Use of a systematic review to assist the development of Campylobacter control strategies in broilers


A. Adkin, Veterinary Laboratories Agency (VLA), Woodham Lane, Weybridge, Surrey KT15 3NB, UK


Aims:  Produce an evidence-based ranking of the major contributing factors and sources of Campylobacter occurrence in broilers produced in England, Scotland and Wales – Great Britain (GB).

Method and Results:  Relevant data were extracted from 159 research papers and findings were grouped into 14 sources of on-farm contamination and 37 contributing factors. A relevancy score was developed to take into account various measures from each study of applicability to GB broilers and strength of findings. Results indicate that major sources of Campylobacter include a depopulation event, another house on-farm, on-farm staff, and other animals on farm. The depopulation schedule (staggered slaughter) and multiple houses on-farm were identified as contributing factors associated with increasing the risk, and those decreasing the risk were use of a hygiene barrier, parent company and certain seasons of rearing.

Conclusions:  Although the review was more resource intensive compared to narrative studies, the system allows an increased level of transparency and the ability to investigate patterns and trends.

Significance and Impact of the Study:  This paper provides the first evidence-based ranking of the major sources and contributing factors for Campylobacter presence in broilers in GB using a systematic review.


Campylobacter is well recognized as one of the major causes of food-borne gastro-enteritis in humans in many countries around the world (Tauxe 2002). In England and Wales the recorded incidence in 2002 of Campylobacter was over 46 000 cases (PHLS 2003). The development and implementation of control strategies in the food chain to reduce the number of human cases is a governmental concern in many countries. However, the relative contribution of different parts of the food chain is unclear. Epidemiological surveys indicate that poultry is a major contributor but it is unclear which on-farm control strategies would be most effective. A comprehensive literature review was conducted to identify relevant data. From this, it was recognized that a vast amount of information has been generated investigating and identifying sources and contributing factors associated with Campylobacter in broilers in Europe and elsewhere. Various on-farm sources for Campylobacter infection have been identified, but for current Great Britain (GB) broiler production systems there was no clear consensus as to the major sources or contributing factors of this organism on-farm (Newell and Fearnley 2003; Mead 2004). A systematic review to investigate the literature on Campylobacter control strategies in broilers was carried out and is described in this paper.

A systematic review, developed by the biomedical industry, is a scientific method that locates, appraises and groups evidence from primary studies. Comprehensive guides are available for assistance in conducting systematic reviews, for example Centre for Reviews and Dissemination (CRD 2001) and Clarke and Oxman (2003). A systematic review provides a structured process that aims to give a comprehensive profile of evidence whilst minimizing bias and errors and may or may not include meta-analysis. Examples from the medical industry can be found in the International Cochrane Collaboration (, and a few examples in veterinary science can be found, including atresia coli in cattle (Constable et al. 1997) the impact-assessment of community animal health services (Martin 2001), lameness in cattle (Hirst et al. 2002), and vector-borne parasitic infections in cats and dogs (Trotz-Williams and Trees 2003).

The aim of this systematic review was to review analytical research and to summarize descriptive information examining the sources and factors contributing to Campylobacter occurrence on broiler farms. This paper describes the review of the primary research, in order to identify the major sources and contributing factors for the target population of GB broilers. In order to assess the applicability of the data to the GB situation and its validity, a ‘relevancy score’ was developed based on a criteria list with weightings, further described here. This paper also provides the opportunity to discuss the advantages and disadvantages found in applying a systematic review and ‘relevancy’ score within veterinary assessments.

Materials and methods

Identification and retrieval of studies

The inclusion criteria were all primary research on the presence or absence of Campylobacter in broilers on-farm. All types of study design were included to maximize available data, for example, observational, experimental, cross-sectional and longitudinal, single/multivariate studies and intervention case studies. The year, language of paper, and country of study were not limiting factors.

