water treatment plants (Bolton et al. 1987;
3 Jones et al. 1990a; Stelzer et al. 1991; Jones and Hobbs
1996; Popowski et al. 1997; Obiri-Danso and Jones 1999a).
Location/Event
Fig. 1 Negative correlation between hours of sunshine (n) and
campylobacter numbers in Morecambe Bay (black columns) and the
Lune estuary (white columns)
Fig. 2 Increase in the density of campylobacters in the river Conder
from freshwater source to estuary
ã 2001 The Society for Applied Microbiology, Journal of Applied Microbiology Symposium Supplement, 90, 68S±79S
70S K . J O N E S
Municipal sewage was stated to be the main source, with
minor inputs from the droppings of wild animals (Popowski
et al. 1997).
3.1.3. Canals. The Lancaster canal in north-west England
contains low numbers of campylobacters. Their density
peaks in the winter and contamination originates from
streams, run-off from pasture and ducks (Jones et al. 1990a).
3.1.4. Ponds and ornamental lakes. Ponds and ornamental lakes, such as the Serpentine in Hyde Park, London,
can be of poor microbiological quality and are rich sources of
campylobacters, which are shed by the large populations of
ducks and wildfowl. For example, water samples taken from
a small lake at Lancaster University contained between 23
and 430 campylobacters per 100 ml of water, and 30% of
faecal samples, shed by a variety of ducks, waterfowl and
peacocks, were positive for Campylobacter. Faecal samples
from mallard ducks (Anas platyrhinchos) contained between
1á6 ´ 106 and 2á7 ´ 107 campylobacters per g dry weight,
and of the 82 isolates, 90% were C. jejuni, 7% C. coli and
3% UPTCs.
3.1.5. Groundwater. Groundwater is widely considered
to be microbiologically clean. It rises to the surface at
boreholes, wells, springs or seeps and is frequently used for
drinking water for livestock on farms. Contaminated
groundwater sources have been implicated in the introduction of Campylobacter into poultry ¯ocks (Pearson et al.
1993) and broiler chickens (VandeGiessen et al. 1996).
However, the ®rst culturable evidence that Campylobacter
can occur in groundwater was provided by Stanley et al.
(1998a). Hydrological evidence suggested that the source of
contamination was a dairy farm situated within the
hydrological catchment of the groundwater, and this was
con®rmed when identical strains of C. jejuni were isolated
from groundwater and the dairy herd. The ability to
culture Campylobacter from these aquifers suggests that the
vertical movement of this organism may signi®cantly
threaten the quality of subsurface aquifers and supports
the conclusions of Rollins (1991) and Pearson et al. (1993),
that contaminated groundwater may be an overlooked
source of campylobacters in animals reared for food. The
environmental conditions found within subsurface aquifers,
i.e. low redox potentials, the absence of molecular oxygen
with increasing depth, all year round low temperatures and
protection from the effects of UV and desiccation, favour
the survival of Campylobacter. Since similar conditions
occur in large aquifers delivering water to cities, it is
possible that these could be a vehicle for the transmission
of campylobacters shed by sheep and birds, as was recently
the case with Cryptosporidium in north-west England (Anon
1999).
3.1.6. Reservoirs. There are reports from Holland that
Campylobacter originating from birds was detected in
pristine reservoirs, but only in winter months (Medema
and Schets 1994). In the most pristine reservoirs, Campylobacter numbers were similar to those for Escherichia coli.
Similar observations were made for impounding reservoirs
in north-west England (Jones et al. 1990a; Jones et al.
1999a), where campylobacters were absent in late spring and
early summer but present in relatively large numbers in
winter. Phenotypic pro®ling was used to trace the origin of
the bacteria from three suspect sources, sheep and Canada
geese grazing the edge of the reservoir and a colony of
black-headed gulls roosting on an island. The sheep and
Canada geese excreted only C. jejuni whereas the blackheaded gulls excreted C. jejuni, C. lari, C. coli and UPTCs,
which matched the pro®le of species found in the water
column.
