Reports of Salmonella in Chickens

According to the 2011 edition of 'Salmonella in Livestock Production in GB', an annual publication from the Veterinary Laboratories Agency, 13.5 per cent fewer Salmonella incidents from chickens were reported in 2011 than in the previous year.
calendar icon 21 September 2012
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By: Banrie

According to the June 2011 Agricultural Census, the total number of poultry in Great Britain was 142.9 million, comprising approximately 43.5 million laying and breeding chickens (including pullets), 88.3 million broilers and 11.0 million 'other poultry'. Compared to 147.3 million poultry in 2010, this is an overall reduction of approximately 3.0 per cent. While there has been an increase of 1.5 per cent in the laying and breeding chicken sector, the number of broilers showed a decrease of 5.4 per cent.

In this chapter, two different systems of reporting are used and therefore the interpretation of the results has to be done bearing this in mind.

  • Incidents are defined as the first isolation and all subsequent isolations of the same Salmonella serovar from an animal, group of animals or their environment on a farm within a defined time period (usually 30 days). An incident can therefore involve more than one flock and/or house sampled at the same time and subsequent crops from the same house or premises. The first part of this chapter describes incidents and includes samples originating from statutory surveillance, voluntary surveillance, investigations into clinical disease and investigations carried out under the Zoonoses Order.

  • The second part of this chapter describes results obtained within the National Control Programmes (NCPs), i.e. results from statutory surveillance. The Salmonella serovars considered to be of public health significance under EU regulations (the regulated serovars) form a very small proportion of the total isolates reported. Results from the NCPs are reported to the European Commission in a way that ensures that every flock with a Salmonella - positive result is counted only once, including cases when more than one flock on the same premises test positive at the same time or repeatedly within a short period of time. Numbers of positive flocks reported within the NCP are therefore expected to differ from the number of reported incidents. However, some flocks may be positive for more than one serovar, in which case they are still only counted once as positive flocks for the NCP. This still applies if there is an interval of more than 30 days between the positive tests.

The total number of chicken submissions to AHVLA/SAC laboratories (for all reasons, including Salmonella) increased by 3.2 per cent in 2011 (6,703 submissions) compared to 2010 (6,497 submissions), after an increase of 1.2 per cent between 2009 and 2010. However, between 2008 and 2009 a much bigger increase of 65.9 per cent (from 3,868 submissions in 2008 to 6,420 submissions in 2009) had been observed. This increase was due to the implementation of the National Control Programmes, whereas the increase between 2010 and 2011 can best be explained by an increase in diagnostic submissions of 23.3 per cent (2,177 in 2011 compared to 1,766 in 2010).

A total of 410 Salmonella incidents were reported from chickens in 2011, which is a decrease of 13.5 per cent compared to 2010. This number includes incidents from statutory surveillance, voluntary surveillance, diagnostic submissions and investigations of clinical disease.

The total number of incidents were distributed among the following categories according to the reason for submission:

  • statutory surveillance: 378 (92.2 per cent)
  • voluntary surveillance: 23 (5.6 per cent)
  • investigations of clinical disease: 7 (1.7 per cent)
  • investigations under the Zoonoses Order: 2 (0.5 per cent)

The proportion of incidents relating to statutory surveillance has been going up since 2008, which is due to the implementation of the NCPs in all production types.

The incidents reported in 2011 originated from the following production types:

  • Breeders: 6 (1.5 per cent)
  • Broilers: 328 (80.0 per cent)
  • Layers: 72 (17.6 per cent)
  • 'Backyard poultry': 4 (1.0 per cent)

Compared to 2010, the number of incidents from breeding flocks decreased from 21 to six, the number of incidents from laying flocks decreased from 104 to 72 and the number of incidents from broilers decreased from 345 in 2010 to 328 in 2011.

Thirty-three different serovars of Salmonella enterica were isolated in 2011, accounting for 391 of the 410 incidents. This compares to 40 different serovars in 2010. Eleven incidents involved untypable Salmonella strains and eight incidents involved Salmonella enterica rough strains.