The systematic retrieval of relevant studies involved both computerized search via published databases, hand searching, discussions with relevant experts and Internet sources, to retrieve both published and unpublished work up to May 2003. The following search terms combined with ‘Campylobacter’ were used; ‘poultry’, ‘biosecurity’, ‘on-farm’, ‘farm’, ‘broiler’, ‘flock’, ‘chicken’, ‘bird’, and ‘risk factor’. Search A included CAB Abstracts (1977 to May 2003); MEDLINE (1966 to May 2003); VetCD (1992–2002), ISI Web of Science (1981 to May 2003); ISI Proceedings (1990 to May 2003); ScienceDirect (1966 to May 2003). After investigating translation resources, published papers written in English, French, German, Italian, Portuguese, and Spanish were retrieved. Search B used the Internet search engine Google: Advanced Search (2003). For any search the first 200 returns were viewed if available. Foreign language articles based on the Roman alphabet in html format were automatically translated online.

Of the records retrieved by search A and B, each was examined for relevant data and checked for relevant citations not currently included in the review. Papers adhering to the inclusion criteria were then selected for the review. From all searches, four papers were found not to be available in GB from the British Library, Royal College of Veterinary Surgeons or Royal Veterinary College. They comprised one thesis (in press), one proceeding, and two foreign bulletin titles.

All selected documents were reviewed, and relevant information extracted and compiled in a searchable database (Access: Microsoft, 2000). Information collected included: authors, which sources or contributing factors of Campylobacter were investigated, whether the authors found that the source or contributing factor had an effect on Campylobacter occurrence, country of study, year and month of trial conducted, sample size, study design, testing methodology, and language of paper. To ensure that the papers selected and the extraction of data was conducted objectively, a colleague not previously involved in the study processed 10% of the selected papers for each step in the review independently, and the results were compared.

Data synthesis

A ‘meta-analysis’ quantitatively combining the numerical results of similar but separate studies was not an aim of the current study as the majority of papers reviewed did not provide sufficient numerical data, or the outputs were qualitative. There were a wide variety of experimental protocols included in the review making many findings not directly comparable by such quantitative methods. Therefore an alternative approach was devised that allows: (i) the findings of the research to be grouped into defined categories of contributing factors and sources and (ii) a comparative score to be allocated to each finding based on specific study characteristics that affect its applicability to GB broilers and the strength of findings. This approach allows categories of contributing factors and sources to be ranked based on a transparent set of attributes.

Entries regarding the same category were grouped. First, a distinction between ‘contributing factors’ and ‘sources’ of Campylobacter infection was made. Contributing factors were defined as those associated with the occurrence of Campylobacter but not thought to be associated with the initial cause. To be deemed as a source, the variable had to be referenced in the study or defined as being the most probable cause of the broiler infection. Second, in refining the list of contributing factors and sources categories were simplified as far as possible. For example, staggered slaughter and slaughter in multiple batches were both defined as depopulation schedule. However, certain variables could not be further reduced.

In order to categorize studies so that their findings can be compared to those from other research, an approach has been developed that provides a comparative score for each grouped contributing factor and source based on the relevance to GB and the strength of the findings of the study. The determination of the strength of the findings is influenced by many factors, and may include the sample size used, the type of evidence that links a source or factor, the main aim of the study, and the sampling methods used in the study (de Vet et al. 2001). There is also the issue with the Internet search concerning the reliability of the data, as unlike papers from journals, the documents may not have been peer reviewed prior to publication. The variables considered of most importance and therefore their relative contribution to a total ‘relevancy score’ are described in Table 1. The overall score for each entry in the database is a sum of these criteria and is then designated as either positive or negative, dependant on whether an association (+) or no association (–) was found on the occurrence of Campylobacter and that variable.

Table 1.  Relevancy score criteria list and weights to rank the findings for applicability to the GB broiler industry and internal strength of findings of the study
  1. GB, Great Britan.

  2. *Europe refers to member countries of the European Union as of January 2004 and Switzerland and Norway.