3.1.7. Drinking water. The numbers of sporadic infections
and outbreaks of Campylobacter enteritis caused by drinking
water have recently been reviewed (Koenraad et al. 1997;
Thomas et al. 1999). World wide, Koenraad et al. (1997)
reported nine outbreaks between 1978 and 1991, each
affecting between 13 and 3000 people; Thomas et al. (1999)
reported a further seven outbreaks between 1990 and 1997,
affecting between 8 and 633 people. They predominantly
arose from consumption of untreated or contaminated water.
This appears to be a particular problem in Scandinavian
countries (Aho et al. 1989), where there is, apparently, a
divine right to drink from streams which appear to be clean
(Gunnarsson, pers. comm.). Koenraad et al. (1997) state that
exposure to contaminated water causes between 1á2 and 170
Campylobacter infections per 100 000 people. In the UK,
data on waterborne disease and water are collated by the
PHLS Communicable Disease Surveillance Centre and
published twice yearly in the Communicable Disease Report
(Anon 2000). Their results show that outbreaks of Campylobacter enteritis derived from drinking water are con®ned to
private water supplies, although the association between
disease symptoms and Campylobacter is frequently `probable' as the bacterium is seldom isolated from the water
source. Such private water supplies are predominantly
found in small rural systems which are more likely to be
contaminated with animal waste (Wyn-Jones 2000). MeÂg4 raud and Serceau (1990) surveyed the water distribution
network of a large urban community in France and were
unable to ®nd thermophilic campylobacters. Of the 14 nonthermophilic strains isolated, 13 came from untreated water
5 and all were sensitive to chlorination. Hanninen et al. (1998)
demonstrated that dairy cows shed more campylobacters in
the summer, when the cattle were drinking lake water, than
in the winter, when they were provided with chlorinated
mains water. However, a similar indoor/outdoor pattern was
ã 2001 The Society for Applied Microbiology, Journal of Applied Microbiology Symposium Supplement, 90, 68S±79S
CAMPYLOBACTERS IN THE ENVIRONMENT
1
not detected in a study of dairy and beef cattle in north-west
England (Stanley et al. 1998c).
Campylobacters have been shown to be widespread in
surface waters in Kumasi, Ghana. Interestingly, samples of
drinking water taken from a water hole in the early morning
contained campylobacters, whereas samples taken in the late
afternoon did not, presumably due to the biocidal effects of
high temperatures and elevated levels of UV radiation
(Adjei, pers. comm.).
3.2. Marine
3.2.1. Coastal waters/bathing waters and sediment.
Studies carried out in Morecambe Bay (north-west England) show that campylobacters are widespread in coastal
water (Jones et al. 1990a; Obiri-Danso and Jones 1999b),
where they show a distinct seasonal variation, i.e. they are
more numerous in the winter and either absent or present
in only low numbers in the summer (Fig. 1). In the bathing
season (May to September) campylobacters exhibited
diurnal variation, i.e. seawater samples were positive for
campylobacters in the early morning and negative in the
late afternoon (Obiri-Danso et al. 1999). Both the seasonal
distribution and the diurnal variation showed statistically
signi®cant correlations with the levels of UV radiation and
changes in temperature (Jones et al. 1990a, 1991; ObiriDanso and Jones 1999b; Obiri-Danso et al. 1999, 2001).
The predominant Campylobacter spp. found in Morecambe
Bay seawater were C. lari and UPTC (Obiri-Danso and
Jones 1999b). A recent study, using natural populations,
showed that C. lari and UPTCs survived for longer in
seawater than either C. jejuni or C. coli (Obiri-Danso et al.
2001).
Thermophilic campylobacters were also found in the
surface layer of the intertidal sediments in Morecambe Bay,
where they displayed similar seasonal patterns and species
composition (C. lari and UPTC) to those in the overlying
sea water (Obiri-Danso and Jones 2000). However, Bolton
et al. (1999) compared Campylobacter contamination of sand
on EEC standard and non-standard bathing beaches, and
showed that campylobacters could be isolated from 50% of
sand samples from non-EEC standard beaches and 40%
from EEC standard beaches, with C. jejuni and C. coli more
prevalent on non-EEC standard beaches and C. lari and
UPTC on EEC standard beaches.