For all Salmonella serovars isolated from chickens from 2007 to 2011, S. Montevideo (86 incidents; 21.0 per cent of all incidents) was the most frequently reported serovar in 2011, and the number of reports of S. Montevideo has increased rapidly over the past few years. While there were only two incidents of S. Montevideo reported in 2008, numbers rose to 13 in 2009, 49 in 2010 and finally 86 in 2011. The reason for this increase is not known, but it is thought to relate to contaminated feed ingredients as an increase in this serovar in feedingstuffs has been noted. S. Montevideo has also become more prominent amongst human cases. S. Kedougou (79 incidents; 19.3 per cent of all incidents) was the second most frequently isolated serovar and has been at a high level since 2009. S. Senftenberg (48 incidents; 11.7 per cent of all incidents), S. Livingstone (42 incidents; 10.2 per cent of all incidents), S. Mbandaka (39 incidents; 9.5 per cent of all incidents) and S. Ohio (29 incidents; 7.1 per cent of all incidents), were the third, fourth, fifth and sixth most common serovars in 2011 respectively, together comprising 78.8 per cent of all incidents. All of these serovars have been associated with feed or hatchery contamination.

S. Enteritidis, which was the most common serovar in 2008 (31.9 per cent of incidents) and in 2007 (18.9 per cent of incidents), only accounted for eight incidents in 2011 (2.0 per cent of all incidents). This represents a reduction of 42.9 per cent compared to 2010 and thus demonstrates the good progress the poultry industry has made in reducing the number of incidents of S. Enteritidis in recent years.

Phagetypes for S. Enteritidis incidents are shown in the report. Due to the low number of incidents, no clear predominance of a certain phagetype could be seen. PT1 and PT4 were each involved in two incidents, one incident was related to phage type 7 and strains were untypable in three incidents. This is a different picture to what was seen in 2010, when 14 of the 17 incidents involving S. Enteritidis were related to PT4.

S. Typhimurium incidents have been fairly stable over the past five years, with a maximum of 5.2 per cent of all incidents in 2008 and a minimum of 2.9 per cent of all incidents in 2011.

Phagetypes for S. Typhimurium incidents are tabulated. There was no clear predominance of any particular phagetype; two incidents each were reported involving DT40 and DT193; single incidents of DT8, DT104, DT104b, DT120, DT135, DT137 occurred, and two incidents involved untypable strains.

Monophasic strains of S. Typhimurium were reported in chickens for the first time in 2010, when two incidents involving S. 4,12:i:- and five incidents involving S. 4,5,12:i:- were recorded. Numbers of monophasic strains of S. Typhimurium remained low in 2011, with two incidents each of S. 4,12:i:- and S. 4,5,12:i:- reported.

Phagetypes for the monophasic strains S. 4,5,12:i:- and S. 4,12:i:- are shown in the report. All incidents of monophasic strains of S. Typhimurium in chickens were DT193.

S. Hadar was not detected in chickens in 2011. S. Virchow (one incident) and S. Infantis (two incidents), which are regulated serovars for breeding flocks only, were detected at very low levels, but not in any breeding flocks in 2011.

A difference between production types can be observed in the ranking of the most common serovars. For broilers, S. Montevideo (85 incidents, 25.9 per cent) was the most common serovar, followed by S. Kedougou (73 incidents, 22.3 per cent), S. Mbandaka (36 incidents, 11 per cent), S. Livingstone (35 incidents, 10.7 per cent), S. Senftenberg (32 incidents, 9.8 per cent), and S. Ohio (28 incidents, 8.5 per cent). In the laying hen sector, S. Senftenberg (14 incidents, 19.4 per cent) was the most common serovar and was mainly found in immature birds, followed by S. Enteritidis (8 incidents, 11.1 per cent), S. Typhimurium (8 incidents, 11.1 per cent), S. Livingstone (7 incidents, 9.7 per cent), S. Derby (6 incidents, 8.3 per cent) and S. Kedougou (4 incidents, 5.6 per cent). In breeding flocks, S. Kedougou and S. Senftenberg were both reported with two incidents each (33.3 per cent).