ACountry of originEuropean studies and those from the GB and Northern Ireland are of greater applicability than those conducted elsewhere due to greater similarities in broiler production systemsGB and Northern Ireland = 10
Europe* = 5
Other = 1
BSample sizeThe greater the number of farms included in the survey or sampled area, the more representative results will beTotal of number of farms sampled
1–10 = 1
11–50 = 3
51–100 = 5
101+ = 7
CStrength of associationFactors or sources linked with the occurrence of Campylobacter by molecular typing methods are of higher validity than those associated by statistical means onlyStatistical association association = 1
Molecular typing = 5
DDocument typePapers from the journal search have been peer-reviewed for scientific integrity, whereas internet articles may not have been reviewed prior to publicationJournal article article = 3
Internet documents = 1

Within each category, comprised of the grouped entries, the relevancy score is given by: inline image where RC = Relevance score for category C, Ri =  Relevance score for entry I, and NC = Number of entries in category C.

In this way, an average score for each factor or source was calculated and opposing research of equal relevance balanced out. This relevancy score was used to rank both factors and sources. Some categories were rarely identified in the literature. These results could cause bias in the ranking, particularly if highly scored. Factors and sources consisting of two entries or one entry were therefore removed from the analysis.

The relevancy score determines the rank of categories and thus may affect the conclusions of the review. In order to assess the effect of various criteria within the relevancy score, a sensitivity analysis was conducted by removing each criterion in turn from the total score, formulating and re-evaluating each category entry. The contributing factors and sources were then ranked according to each of these new tallies.

Areas of agreement and conflict in the data

Within one category, some trials find no effect from a parameter whilst others find it important or associated with Campylobacter occurrence. By reviewing the smallest fraction of opposing studies weighted by the fraction of studies reporting on that parameter, areas of agreement and conflict were ranked.


Study selection

From initial searches totalling more than 23 000 returns 159 papers (151 from reference journals within search A and eight from the Internet within search B) were identified in which primary research on Campylobacter on-farm in broilers was studied. These references are available in the bibliography supplied in the supplementary information. Figure 1 shows a flow diagram of the screening and selection process for the searches A and B. Thirty-four were found to investigate only one factor or source, whilst 39 contained multiple parameters of interest. Only five studies were identified with an intervention strategy, and 92 provided other qualitative information. Search A retrieved a number of different study designs (observational, experimental, cross-sectional and longitudinal) from various publication formats; journal articles, abstracts and conference proceedings. The information found by search B but not A consisted of on-going work with preliminary results, finished work where no resulting publication could be found and poster presentations. After screening the papers for inclusion, 74 papers provided appropriate data into the main database from studies on nearly 2000 farms with 1200 flocks.

Figure 1.

Stages of the selection process of journal papers and Internet pages

Characteristics of the studies

Of the papers selected for the database the majority were from research performed in the USA (25%). The combined European total was approximately 58%, including GB and Northern Ireland (16%), Netherlands (13%) and Denmark (9%). English was the predominant language at 93%. Of the foreign language papers included, only Portuguese, German and Italian translations were found to contain information of relevance to the study. The most popular year of publication was 2001 (23%), with a smaller peak of papers published in 1997.

Quantitative data in this field of research was provided in the form of (i) statistical associations between a contributing factor/source(s), (ii) genetic or phenotypic typing of various Campylobacter strains to identify sites harbouring the same strain that eventually occurred in the broilers, and (iii) anecdotal evidence provided by the authors arising from the monitoring. The sample size used in studies varied from 1 to 350 farms. No study investigated the levels of Campylobacter contamination associated with sites prior to the occurrence of the organism in the monitored flock. Although nonhoused poultry (for example, organic and free-range) were included in the review, almost all of studies involved housed, conventionally reared broilers.