3.2.2. Sources of campylobacters for coastal bathing
waters. It had been assumed that the main source of
campylobacters for bathing waters was sewage ef¯uent, even
though the bacteria in ef¯uent survived for only a short time
at ambient temperatures in seawater (Jones et al. 1990a, b).
The introduction of a waste water treatment works
(WWTW) at Morecambe in north-west England provided
71S
an opportunity to test whether this assumption was valid.
Prior to 1997, Morecambe's sewage had been macerated and
discharged via a short sea outfall into the ebb tide. After
1997 the sewage was subject to secondary treatment and
discharged via a long sea outfall several miles south of the
original outfall. Seawater samples were taken twice monthly
for a year both before and after the treatment plant came
on-line, and tested for thermophilic campylobacters and
faecal indicators. The introduction of sewage treatment
resulted in a reduction in the density of faecal indicators in
the bathing waters but not in the density of campylobacters
(Obiri-Danso and Jones 1999a). It has also been shown that
the species composition of campylobacters in the seawater
and sediments of Morecambe Bay is made up of 20±40%
C. lari and 60±80% UPTC, whereas in sewage ef¯uent it
consists of 83% C. jejuni and 17% C. coli (Jones et al. 1999b;
6 Obiri-Danso and Jones 1999c, 2000). As Morecambe Bay
supports large ¯ocks of wild birds such as oystercatchers,
knots and various types of gull, which excrete large numbers
of Campylobacter with the same pro®le of species (C. lari and
UPTC) found in the seawater and sediments (Jones et al.
1998; Fitzgerald et al. 1998), it is probable that birds and not
sewage are the source of campylobacters for these coastal
bathing waters.
3.2.3. Estuaries. Estuaries have a similar seasonal pattern
of campylobacters as coastal waters (Jones et al. 1990a). A
study of the Lune estuary in north-west England con®rmed
that Campylobacter numbers were higher in the winter than
in the summer, that they increased towards the mouth of the
estuary and that densities were higher at high water than low
water (Zainuldin and Jones 1996). There were a variety of
sources of campylobacters, namely, the fresh water section
of the river, various streams and contaminated over¯ows,
Lancaster's WWTW, sheep and cattle grazing the salt
marshes, a large gullery on an urban waste tip and the
incoming seawater. A full range of Campylobacter species
were isolated, with C. jejuni, C. coli, C. lari and UPTCs
present in roughly equal proportions, depending on when
and where in the estuary samples were taken. Samples taken
at low water, furthest from the estuary mouth and close to
the gullery, had the same species composition (C. jejuni,
C. coli, C. lari and UPTC) as the gulls, which move onto the
water and forage on the intertidal sediments of the river at
low water. At the mouth of the estuary the species
composition depended on when samples were taken.
Incoming seawater contained C. lari and UPTCs, whereas
samples taken 4 h after high water (coinciding with a plume
of sewage ef¯uent from Lancaster's WWTW reaching the
mouth of the estuary) contained C. jejuni. Cockles and
mussels at the mouth of the estuary contained the same
species of Campylobacter as found in seawater and oystercatchers, namely C. lari and UPTCs (Jones et al. 1999b).
ã 2001 The Society for Applied Microbiology, Journal of Applied Microbiology Symposium Supplement, 90, 68S±79S
72S K . J O N E S
4. CAMPYLOBACTERS IN SEWAGE
Results from several continents have shown that campylobacters are ubiquitous in sewage and that humans and
animal waste from abattoirs and animal treatment plants are
the major sources (Arimi et al. 1988; HoÈller 1988; Stelzer
et al. 1988, 1991; Jones et al. 1990a, b; Betaieb and Jones
7 1990; Stampi et al. 1992; Koenraad et al. 1994; LauriaFilgueiras and Hofer 1998; Stampi et al. 1999). Analysis of
individual sewers in Lancaster, UK, showed that Campylobacter numbers were related to the incidence of campylobacteriosis in subdivisions of the city and to the presence
of animal ef¯uent from abattoirs and poultry processing
(Jones et al. 1990b). Campylobacters in sewage showed an
identical seasonal pattern to that of the human population
(Fig. 3), namely, a large peak in late May and June and a
minor one in September or October (Jones et al. 1990a, b;
8 Jones and Telford 1991). In Italy, Stampi et al. (1992) also
found higher counts in May, June and July. In 1989, 73% of
the year's input of campylobacters into Lancaster's sewage
occurred in May and June compared with only 29% of
Lancaster's cases of campylobacteriosis. This led to the
hypothesis that annual peaks in human infections are related
to increased amounts of Campylobacter in the environment,
which are in turn determined by changes in the numbers of
Campylobacter within livestock, poultry and wild animals
(Jones and Telford 1991).