Some serovars which were isolated in 2011 had not been isolated from chickens for several years; these include S. Haifa (last recorded in 2005), S. Oslo (last recorded in 2006) and S. Schwarzengrund (last recorded in 2006). There was one incident of S. Dakota in 2011; this serovar has never been recorded in chickens in Great Britain before. Some unusual phage types of S. Typhimurium were recorded in 2011; DT40, DT135 and DT137 were all recorded for the first time from chickens in 2011. DT40 is a recognised wild bird-related strain and DT135 has been associated with game birds and horses.

S. Gallinarum was not isolated from chickens in 2011, with the last incident recorded in 2007.

Three S. Pullorum incidents were reported from chickens on three different premises; all of the birds were recorded as 'pets'. None of these premises were involved in S. Pullorum incidents in 2010.

National Control Plan for Salmonella in Breeding Flocks of Chickens

The Zoonoses Regulation 2160/2003, which came into force on 21 December 2003, aims to reduce the prevalence of certain zoonotic infections at the primary production level, by requiring the implementation of species-specific Salmonella National Control Programmes (NCPs). The NCP is enforced by separate, equivalent legislation in England, Scotland and Wales. These regulations set up detailed sampling requirements for Industry and procedures to follow when positive flocks are identified.

Together, the Control of Salmonella in Poultry Orders (CSPO) implement the NCP for breeding flocks (of chickens – Gallus gallus) as required by Regulation (EC) No. 200/2010, which sets a target for the breeding flock sector to ensure that no more than 1 per cent of the adult breeding flocks with more than 250 birds remain positive for regulated Salmonella serovars annually. The EU target was based on the five most frequent serovars in human cases in 2003, which were: S. Enteriditis, S. Typhimurium, S. Virchow, S. Hadar, and S. Infantis. This regulation amends Regulation (EC) No. 1003/2005 (which had set out a target for reduction to the end of 2009), and allows for the new option of collection of at least one pair of boot swabs representing the whole area of the house together with an additional dust sample as an option for operator and official sampling in holdings.

As the UK breeding sector achieved the former reduction target in 2007 and 2008, from April 2009 breeding companies could, at the discretion of the Competent Authority, and as set out in Regulation (EC) 213/2009, reduce the frequency of operator sampling from every second week to every third week, and the Competent Authority could reduce the number of official samples from three to two. Not all breeding companies in the UK have chosen to implement this extended testing interval.

To facilitate collection of official samples, owners must inform the Competent Authority of the expected date of movements to the laying unit and also the date on which the flock is expected to reach the end of the production cycle.

The operation of the NCP for breeding flocks is governed by the relevant EC and UK legislation.

While the EC target is concerned with regulated serovars in adult stage flocks only, the CSPO (and in turn the NCP) sets out sampling and recording requirements for both in-rear and adult flocks and AHVLA monitors results from testing in both stages.

Salmonella in breeding flocks is reported in terms of positive flocks, as required by legislation (EC Regulation 200/2010). A flock is counted only once regardless of the number of separate incidents reported in that flock or the number of distinct serovars identified. If more than one positive flock is identified on the holding within the year, these are counted separately.

Positive flocks identified in the NCP for breeding flocks in 2011

A summary of the numbers of positive flocks identified from CSPO testing in GB in 2011, with numbers of flocks confirmed with individual Salmonella serovars, is provided in the report. In Great Britain, a total of 1,107 adult breeding flocks were tested: only two flocks (0.18 per cent) on two holdings tested positive for any Salmonella serovar with one of those (a small ‘niche’ breeder flock) confirmed with a regulated serovar (S. Typhimurium).

No isolations of the monophasic Salmonella variant S. 4,5,12:i:- were identified from CSPO testing of breeding flocks during the year. An amendment to Regulation No. 200/2010 - Regulation (EC) 517/2011 of 25 May 2011 specifies that monophasic strains of Salmonella with the antigenic formula S. 1,4,[5],12:i:- should be counted as S. Typhimurium for the purposes of assessing achievement of the reduction target.