A number of critical observations by the review team were made on the method used in the studies included in the review. The process of how farms were selected for studies was often not described, but was, where mentioned, an agreement with large poultry companies rather than the result of random selection. The number of samples taken per flock to test for Campylobacter presence was frequently given as a number per flock without detailing the mean flock size. A wide range of testing methodologies for samples was found including transport media, enrichment broths, selective agars, incubation parameters and identification techniques, often depending on the researchers involved or the year when the study was conducted.

Common foci of studies

From 74 studies identified from the review, 51 different categories were identified: 37 contributing factors and 14 sources of Campylobacter infection. The number of separate entries in the database that detailed the association or irrelevance of categories was 358. The most frequently reported, though not necessarily the most associated, contributing factors in the database were season of rearing, presence of other animals in the vicinity of the flock and litter characteristics. For sources of Campylobacter infection, the most frequently reported categories were vertical transmission, origin of water supply, and sequential spread from previous flock (carry-over).

For some categories the low number of studies involved (two or one) meant that these categories were not further analysed. These included the type of disinfectant used on house, dust removal methods, lighting programme, surface water (presence of puddles), presence of other farms nearby and visitor numbers.

Major sources and contributing factors for GB

Using the relevancy score, Table 2 lists the ranked sources and contributing factors for Campylobacter occurrence. To interpret the rank, a high positive scoring relates to an aggregated finding of an association between the category and the occurrence of Campylobacter according to the studies included, applicability to the GB poultry industry, and the strength of the reported findings. The depopulation schedule, presence of a hygiene barrier and the number of broiler houses on-farm were found to be the top ranking contributing factors, whilst a depopulation event (point of entry of infection), cross-house transfer and on-farm staff were found to be the highest ranked sources associated with Campylobacter infection.

Table 2.  Ranked sources* and contributing factors† of Campylobacter using the relevancy score‡
Contributing factorRelevancy scoreSourceRelevancy score
  1. *Surface water not included in analysis as the number of papers was below the cut off value of 2 or less entries.

  2. †Other farms, visitor numbers, lighting programme, dust removal method, and disinfectant type are not included in analysis as the number of papers was below the cut off value of 2 or less entries.

  3. ‡To interpret the rank, a high positive scoring relates to an aggregated finding of an association or effect caused by the category by studies that are of relevance to the GB broiler industry and strength of findings. High negative scoring relates to an aggregated finding that the category has little bearing on Campylobacter occurrence by studies.

Depopulation schedule14·17Depopulation event12·70
Hygiene barrier10·13Cross-house transfer11·67
Multiple houses9·80On-farm staff9·14
Parent company/abattoir7·60Other livestock8·00
Season of rearing7·44Wild birds–0·71
Disinfectant footbath6·71Small mammals–4·10
Outside access6·40Insect carriage–5·00
Number of staff6·00Dust/air–5·25
Water disinfection4·50Carry over–5·43
Presence of other animals2·38Vertical transmission–5·84
Age at sampling2·13Water supply–8·41
Flock stress1·50Litter–9·00
Down-time and cleaning routine0·30Feed–11·44
Insect presence–1·00  
Litter characteristics–1·64  
Age of housing/state of repair–2·67  
Clothing routine–4·00  
Performance of farm–5·33  
Staff hygiene: hands–6·50  
Medication usage–7·33  
Broiler line/sex–8·40  
Disease occurrence–10·00  
Flock size–10·38  
Floor/yard material–10·71  
Water equipment–11·13  
Feed equipment–11·50  
Rodent control–14·67  
Stocking density–14·67  
Manure routines–15·25  
Removal of dead birds–16·00  

A high negative scoring relates to an aggregated finding that the category had little bearing on Campylobacter occurrence by studies that are of relevance to the GB situation and strength of findings. The contributing factors found to have the least bearing on Campylobacter occurrence were the routines of removing dead birds, routines for manure removal and storage and stocking density. The sources, which have been identified as the least likely to cause Campylobacter infection were feed, litter and the water supply.