4.1. Sewage treatment
Treatment by primary settlement in Lancaster's WWTW
produced ef¯uent containing between 262 and 79 000
campylobacters per 100 ml of ef¯uent, depending on the
time of the year. Arimi et al. (1988) showed that primary
settlement resulted in reductions of 78% in the number of
campylobacters.
Reports in the literature for the effects of secondary
treatment of sewage by trickle ®ltration, activated sludge and
oxidation ponds on the numbers of Campylobacter, show
reductions of between 88% and 99% (Stelzer et al. 1988;
Stampi et al. 1992; Lauria-Filgueiras and Hofer 1998). In
the UK, reductions of between 86% and 99% were obtained
for a large WWTW at Salford (Greater Manchester), of
between 79% and 99% for a rotary bio®lm treatment system
at Middleton (Morecambe) and of between 95% and 100%
for a small WWTW at Caton. During hot, sunny weather
campylobacters did not survive the treatment process in the
small trickle ®lter WWTW at Caton. HoÈller (1988) found no
seasonal differences in Campylobacter numbers in treated
ef¯uent in Germany. Tertiary treatment of ef¯uent with
9 chlorine eliminates campylobacters (Betaieb and Jones 1990;
Stampi et al. 1992).
Overall, the number of thermophilic campylobacters in
the ®nal ef¯uents from WWTWs depends on the type of
treatment. Primary settlement reduces the numbers slightly
and they still show the same seasonal pattern as the inputs.
Secondary treatment reduces the numbers considerably and
tertiary treatment completely eliminates them.
4.2. Effects of sewage ef¯uent on receiving
surface waters
Sewage ef¯uents from WWTWs discharging into freshwater
rivers contribute to the overall loading of campylobacters in
the rivers (Bolton et al. 1987; Jones et al. 1990a). However,
die-off and dilution signi®cantly reduce the numbers downstream of the discharge point (Obiri-Danso and Jones 1999a).
Research into the seasonality of campylobacters in coastal
waters and an estuary receiving untreated sewage discharges,
showed that the numbers of culturable campylobacters
declined very quickly (Jones et al. 1990a). Natural populations of Campylobacter in sewage ef¯uent became unculturable after only 15 min of direct sunlight (Jones et al. 1990b)
and short in situ survival times for natural populations in
seawater were demonstrated by Obiri-Danso and Jones
(1999b) and Obiri-Danso et al. (1999, 2001). Wallace (1994)
showed that the survival of pure cultures of C. jejuni in water
depended on the time of year. They survived for only a few
minutes during June and July compared with up to 4 h
during December and January. Not only were campylobacters more susceptible to high light intensities than other
bacteria, but they were unable to repair damage to DNA.
4.3. Sewage sludge
Fig. 3 Seasonal variation in Campylobacter infections in Lancaster (h)
and the numbers of campylobacters in sewage ef¯uent (black columns)
and undigested sewage sludge (white columns) in the same year
Fresh sewage sludge contains high numbers of campylobacters, which, in the north-west of England, show the same
seasonality as human infections (Fig. 3) (Jones et al. 1990c).
Sludge digestion normally reduced Campylobacter numbers
ã 2001 The Society for Applied Microbiology, Journal of Applied Microbiology Symposium Supplement, 90, 68S±79S
CAMPYLOBACTERS IN THE ENVIRONMENT
1
to zero but occasional positive samples were obtained in the
winter. On these occasions it was unclear whether the
campylobacters had survived sludge treatment or whether
fresh, untreated sludge from another WWTW had been
added post-treatment. Other workers have also shown that
campylobacters in sludge are eliminated by digestion
processes (Stelzer et al. 1991; Stampi et al. 1999). However,
Stampi et al. (1999) have also warned that large numbers of
Arcobacter survive sludge digestion and thickening and have
the potential to contaminate crops.
