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veterinarymicrobiology

Veterinary Microbiology 50 (1996) 117-127

Determination of an effective sampling regime to

detect salmonella enteritidis in the environment of

poultry units

Robert H. Davies * Clifford Wray

Bacteri ology Department, Cent ral Veterinary Laboratory , New Haw , Addl estone, Surrey K Tl5 3NB, UK

Received 11 October 1995; accepted 5 February 1996

Abstract

A study of the dissemination of Salmonella enteritidis in the poultry breeder industry in the

UK showed that the choice of sites for sampling the environment of occupied houses and emptyhouses which had been disinfected after depopulation had a significant influence on the outcome.

Increased isolation rates could be achieved by sampling nest box floors and dust in open slave

feed hoppers in occupied poultry houses. Nest box floors were the most sensitive sites for

detection of residual environmental contamination in poultry houses where enrofloxacin treatment

had been used. Floor sweepings, nest box floors, slave feed hoppers, hydrated wall fabric

junctions and high beams and pipes were the most sensitive sample sites in cleansed and

disinfected poultry houses. The use of universal disinfectant neutralisers gave good results in

laboratory trials but appeared to reduce the isolation rate from field samples.

Keyw ords: Salmonell a enterit idi s; Chicken; Cleansing and disinfection; Sampling methods

1 Introduction

Persistent environmental contamination of housing is an important factor in mainte-

nance of Salmonella enteritidis infection in poultry flocks (Kradel and Miller, 1991;

Baggesen et al., 1992). Shell eggs (Humphrey, 1990) and poultry meat products (Poppe

et al., 1991) are regarded as important sources of human salmonellosis so it is essential

to reduce the level of contaminated material entering the human food chain to avoid

* Corresponding author, Tel.: 01932-347487, Fax: 01932-347046.

0378-1135/96/ 15.00 0 1996 Elsevier Science B.V. All rights reserved

PII SO378-1135(96)00031-4



118 RaberrH. Danvies,C. Wray/ Vet erinar y M it t- abiol ogy 50 t /996) 117-127

food borne infections and consequent economic loss ((Roberts, 1988, Todd, 1989,

Bender and Ebel, 1992, Bailey, 1993).

The effective decontamination of housing of salmonella infected flocks beforerepopulation is a highly important consideration in a HACCP approach for poultry

breeder units (Anon, 1991). It is therefore extremely important that an effective

monitoring protocol for the detection of residual salmonella contamination after cleans-

ing and disinfection is used to assess the success of the operation.

More effective techniques for sampling poultry houses combined with maximising

the sensitivity of salmonella culture (Davies and Wray, 1994) will also increase the

chance of detecting infected flocks at an early stage and enable action to be taken to

reduce further dissemination of the infection.

2. Materials and methods

2 I Sampling methods

Solid samples such as litter or dust were collected directly into jars of sterile buffered

peptone water (BPW, Oxoid CM509). Environmental swabs were taken by vigorous

swabbing of 0.5 1.0 m* surface area using a bunch of six gauze surgical swabs

(Robinson Healthcare, Chesterfield, UK: No. 63024) which had been autoclaved within

jars of BPW. The swabs were returned to the jars after swabbing.

Sweepings samples were gathered using autoclaved stiff deck brooms. Each samplewas estimated to provide 15-25 g of material which was swept up into the jar of BPW

using the moist gauze swabs. Wall fabric junctions were hydrated by pouring 200 ml of

BPW over junctions between boarding and concrete parts of the wall. Surface swabs

were then taken after 30-60 min.

2.2, Salmonella culture methods

These were as described in Davies and Wray (1994) briefly: samples were pre-en-

riched in BPW at 37°C for 18 h followed by selective enrichment in Semi-solid

Rappaport Medium (MSRV, LabM; Lab 150) for 48 h at 41.5”C. Subcultures werestreaked on to Rambach agar (Merck 7500) which was incubated at 37°C for 24 h.

Suspect salmonella colonies were confirmed by full serotyping.

2.3. Universal disinfectant neutraliser

This was prepared according to the following formula:

BPW

Sodium thiosulphate

0.25 N Phosphate buffer

Tween 80L-Histadine

Lecithin

Ammonium chloride

960 ml

5g10 ml

30 ml

lg

3g

1Og



RobertH . Davies, C. Wray / Veteri nary M icrobiol ogy 50 (19 ) I 1 7-l 27

2.4. Definition of terms used to describe poultry house equipment

119

Slave feed hoppers - these are open short-term feed reservoirs which house and feedthe motor units which power the chain feeder system.

Chain feeder system - this is a system of metal channels arranged to convey feed

around the poultry house by means of a moving chain within the channel.