Areas of agreement and conflict in the data

For some categories there was total agreement between study results, such that all studies that reported on a category found it to be associated with the occurrence of Campylobacter, or that all identified research found that there was no association between the category and occurrence. Such agreement included contributing factors (depopulation schedule, manure routines, removal of dead birds, rodent control and stocking density) and five sources of Campylobacter (cross-house transfer, depopulation event, feed, litter and on-farm staff). At the other end of the scale, there were several categories where many of the findings were in disagreement, signified by the highest scores. The highest level of conflict over whether a variable is, or is not associated with Campylobacter occurrence for sources was found from vertical transmission, followed by sequential spread from previous flock (carry over). The greatest amount of conflict for contributing factors was downtime and cleaning procedure, followed by litter characteristics and presence of other animals in the vicinity.

By using the ‘disagreement’ score proposed, the resulting rank is listed in Table 3 for source categories and Table 4 for contributing factors. These tables also provide a brief description of each contributing factor and source identified.

Table 3.  Sources (13*) of infection, with the number of studies identified which found an effect or no effect on the occurrence of Campylobacter listed by score describing degree of conflict between findings from studies
SourceDescription associated with sourceTotal number of studies‘Disagreement’ score (>0 scores indicate conflict)
No effectEffect
  1. *Surface water not included in analysis as the number of papers was below the cut off value of 2 or less entries.

Cross-house transferPattern of serotypes between sheds; con-current infection on-farm030
Depopulation eventContaminated external crew, lorry, slaughterhouse crates identified as source0100
FeedIsolation from feed samples, feed mill, association with feed type900
LitterIsolation from litter samples500
On-farm staffFarmers’ boots; breach at personnel entrance070
Other livestockSerotype comparison between livestock, association with the management of other livestock (cattle, sheep, pigs)151·2
Dust/airIsolation from dust and air samples311·3
Insect carriageIsolation from on-farm insects, association with occurrence of insects in sheds522·8
Water supplyIsolation from water samples, association with origin (private, municipal, borehole, ground water, and well)1433·6
Small mammalsIsolation from rodents, other small mammals, association with occurrence of rodents in sheds734·3
Wild birdsIsolation from on-farm wild birds, association with prevalence of wild birds345·3
Carry overSequential spread in house between flock. Serotype comparison between cycles, isolation prior to chick arrival, analysis of consecutive cycles1045·6
Vertical transmissionSerotype comparison between breeders/hatchery, isolation from eggs and chicks, association with breeders/hatchery1967·9
Table 4.  Contributing factors (32*) of infection, with the number of studies identified which found an effect or no effect on the occurrence of Campylobacter listed by score describing degree of conflict between findings from studies
Contributing factorDescription associated with contributing factorTotal number of studiesDisagreements score (>0 scores indicate conflict)
No effectEffect
  1. *Other farms, visitor numbers, lighting programme, dust removal method, and disinfectant type are not included in analysis as the number of papers was below the cut off value of 2 or less entries.

Depopulation scheduleStaggered or batch slaughter practice060
Manure routinesManure equipment, removal, destination and time schedule400
Removal of dead birdsRoutine/storage of removing dead birds300
Rodent controlOperator, baiting procedure, evidence of presence, damage600
Stocking densityStocking density, floor space available300
Disease occurrenceClinical disease, general health, mortality811·13
Feed equipmentFeeder systems, feed type, supplier711·14
Flock sizeFlock size711·14
Hygiene barrierUse of change room, separating bench, chalk line and/or separate footwear171·14
Water equipmentWater equipment, drinker type711·14
Floor/yard materialShed floor material, yard material611·17
Broiler line/sexBreed, sex of broiler411·25
Outside accessEscaping and re-entering poultry, free-range, organic141·25
Parent Company/abattoirParent broiler company/abattoir141·25
Flock stressVarious bird stresses: transport time of chicks; withholding feed and water131·33
LocalityGeographical location/presence of nearby features (water, forests)311·33
Clothing routineAbsence of separate clothing211·50
Number of staffNumber and several different staff121·50
Performance of farmLow weight, production indexes211·50
Multiple housesNumber of sheds on farm, other poultry close by, staff handling other poultry282·50
Medication usageMedication used722·57
Disinfectant footbathNumber used, replenishment252·80
Ventilation/heatingTypes of climate control: room climate, ventilation fans, heating system522·80
Staff hygiene: handsHand washing, toilet facilities423·00
Season of rearingSeasonal variation; temperature, rainfall, sunshine hours3133·69
Insect presencePresence, lack of control of insects224·00
Age of housing/state of repairIncreasing age of shed, amount of structural repair required634·50
Age at samplingIncreasing age354·80
Water disinfectionWater cleaning and disinfection routines, chlorination, acidification466·67
Presence of other animalsOther livestock, domestic pets588·13
Litter characteristicsMaterial, condition, refill procedure storage time569·17
Down-time and cleaning routineTime period, cleaning routine between flocks5510·00