The proportion of tested flocks confirmed with a regulated Salmonella serovar is 0.09 per cent (1/1107). This figure is well below the EC target of 1 per cent and maintains the low prevalence reported in recent years (0.54 per cent in 2008, 0.15 per cent in 2009; 0.07 per cent in 2010). There have been no reports of S. Enteriditis in breeding flocks during the five years of statutory testing under the NCP.

The prevalence of all detected serovars is the lowest recorded since the commencement of the NCP and continues the decline seen in recent years.

Non-regulated serovars were isolated from one other adult breeding flock (S. Mbandaka) and one in-rear flock (S. Kedougou). Salmonella Mbandaka has appeared in the breeding sector NCP results in all four previous years 2007 – 2010 and is among the top ten serovars in chicken flocks from all modes of surveillance.

National Control Programme for Salmonella in Laying Hen Flocks

Commercial laying flocks are subject to statutory Salmonella testing programmes in order to fulfil the requirements of EU legislation. Regulation (EC) No. 2160/2003 and Commission Regulation (EU) No. 517/2011.

In the EU baseline survey of Salmonella in laying hen flocks conducted in 2004/20057, about 8 per cent of layer flock holdings in the UK were found to be positive for S. Enteritidis and/or S. Typhimurium. A target was set (Regulation (EC) No. 1168/2006) to annually reduce the number of adult laying flocks positive for these serovars by at least 10 per cent compared with the previous year, starting in 2008, to a maximum of 2 per cent of flocks remaining positive for these regulated Salmonella serovars.

All Member States were required to have a National Control Programme (NCP) in place in 2008. The National Control Programme for Salmonella in Laying Flocks includes all commercial egg laying flocks except where producers only supply small quantities of eggs direct to the final consumer (Regulation (EC) No. 2160/2003, Article 1 paragraph 3).

Monophasic strains of Salmonella Typhimurium, with the antigenic formula S. 4,[5],12:i:-, have rapidly emerged over the past few years to become amongst the most common Salmonella serovars in several animal species as well as human clinical cases. As monophasic strains are considered to pose a public health risk comparable to other Salmonella Typhimurium strains, the legislation was amended in 2011 to include S. 1,4,5,12:i:- and S. 1,4,12:i:- in the targets for regulated serovars, along with S. Enteritidis and S. Typhimurium.

The NCP is enforced by separate, equivalent legislation in England11, Scotland and Wales. These regulations set up detailed sampling requirements for Industry and procedures to follow when positive flocks are identified.

Positive flocks identified in the NCP for laying flocks in 2011

For the purposes of reporting results of the NCPs to the European Commission, every positive flock identified during the year is counted, irrespective of the number of positive flocks on a given farm at any one time and a positive flock is counted only once regardless of the number of times a positive result is returned.

A summary of positive flocks detected within the NCP in 2011 and the numbers of flocks positive for each serovar by status of sampling is shown in the full report for adult flocks and in-rear flocks.

Under the statutory testing programme, 44 laying flocks (29 adult flocks and 15 in-rear flocks) were detected as positive with any Salmonella serovar in 2011.

The number of adult flocks that tested positive for Salmonella spp. represents a 29.3 per cent decrease compared with 2010 (41 positive flocks) and 56.7 per cent decrease relative to both 2009 and 2008 (67 positive flocks in both years). Of the 29 positive adult flocks in 2011, five had S. Enteritidis and two other flocks had S. Typhimurium (one of which had S. Typhimurium DT135, which has never previously been recorded in chickens in Great Britain). These figures are marginally lower than those from 2010 (when six flocks tested positive for S. Enteritidis and three for S. Typhimurium) and 2009 (when seven tested positive for S. Enteritidis and three for S. Typhimurium). No monophasic strains of S. Typhimurium were recorded in adult flocks tested under the NCP during 2011, whereas two flocks tested positive for S. 4,12:i:- during 2010. Thus, a total of seven flocks were detected positive with regulated serovars in 2011 compared with 11 flocks in 2010, 10 flocks in 2009 and 53 flocks in 2008.