4.3.1. Sewage sludge put to land. Although the inability
to ®nd measurable numbers of Campylobacter in sludge put
to land has been reported (Jones et al. 1990c), in 1998, 8%
of swab samples taken from sludge put to land were positive
for C. jejuni (unpublished). As sludge production is
increasing and the amount put to land in the UK is likely
to double over the next few years, the possible contamination of sewage sludge with campylobacters and arcobacters
should be re-addressed. With the implementation of The
Safe Sludge Matrix (ADAS 1999), the disposal of sewage
sludge to land has become tightly regulated, but, as with the
disposal of the less well regulated farm slurries, much seems
to depend on the integrity of the farmer.
5. CORRELATION WITH FAECAL
INDICATORS
It is generally accepted that campylobacters are only found
in the presence of faecal coliforms and faecal streptococci.
However, there is not always a good correlation between the
densities of the Campylobacter population and of the
indicators. For example, Carter et al. (1987) isolated
campylobacters from a number of natural water sources in
central Washington (USA) including ponds, lakes, and small
mountain streams, and although campylobacters were
recovered throughout the year, especially in autumn and
winter months, their densities did not show signi®cant
correlation with the faecal indicators. Arvanitidou et al.
(1995) examined 86 river and lake samples from eight
sampling sites in northern Greece for the presence of
pathogens and faecal indicators and they too found that the
density of campylobacters could not be predicted by the
density of the standard indicator bacteria. At two inland
bathing sites on the river Lune (UK) faecal coliforms were
poorly correlated with the density of campylobacters
(P < 0á212 during 1996 and P < 0á155 during 1997)
(Obiri-Danso and Jones 1999a). The density of faecal
streptococci showed a reasonable correlation with the
density of campylobacters in 1996 (P < 0á051) but not
during 1997 (P < 0á513). In Morecambe Bay (UK) there
was a poor relationship between indicators and Campylo-
73S
bacter. For example, the installation of a more ef®cient
WWTW and a longer sea outfall reduced the numbers of
faecal indicators but had no effect on the numbers of
campylobacters (Obiri-Danso and Jones 1999b). In this
case it was because the campylobacters and faecal indicators came from different sources, the campylobacters
coming from wild birds and the indicators from sewage
ef¯uent. Similarly, in the mouth of the Lune estuary,
changes in Campylobacter numbers correlated with the
incoming tide, while those for indicators were associated
with ef¯uent from Lancaster's WWTW upstream of the
sampling site (Zainuldin and Jones 1996). During activated
sludge sewage treatment, Stelzer et al. (1988) found a
signi®cant reduction (94á5%) in campylobacters but not in
indicator bacteria.
On the other hand, Stelzer et al. (1989) showed a high
correlation coef®cient (P < 0á05) between the numbers of
campylobacters and total coliforms in river water polluted
by waterfowl and a poultry farm, and Skjerve and
Brennhovd (1992), using a multiple logistic regression
model to predict the occurrence of C. jejuni/coli related to
three groups of index bacteria, showed that faecal
coliforms, but not faecal streptococci, were strong predictors for C. jejuni/coli in a water source in southern
Norway. In a further study, Brennhovd et al. (1992) used
the same logistic regression analysis to demonstrate a
highly signi®cant relationship between the prevalence of
Campylobacter and the numbers of all three indicator
groups (faecal coliforms, faecal streptococci and sulphitereducing clostridia).
It is not surprising that the populations of indicators and
campylobacters do not always correlate given that campylobacters become non-culturable much faster than the
indicators and that the origins of the bacteria can differ.
6. MISCELLANEOUS ASPECTS
OF SURVIVAL
The growth of Campylobacter in the environment is limited
by its thermophilic and micro-aerophilic nature and the
organism is susceptible to environmental stress, such as to
ambient temperatures and temperature cycling (Blaser et al.
1980; Rollins and Colwell 1986; HoÈller et al. 1988), atmo10 spheric oxygen concentrations (Hoffman et al. 1979), UV
radiation (Bolton et al. 1987; Jones et al. 1990a; Jones et al.
1991; Obiri-Danso and Jones 1999a; Obiri-Danso et al.