Sensitivity analysis of relevancy score

The importance of each of the four relevancy criteria (described in Table 1) to the overall relevancy score were analysed by completing a sensitivity analysis. This produced four new ranks of the categories, each based on three of the relevancy criteria. It was found that with any criterion absent, the ranks of the categories were very similar to the baseline rank using all four criteria. The category found most relevant did not alter, and for sources of Campylobacter, the top five categories in the baseline rank were in the top five of the new ranks with minor changes in their order.


Main findings from systematic review –Campylobacter

Study selection.  Only 74 of a total 1467 identified papers contained primary research from published journals, with the vast majority of identified papers presenting commentary on other issues or results presented elsewhere. Primary data was found to be particularly lacking for intervention studies, with only five presenting primary research. For search B, of 456 websites reviewed, only eight documents were finally selected in addition to those identified from search A.

Characteristics of the studies.  The review allowed certain trends to be analysed in the areas of country of origin, language of publication and most prolific year for publications. The finding from the review that around 25% of relevant studies had been performed in the USA may be a reflection of the size of the poultry industry in that country. In 2002, the US market share for world broiler production was 27% (USDA 2004). Although approximately 58% of studies were completed in Europe (European Union (EU), Switzerland and Norway), poultry production in the EU for 2002 amounted to only 13% of the world total (USDA 2004).

Considering the fact that scientific journals with the largest impact are written in English, it is therefore unsurprising that 93% of relevant publications were written in English. The review also revealed that there were variations between studies on sampling and testing methods, such that no two studies were the same. Unfortunately, the study sample sizes at the individual category level were too small to investigate whether differences in method were the cause of any conflicting results.

Common foci of studies.  It was found that many factors are frequently tested for their association with Campylobacter occurrence, whilst others were rarely mentioned in the papers. The frequency with which vertical transmission has been selected for investigations may reflect the initial assumption that Campylobacter epidemiology was similar to that previously found for Salmonella, where vertical transmission is an important factor (Newell and Fearnley 2003). Or it may be an indication of research into the importance of transfer mechanisms that enable control strategies to be implemented, such as increased biosecurity.

Since vertical transmission has been frequently investigated and not emerged as a major source of Campylobacter transmission, limited funding resources may be better spent investigating the contribution of other sources more rarely investigated, such as the presence of surface waste (puddles) outside broiler houses.

Most relevant factors and sources of Campylobacter infection in GB broilers.  It is interesting to note that the top three sources and contributing factors to Campylobacter occurrence are self-supporting, with a paired source and factor concerning (i) movement on farm during depopulation, (ii) between broiler houses and (iii) transfer by staff. In addition, the outcomes of this systematic review are in agreement with those from narrative reviews, for example, Newell and Fearnley (2003).

These three identified variables may be priorities included in further fieldwork. However, those contributing factors and sources with negative scores, such as routines of removing dead birds, feed and litter, have been found here to have the least bearing on Campylobacter occurrence for GB broilers, and therefore should not be the primary focus of any trials.