Nest box front beam - this is the wooden plank at the front of the nest boxes which

retains litter.

Perches - these are wooden rails fixed to nest box frames on which birds perch to

gain entry to nest boxes.

2.5. Statistical methods

Probability values were obtained with the Chi-Square test (Yates Correction) using

2 X 2 tables on EPI-INFO Statcalc programme. Results shown in each table were pooled

for analysis as described in the Results section.

3. Results

3.1. Detection of salmonella in occupied poultry houses

Comparative results of sampling in occupied poultry houses are shown in Table 1.

There was a threefold higher salmonella isolation rate from nest box floors and dust on

in-house slave feed hoppers ( p < 0.01) than from drinkers, chain feeders, slats, perches

Table 1

Detection of 5. enterifidis in occupied poultry houses - SalmaneEZa isolation from various sample sites

Poultry Type of unit Slave feed hopper Nest boxes Other sites

unit

code

No. of No. positive No. of No. positive No. of No. positive

samples for Salmonella a samples for Salmonella a samples for Salmonella a

A Broiler breeder 4 1 (25.0) 5 1 (20.0) 20 0

B Turkey breeder ’ 12 2 (16.7) 6 0 26 0

C Broiler breeder 1 1(100.0) 4 0 24 l(4.1)

D Layer 4 3 (75.0) NA - 32 l(3.1)

E Layer 4 1 (25.0) NA - 38 0

F Broiler breeder 3 1 (33.3) 9 7 (77.8) 24 1 (4.7)

G Broiler breeder 4 4 (100.0) 16 11 (68.7) 64 33 (51.6)

H Broiler breeder 2 2 (50.0) 16 8 (50.0) 64 9 (21.8)

(sep. feed bin

in ante-room)

Totals 34 15 (44.1) 56 27 (48.2) 292 45 (15.4)

a % of samples positive for S. enteritidis in brackets.

b S. heidelberg infection.

NA = Not applicable.



12 RobertH. Daoies. C. Wray/ Veterinav Microbiology 50 (1996) I1 7-127

and dust on beams and ventilation ducts. In broiler breeder houses salmonella was

isolated from all the egg sorting tables and 75% of the egg collection trolleys sampled.

3.2. Detection of S. enteritidis contamination of poultry houses after antibiotic treatment

of the flock

Table 2 shows results of sampling in occupied broiler breeder houses where the flock

had recently received antimicrobial (Enrofloxacin) treatment in the water supply. In

these cases there was a general reduction (pre-treatment sampling data not shown) in the

prevalence of salmonella in environmental samples after treatment which was less

marked on nest box floors, whereas, there was a substantial reduction in the prevalence

of salmonella in other sample sites. The slave hoppers were not a sensitive sample site

following antibiotic treatment.

3.3. Detection of persistent S. enteritidis by periodic sampling of a trial poultry house

after cleansing and disinfection

The results of sampling a breeder house at 1, 2, 6 and 12 weeks after cleansing and

disinfection following depopulation of a broiler breeder flock which was naturally

infected with S. enteritidis are shown in Table 3. A sampling regime comprising floor

sweepings, in-house feed hoppers and hydrated wall fabric junctions successfully

detected persistent salmonella contamination on each occasion compared with swabbing

of floors, walls, beams and drinkers which gave negative results (p < 0.05). Liquid

vacuum suction, using a BPW filled domestic vacuum/carpet cleaner which had been

sterilised by fumigation with ethylene oxide, failed to detect salmonella despite collect-

ing a much larger volume of dust from the floor than was obtained by sweeping.

3.4. Detection of persistent S. enteritidis infection in commercial poultry breeder houses

after cleansing and disinfection

Table 4 compares salmonella isolation rates obtained from various sample sites in

commercial broiler or layer breeder houses after cleansing and disinfection. Floor

sweepings and nest box floors were the most sensitive sample sites followed by slave

feed hoppers, hydrated wall fabric junctions and high beams and pipes p < 0.01).

Samples from wall comers, floor expansion joints, fan ventilation shafts, chain feeders,

drinkers, perches and nest box front beams were relatively insensitive with 15/ 16 (94%)

of the houses being identified as salmonella negative when these sample sites were used

in a simulated standard sampling regime of 23 sites per house. The most useful other

sample sites were egg collection buggies and egg handling tables. Where dead mice or

mouse droppings were present these too usually had a high prevalence of salmonella.

3.5. Use of universal disinfectant neutraliser for enhanced detection of salmonella ondisinfected sur aces

Table 5 shows the results of a small study using universal disinfectant neutraliser

added to the BPW used for swabbing and culture.