11 1999, 2001) and desiccation (Doyle and Roman 1982). In the
absence of spores or any robust physiologically based
protective mechanism, the main survival strategy for
Campylobacter appears to be the production of huge
numbers, in the hope that once out in the `environment',
enough will survive to infect another host.
ã 2001 The Society for Applied Microbiology, Journal of Applied Microbiology Symposium Supplement, 90, 68S±79S
74S K . J O N E S
6.1. Protection in bio®lms
It has been demonstrated that campylobacters can persist,
but not grow, in bio®lms, where they are protected from
biocidal activity (Buswell et al. 1998). However, this may
12 not be widespread as Stanley et al. (1998a) were unable to
isolate them from riverine bio®lms on rocks, from pipes
immersed in rivers or from pipes in groundwater. Similarly,
13 Popowski et al. (1997) were unable to ®nd campylobacters
playing a role in bio®lm formation on the surfaces of wood,
metal and plastic immersed in surface waters.
6.2. Viable but non-culturable Campylobacter
Since the viable but non-culturable (VBNC) form of
14 Campylobacter was ®rst reported (Rollins et al. 1985; Rollins
and Colwell 1986) its presence has been demonstrated in a
variety of aquatic systems. Yet, its signi®cance for infection
of animals and as the cause of disease for humans is still
uncertain. For example, in their review, Koenraad et al.
(1997) state that `The contribution of viable but nonculturable Campylobacter cells in the contamination cycle has been
found to be negligible' whereas, Thomas et al. (1999) sum
up their review with the statement: `The virulence of VNC
forms should be considered to be equivalent to that of the
culturable forms, with the added risk that they are not
detectable by conventional culturable methods'. Recent
research appears to favour the view that VBNC cells of
Campylobacter have an important role in the transmission of
the disease, at least for certain strains (Cappelier et al. 1999;
Lazaro et al. 1999; Tholozan et al. 1999).
6.3. Survival of an infective dose
In the absence of cross contamination, the number of
Campylobacter in a carcass or a meat product will depend on
the extent of contamination at slaughter together with the
ability to survive during processing, transport and storage.
Campylobacters survive best in dark, moist and cool
conditions (Phebus et al. 1991; Hazeleger et al. 1998; Lee
et al. 1998), which are precisely those which are used in the
packaging, storage and transport of meat products from
processing plant to the refrigerator in the kitchen. These
conditions, which are designed to prevent the multiplication
of food poisoning bacteria such as Salmonella and E. coli
0157, are those which help to ensure the survival of an
infective dose of Campylobacter.
7 . E N V I R O N M E N T A L LO A D I N G
AND SEASONALITY
The seasonal pattern of human infections caused by
Campylobacter spp. has remained remarkably constant in
northern temperate zones over the last 20 years or so. There
is a major peak in late spring and early summer and a smaller
one in September (Jones and Telford 1991). After several
environmental investigations in the north-west of England,
the only `environment' which has shown the same seasonal
pattern is sewage (Fig. 3) (Jones et al. 1990b, c). However,
sewage is unlikely to be a major environmental reservoir for
campylobacters because those in sewage ef¯uent survive for
only a short time in surface waters (Jones et al. 1990a; ObiriDanso and Jones 1999b), and they are largely absent from
digested sewage sludge put to land (Jones et al. 1990c). As
Campylobacter cannot grow in the environment and survival
is limited, it has been suggested that changes in the size of
the Campylobacter population within livestock and poultry
15 (Jones and Telford 1991) and the vehicles and vectors which
transmit Campylobacter from one host to another, play a
signi®cant role in the epidemiology of this organism (Stanley
et al. 1998a).
7.1. The farm as an environmental
reservoir of infection
Quantitative data for the intestinal carriage of campylobacters is available for most farm animals and birds, for example,
beef and dairy cattle (Stanley et al. 1998c), sheep (Stanley
16 et al. 1998d), pigs (Weijtens et al. 1997), chickens (Wallace
et al. 1997) and turkeys (Wallace et al. 1998). They show
that most, if not all, livestock and poultry carry Campylobacter and that the numbers of bacteria can be very large,
especially in poultry (Table 3). There are cyclical variations
in the size of the Campylobacter populations within the
intestines of cattle, sheep and chickens, which may be
responsible for different levels of carcass contamination at
different times of the year and contribute to the seasonality
of infections shown in man. Campylobacters are readily
isolated from the rumen of cattle and sheep (Stanley et al.