The number of positive in-rear (immature) flocks represents a 50.0 per cent decrease compared with 2010 (30 positive flocks) and 60.5 per cent decrease compared with 2009 (38 positive flocks). None of the 15 positive rearing flocks was infected with regulated serovars, compared with one S. Enteritidis-positive flock in 2010, seven S. Typhimurium-positive flocks in 2009, and four S. Enteritidis-positive flocks and one S. Typhimurium-positive flock in 2008. Two-thirds (10/15) of the in-rear (immature) Salmonella-positive flocks in 2011 were identified with S. Senftenberg, which was also the dominant serovar among immature flocks in 2010 (responsible for 24 of the 30 positive flocks) and 2009 (responsible for 28 of the 38 positive flocks). S. Senftenberg is a hatchery-associated serovar which appears to persist poorly into adulthood as it was only isolated from one flock during the laying phase in both 2010 and 2011. One in-rear (immature) flock tested positive for S. Haifa in 2011, which has never previously been recorded from routine surveillance in chickens in Great Britain.

A comparison of the serovars identified in adult laying flocks in the NCP each year between 2008 and 2011 is shown in the report. S. Enteritidis remained the most commonly isolated Salmonella serovar in 2011, although as in previous years there was no particular dominance by any serovar in the adult flocks. S. Kedougou was the second most common serovar among layers, which is identical to its ranking among chickens overall. However, there were no isolations of S. Montevideo from layers, which was the most common serovar among broilers overall. Neither S. Agama nor S. Agona were identified in layers in 2011; both have declined among layers since 2009, which is also reflected in their frequency among chickens overall.

Several unusual serovars were also isolated from layers in the NCP in 2011, including S. Dakota (which had never previously been recorded in chickens in Great Britain), S. Oslo (which had never previously been recorded from routine surveillance in chickens in Great Britain), and S. Schwarzengrund (which was last recorded in chickens in 2006).

Using the number of laying flocks subject to at least one official test during 2011 as the denominator population, the estimated prevalence of Salmonella-positive adult egg laying flocks in Great Britain from statutory testing was 0.75 per cent (29/3,865). The estimated prevalence of Salmonella Enteritidis, S. Typhimurium and monophasic strains of S. Typhimurium in adult egg laying flocks in Great Britain was 0.18 per cent (7/3,865) in 2011, well below the definitive target of 2 per cent. This compares with an estimated prevalence for all Salmonella serovars of 1.00 per cent in 2010, 1.60 per cent in 2009 and 1.25 per cent in 2008, and an estimated prevalence for S. Enteritidis, S. Typhimurium and/or monophasic strains of S. Typhimurium of 0.27 per cent in 2010, 0.24 per cent in 2009 and 1.00 per cent in 2008. The considerable reduction in Salmonella prevalence since the EU baseline survey of 2004/05, while not directly comparable to the NCP monitoring results due to different sampling methods and denominator data, does indicate the substantial progress that continues to be made in controlling Salmonella in the layer sector.

National Control Programme for Salmonella in Broiler Flocks

Commercial broiler flocks are subject to statutory Salmonella testing programmes in order to fulfil the requirements of EU legislation Regulation (EC) No. 2160/2003 and Commission Regulation (EC) No. 646/2007.

In the EU baseline survey on the prevalence of Salmonella in broiler flocks conducted in 2005/2006, S. Enteritidis was not isolated from any commercial broiler holdings and S. Typhimurium was reported from only one eligible holding, giving an estimated prevalence of 0.3 per cent for these serovars for the UK. A target was set (Regulation (EC) No. 646/2007) for a maximum of 1 per cent of broiler flocks to remain positive for S. Enteritidis and S. Typhimurium by December 2011.

A National Control Programme (NCP) for Salmonella in broiler flocks was implemented in 200918. All flocks of chickens reared for meat are included unless exempted in Regulation (EC) No. 2160/2003 under Article 1.3 (as amended by Regulation (EC) No. 199/2009), i.e. birds produced for private domestic consumption, or where there is direct supply of small quantities of products to the final consumer or to local retail establishments directly supplying the primary products to the final consumer.

The NCP in England is enforced by The Control of Salmonella in Broiler Flocks Order 2009 (CSBO) and there is separate equivalent national legislation for Scotland20 and Wales.