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Table 5

Use of universal disinfectant neutraliser for Isolation of Mrrwnellu on disinfected surfaces

No. of Positive for Salmonellu Positive for Salmonellusample\ by standard culture using neutraliser

No. ‘Z NO. c/r

Laboratory floor surface5 133 52 39. I 14 55.6

Poultry house environmental -1x -I6 95.X 39/w 72.5

SUd2KY?

Laboratory floor surfaces which had been accidentally contaminated with salmonella

were disinfected with various chemical disinfectants. Swabbing after 2-8 h contact timeproduced a significantly increased salmonella isolation rate ( p < 0.01) when the disin-

fectant neutraliser was used This contrasted with the situation in a naturally contami-

nated poultry house where the isolation rate was reduced ( p < 0.01) when disinfectant

neutraliser was used.

4. Discussion

Environmental monitoring of the poultry house has been shown to be a highly

effective means of detecting salmonella infection in the flock (Kradel and Miller, 1991,

Poppe et al., 1992). A well designed environmental monitoring programme can therefore

be a useful adjunct to regimes designed to detect infection in faeces, post mortem tissues

and meconium. Monitoring regimes commonly also involve pooling of samples for

culture, but this has been shown to reduce detection sensitivity (Giessen et al., 1991) so

it is best to culture as many individual samples as economically possible.

The object of these studies was to define specific sampling sites within poultry

houses for enhanced detection of salmonella. particularly after cleansing and disinfec-

tion. In occupied poultry houses swabs taken from nest box floors and slave feed

hoppers gave higher isolation rates than litter, dust and drinker samples. Nest boxes are

kept relatively clean so there is little competitive “litter effect” which leads to reduction

of salmonella as a result of direct competition for space and nutrients and toxic effects

of metabolites produced by the action of other bacteria in the littered areas of the house

(Opara et al.. 1992). Thus salmonellas excreted by birds during the early stages of

infection may persist preferentially in nest boxes, despite the widespread use of

paraformaldehyde prills or powder as a nest box litter disinfectant. The body heat of the

birds may also lead to multiplication of salmonellas within nest boxes.

In-house slave feed hoppers in broiler breeder houses or spilled feed from caged layer

flock conveyor feeding systems were also highly sensitive sample sites. It is likely that

the organic matter in feed dust supplies a protective nutritive matrix to enhance the

survival of salmonellas. We have demonstrated survival of S. enteritidis inoculated into

poultry feed at 10” organisms/100 g feed, for at least two years (unpublished data).



RobertH . Dauies, C. Wray/ Veteri nary M icrobiology 50 (1996) I1 7-127 125

The most sensitive of the other sample sites in occupied breeder houses were the egg

sorting tables and egg collection buggies. Swabs taken from slats, perches and the front

boards of nest boxes were not very useful unless a high level of general salmonellacontamination was present.

When antibiotic treatment is used in salmonella infected flocks there may be a

subsequent effect on the level of environmental contamination through excretion of the

antibiotic and its metabolites by the birds and suppression of ongoing excretion of

salmonella in faeces. When enrofloxacin has been used the reduction of environmental

contamination makes environmental monitoring less useful but nest box floors were still

a sensitive sampling site. Interestingly the isolation rate of salmonella from slave feed

hoppers dropped dramatically after treatment. This suggests that feed dust in slave feed

hoppers may enhance detection of current excretion of salmonellas which is reduced

after antibiotic treatment.

The objective of sampling poultry houses for salmonella after cleansing and disinfec-

tion is to ensure that decontamination has been successful. After cleansing and disinfec-

tion we investigated the use of various sampling techniques and sample sites. Large

gauze swabs were used to maximise the surface area which could be sampled and to

provide abrasive properties for vigorous rubbing of cleaned surfaces. Even using these

large swabs it was not possible to isolate salmonella during periodic sampling of floor

and wall surfaces in a disinfected poultry house whereas S. enteritidis was found on

swabs taken from open feed hoppers, hydrated wall fabric junctions and floor sweep-

ings. Interestingly liquid vacuum suction of large areas of floor surfaces did not enhancesalmonella detection. This may be because the organisms were intimately attached to

floor surfaces in established biofilms and vacuum suction has little abrasive effect. It has

been shown that sampling such biofilms may give false negative results (Kim et al.,

1993, Wirtanen and Mattila-Sandholm, 1993) and that vigorous physical abrasion such

as brushing is the best means of detaching organisms from the biofilms (Carpentier and

Cerf, 1993). It is also possible to quickly sample a much larger surface area of cleaned

floor surface by sweeping than by swabbing.