1998c, d) which suggests that they are continuously ingesting new strains of the bacterium on the farm. Campylobacters from the intestines of farm animals and poultry enter
the wider environment as contamination on meat products,
slaughterhouse waste discharged into sewers, and as faeces
during grazing. Farm visits, especially by children, can
result in campylobacteriosis (Dawson et al. 1995), as can
consumption of unwashed vegetables contaminated with
manure (Park and Sanders 1992).
7.2. Shedding of campylobacters in faeces
of livestock
Although most livestock exhibit intestinal carriage of
campylobacters, shedding in faeces is intermittent. For
example, in sheep at pasture approximately 30% of faecal
samples are positive for campylobacters but this rises to
ã 2001 The Society for Applied Microbiology, Journal of Applied Microbiology Symposium Supplement, 90, 68S±79S
CAMPYLOBACTERS IN THE ENVIRONMENT
1
100% after lambing and when sheep are moved to fresh
17 pasture (Jones et al. 1999a). Factors which encourage faecal
shedding of campylobacters by cattle, pigs and sheep
include: giving birth, weaning, change of pasture, move18 ment outdoors and transport (Weijtens et al. 1997; Wesley
19 et al. 2000; Stanley et al. 1998c, d; Jones et al. 1999b).
Factors which reduce shedding include: gestation, a diet of
silage or hay and housing indoors. Although lambs and
calves are not contaminated with Campylobacter at birth,
when they do become infected, they shed the bacteria at
higher rates than adult animals (Stanley et al. 1998c; Jones
et al. 1999b). Faecal shedding contributes to the environmental load of campylobacters on pasture and in agricultural
run-off.
7.3. Campylobacters in farm waste
Cattle produce approximately 50 l of liquid faeces a day,
which is deposited on pasture, spread around the farm when
cows are brought in for milking and accumulates as slurry or
in bedding when cattle are housed indoors in the winter. On
a wet day a farm yard is covered in a ®lm of cattle manure
which is picked up on farmers' boots and by farm dogs
and cats. It is unsurprising that raw milk frequently
contains campylobacters (Hutchinson et al. 1985). A 100cow dairy herd produces approximately 750 m3 of slurry
20 in a 6-month period (D. Patterson, http://www greenmount.ac.uk). Slurries are collected and stored in large
slurry tanks where campylobacters can survive for long
periods (Kearney et al. 1993). Slurry from the tanks is
disposed of by spreading onto land, where impact varies
with the time of year. Stanley et al. (1998b) showed that not
only did aerated slurries put to land in summer contain
fewer campylobacters than non-aerated slurries put to land
in the winter, but the survival times, after the slurry had
been applied to land, were much longer in the winter than in
the summer, leading to a greater likelihood of contaminated
agricultural run-off in winter than in summer. A Code of
Good Practice governs the disposal of slurry onto land for
the Protection of Water (MAFF 1999), which states that
animals should not be grazed on grassland for at least 21 d
after slurry has been applied. However, compared to the
situation with sewage sludge, the lack of quality control on
the disposal of farm slurries put to land is a cause of
increasing concern (McCann 1999). Co-disposal of spent,
pyrethroid-based sheep dip with farm slurry resulted in the
disappearance of campylobacters from the slurry (Semple
et al. 2000).
Faecal waste accumulating in bedding used for cattle
housed indoors also contains campylobacters which persist
for long periods in dung heaps in the farm yard. Such waste
contains straw, is lumpy and is disposed by muckspreading
onto pasture. Campylobacters are protected in the lumps
75S
and survive for longer than they do in slurries, which are
added as a relatively thin ®lm.
Faeces from grazing livestock and slurry and muck put to
land are attractive to a variety of birds, including gulls,
corvines and shellducks, which peck at the material and
potentially transfer the contaminating campylobacters over
large distances.
Overall, the farm environment acts as a self-perpetuating
reservoir of infection with campylobacters cycling between
farm animals, wild animal and avian vectors and inanimate
vehicles (boots, tractors).