Positive flocks identified in the NCP for broiler flocks in 2011

For the purposes of reporting results of the NCPs to the European Commission, every positive flock is counted, irrespective of the number of positive flocks on a given farm at any one time and a positive flock is counted only once regardless of the number of times a positive result is returned.

In total, 516 broiler flocks tested positive for Salmonella spp. under the statutory testing programme in 2011. This is slightly lower (1.7 per cent) than in 2010 (525 flocks) but 42.1 per cent higher than in 2009 (363 flocks). Two flocks tested positive for S. Typhimurium, which is lower than in 2010 (seven S. Typhimurium-positive flocks) but identical to 2009. In addition, one flock tested positive for Salmonella 4,5,12:i:- in 2011, compared with three in 2010 and none in 2009. No flocks were found to be infected with S. Enteritidis in 2011, which was also the case in 2010, whereas ten flocks tested positive for S. Enteritidis in 2009. Thus, only three flocks tested positive for regulated serovars in 2011 compared with ten flocks in 2010 and twelve flocks in 2009.

A comparison of the serovars identified in the broiler NCP each year between 2009 and 2011 is shown in the report. As broilers are responsible for a large proportion of the Salmonella reports from chickens as a whole, there is a close similarity between the most common serovars found; for example, S. Montevideo was the most frequently reported serovar from broilers as well as chickens overall.

S. Kedougou has accounted for roughly a quarter of Salmonella-positive broiler flocks each year since the start of the NCP. S. Kedougou is a feed-related serovar which can sometimes be found in oil seed meal ingredients and as a coloniser of the pellet cooling system in feed mills.

Reports of S. Montevideo in broilers have increased substantially since the start of the NCP, from 15 positive flocks (4.1 per cent of all Salmonella-positive flocks) in 2009 to 160 flocks (31.0 per cent of all Salmonella-positive flocks) in 2011. There have been no parallel increases in laying chickens or turkeys. However, there have been increases in cattle and sheep as well as in feeds, including poultry feed. S. Montevideo originates largely from soya bean meal so this increase is likely to be feed-related.

Most other serovars remained at comparable levels to the previous year or declined. Notable reductions include S. Ohio (51.6 per cent decrease from 95 positive flocks in 2010 to 46 positive flocks in 2011) and S. Livingstone (40.5 per cent decrease from 79 positive flocks in 2010 to 47 positive flocks in 2011), which may have contributed to their reduction in chickens overall.

There were two reports of S. Infantis in 2011, which is the first time this serovar has been detected in the broiler NCP. As per S. Montevideo, there has been no comparable increase among laying chickens or turkeys, but the increase does correlate with a rise of this serovar in feed (including poultry feed) and dairy cattle in 2011. S. Infantis has been associated with imported brewer’s yeast so this increase may also be feed-related.

The other predominant serovars identified in broilers are also most likely to be associated with contamination of feed (e.g. S. Ohio and S. Mbandaka) or hatchery equipment (e.g. S. Senftenberg and S. Livingstone). One broiler flock was found to be infected with S. Schwarzengrund in 2011, which was last recorded in chickens in 2006.

An estimated 33,116 broiler flocks were tested according to the requirements of the Salmonella NCP in Great Britain during 2011, which gives an estimated prevalence of Salmonella positive broiler flocks in Great Britain from statutory testing of 1.56 per cent (516/33,116). The estimated prevalence of the target Salmonella serovars, S. Enteritidis, S. Typhimurium and monophasic strains of S. Typhimurium, in broiler flocks in Great Britain was 0.01 per cent (3/33,116) in 2011. This compares with an estimated prevalence for all Salmonella serovars of 1.58 per cent in 2010 and 1.34 per cent in 2009, and an estimated prevalence for the regulated serovars of 0.03 per cent for 2010 and 0.04 per cent for 2009. This is well below the target of one per cent specified in the legislation.

Further Reading

You can view the full report by clicking here.

For the summary of the AHVLA report, click here.

For the chapter on Salmonella in feedstuffs, click here.



September 2012
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