Hydration of wall fabric junctions was successful in isolating salmonella but this was

not true of cracks and expansion joints in the floor. During field trials sampling such

cracks after disinfection was similarly unrewarding despite large quantities of residual

organic matter of&en being present. It may be that floor cracks remain wet for long

periods after disinfection lending to anaerobic conditions favouring competitive bacteria.

Also disinfectant activity is likely to be better in floor cracks because of pooling of the

liquid compared with rapid run-off and evaporation from vertical wall surfaces,

Field studies of poultry houses after cleansing and disinfection confirmed the value of

sampling floor sweepings, slave feed hoppers and hydrated wall fabric junctions. In a

few cases there had been recontamination of the environment by S. enteritidis in

droppings from a residual infected mouse population. Sweepings samples and samples

from slave feed hoppers were more likely to detect mouse droppings which may not benormally noticed unless supplementary bright lighting is used to assist inspection of the

building.

There was also a high isolation rate from nest box floors, which were often not

disinfected as thoroughly as other fittings even though they are the most highly



126 RohrrtH. Da s. C. Wruy / Veterinap Microhivlvg~ 50 II9961 I 7- 127

contaminated item in a breeder house. High beams and pipes were also worthwhile

sample sites with salmonella persisting largely through inconsistent cleansing and

application of disinfectant to less accessible areas.Swab samples from floor expansion joints, wall comers, fan boxes, slats and perches.

drinkers, chain feeders and nest box front beams were very poor for isolation of

salmonella and only the most contaminated house was identified when these samples

were used

It was interesting that no salmonellas were isolated from water header tanks in this

study even though in some cases the tanks were not covered and had been poorly

cleaned. Some bacteria are capable of long-term persistence in biofilms in water tanks

and pipes (Manz et al., 1993). It is uncertain whether failure to detect salmonella in this

work reflects true absence of the organism or the presence of a dormant non-culturable

state (Roszak et al., 1983). We have observed an increased isolation rate of S. erzteritidis

from open drinkers and dust samples taken from occupied poultry houses when small

pieces of cellulose sponge are used during pre-enrichment culture as a protective matrix

(unpublished data). This suggests that dormancy and poor culturability of salmonella

may occur in aqueous and dry poultry house environmental samples.

Universal disinfectant neutralisers have been recommended for use in environmental

sampling after cleansing and disinfection (F. Sellars and G.P. Wilding, personal

communications).

Our laboratory based studies confirmed an increase in salmonella isolations in swabs

taken from disinfected surfaces (Table 5) but the opposite occurred with samples takenin a disinfected poultry house where sub-lethal concentrations of disinfectant had

inadvertently been used. In disinfected poultry houses it is common to find single figure

levels of salmonella against a background of 4-8 log ,(I levels of other coliforms. It may

be that ingredients such as lecithin and histidine promote overgrowth of salmonella by

competitive organisms during pre-enrichment culture of field samples. Similarly, a low

environmental salmonella isolation rate in disinfected hatcheries produced by swabbing

using disinfectant neutraliser has been shown to produce a underestimate of the extent of

contamination compared with use of BPW for swabbing (unpublished data). More work

is required to evaluate the use of disinfectant neutralisers under controlled conditions in

the field.

It is difficult to evaluate the hazard posed by survival of salmonella in poultry houses

after cleansing and disinfection. The presence of salmonella contamination may not

always result in infection of the flock (Bailey, 19931 but it is difficult to carry out risk

assessment studies in the field because disinfection is normally repeated when persistent

environmental contamination has been demonstrated. This was true of this study except

for houses A. B and F (Table 4) where there was insufficient time for redisinfection

before restocking. In houses A and F there was a rapid re-infection of the new broiler

breeder flocks and in house B, which was on the same site as house A re-infection

occurred later and so S. enteritidis may have spread from the flock in house A.

This work shows that improvements in choice of sampling sites and techniques for

detection of salmonella on poultry units can be made. Although much work remains to

be done. sampling strategies based on the methods use in this study, particularly

swabbing nest box floors, egg handling equipment and slave feed hoppers, and the use



RobertH . Davi es, C. Wray / Veteri nar?, M i crobi ol ogy 50 (1996) 117-127 127

of floor sweepings samples, should enhance control measures for S, enteritidis in the

poultry industry.

Acknowledgements

This work was funded by the Ministry of Agriculture, Fisheries and Food. The

authors are grateful to Mrs S. Bedford and Mrs K. McIntosh for technical assistance, and

would also like to thank colleagues in the Animal Health (Zoonoses) Division and State

Veterinary Service for their assistance with arranging field work.

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