7.4. Wild animals, wild birds and pets
Campylobacters have been found in a variety of wild animals
21 and pets (Fricker and Park 1989; Park et al. 1991; Cabrita
et al. 1992) where they serve as environmental reservoirs of
infection for water catchments and, in the case of pets, direct
contamination of people and their domestic environment.
Birds appear to be the main zoonotic reservoir for thermophilic campylobacters, presumably because of their high
internal temperature (Kapperud and Rosef 1983; Fricker
and Metcalfe 1984; Pacha et al. 1988; Whelan et al. 1988;
Ogg et al. 1989; Glunder et al. 1992; Quessy and Messier
1992). Wild birds have been implicated in contaminating
drinking water settling tanks with Campylobacter in Greensville, Florida, USA (Sacks et al. 1986) and there is evidence
that birds contaminate milk bottles with campylobacters by
pecking at the bottle tops, perhaps after moving from cowpat to milk bottle on the doorstep (Hudson et al. 1990;
Southern et al. 1990; Riordan et al. 1993; Palmer and
McGuirk 1995). Wild birds also cause aesthetic damage in
22 towns (MeÂgraud 1987; Casanovas et al. 1995), contaminate
23 shell ®sh beds (Teunis et al. 1997; Jones et al. 1999c) and
are the source of campylobacters in coastal bathing waters
(Obiri-Danso and Jones 1999b, 2000; Obiri-Danso et al.
24 2001). The presence of campylobacters in migratory birds
(Pacha et al. 1988) is indicative of the large distances that
campylobacters can be transferred.
7.5. Are campylobacter strains found
in the environment important?
Although it is now realized that campylobacters are
widespread in the environment, the extent of the risk to
health is not known. In north-west England we have shown
that the same strains of C. jejuni isolated from patients' stool
samples can be found in livestock, poultry, wild birds, farms,
sewage and surface waters. However, apart from the
consumption of contaminated food, we still do not have a
clear route for the transfer of Campylobacter from the
environment to the consumer. Concerted programmes of
molecular genotyping to match environmental and human
ã 2001 The Society for Applied Microbiology, Journal of Applied Microbiology Symposium Supplement, 90, 68S±79S
76S K . J O N E S
strains of Campylobacter, and environmental epidemiology to
trace infection routes, are necessary before the health risks
can be fully understood.
8. CONCLUSIONS
1. Thermophilic campylobacters are almost certainly ubiquitous in the intestines of farm animals, poultry, pets,
wild animals and wild birds. The size of the Campylobacter population in animals is variable and may be
responsible for different levels of carcass contamination
at different times of the year.
2. Shedding of the bacteria in faeces by animals is
intermittent and is dependent on diet and stress. The
excretion of large numbers of campylobacters in faeces is
a signi®cant survival strategy for Campylobacter.
3. Contamination of the environment is inevitable and
varies seasonally with changes in shedding by animals
and inputs from human and animal-derived sewage
ef¯uent. Sewage treatment substantially reduces the
numbers of Campylobacter in sewage ef¯uent.
4. The presence of campylobacters in environmental
samples correlates qualitatively with the presence of
faecal indicators, but the origins of Campylobacter and
the indicators are not always the same and densities of
Campylobacter and indicators frequently do not correlate
quantitatively.
5. Campylobacters cannot multiply outside the animal host
and survival in the environment is relatively poor.
Survival of Campylobacter is enhanced by moist, cold
conditions, such as those found in refrigerated meat and
poultry.
6. It is not known what proportion of the strains of
thermophilic Campylobacter found in the environment
are pathogenic, nor is there a clear infection route from
the environment to the consumer.
9. ACKNOWLEDGEMENTS
I wish to express my gratitude for the valuable research
carried out at Lancaster University by Drs Mailoud Betaieb,
Collette FitzGerald, Kwasi Obiri-Danso, Karen Stanley and
Joanne Wallace, with funding from the Libyan Government,
the Department of Health, the Ghanaian Government,
Lancaster City Council and the Ministry of Agriculture,
Fisheries and Food, and for the assistance of several M.Sc
and ®nal year project students.
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