Analysis of agreement and conflict in the data.  Several of the results found by this analysis were not surprising. Both feed and litter were unanimously found to have no effect on Campylobacter presence. Vertical transmission, which was found to have one of the highest disagreement scores, is an acknowledged area of substantial differences in opinion in this field of research (Newell and Fearnley 2003).

Gaps in knowledge.  Quantitative information was absent on the level of Campylobacter contamination associated with the various potential sources. An advantage of this review is that it is attached to a national scale survey that has currently completed its pilot phase. In this way, certain data that have been found absent from this systematic review have been requested within the framework of the experimental on-farm testing to be conducted in GB. In addition, the systematic review performed did not include the contacting of authors for raw data or further information on their current research. It has been established from discussions with experts in this field that substantial amounts of raw data are available but have not been published due to the low impact of such a publication. In response to this finding, a separate request for data and information within Europe research groups was initiated. It may be useful to compare any unpublished information that is submitted from this request to that contained in the systematic review to evaluate the amount of useful data that goes unpublished.

Evaluation of a systematic review approach

From conducting a systematic review rather than a traditional literature review, a number of advantages have been proposed and supported by the work conducted here. The approach is a reproducible and transparent method, which can be validated. The criteria for identification, selection, assessment and integration are detailed which is not the case for narrative reviews. In this review, extracts of the database (the selection phase and extraction of data) were reviewed a second time independently by a colleague not previously involved to ensure that these processes were objectively conducted. The analysis of primary studies was completed in a manner to prevent bias. Also outputs included the characteristics of publications (country of study, year of publication, language, location, testing method), most frequently studied parameters, areas of conflict and agreement in the data and the identification of knowledge gaps. An additional output of the approach is the construction of a database, which can be easily used and transferred to other people in the field.

Although the basic principles of conducting a systematic review are the same regardless of the area of research, there are specific procedures that need adapting for veterinary applications. Within veterinary science, the literature base is smaller that that of the biomedical industry where systematic reviews are commonly conducted. Therefore, the inclusion criteria taken for Campylobacter were necessarily broad, including all descriptions of contributing factors and sources of infection on-farm, as many languages as possible, were not dependent on country of origin, all types of observation or experiment design (including nonrandom farm selection). Using this approach, there were few exclusion criteria based on the quality of methods.

Another difference from traditional biomedical reviews is that meta-analysis, or the analysis of the numerical results from each selected study, was not possible due to the great heterogeneity between the papers that were included in the review. This has been a finding from other systematic reviews that have been conducted in the field of veterinary science (Le Fevre et al. 2002; Trotz-Williams and Trees 2003), which may indicate a lack of standardized reporting structure for publications and study design to enable the pooling of appropriate results. Therefore, a relevancy scoring system was developed to enable the combining of selected findings and ranking according to their applicability to GB and the internal strength of findings and level of precision.

The relevancy score approach allows the estimation of the major contributing factors and sources whilst addressing concerns over the precision, applicability and internal strength of findings of the studies included. It has been found that the type of scale used to assess trial quality can dramatically influence the interpretation of combined studies (Juni et al. 1999). A sensitivity analysis was carried out on the score which found that the removal of any one criterion did not considerably alter the baseline rank of contributing factors or sources, which infers that no one criterion dominates the score. However, the use of any type of meta-analysis or quality scoring of results has been criticized as introducing bias (Petitti 1994; Juni et al. 1999).

To investigate the importance of language bias the number of languages that contributed to the database was assessed. It was found that although translation facilities exist, very few papers considered relevant to this study had been fully published in a language other than English. In this review, efforts have been made to reduce the effect of publication and trial bias in a number of ways: (i) a nonpublished format was included – the Internet search. However, only eight documents were included from this search, compared to 151 published papers. (ii) Using the relevancy score, an average score for each factor or source was calculated to remove the potential bias from the number of publications concerning one category. However, despite all efforts to prevent bias, the quality of the results produced by this approach cannot exceed the quality of the reported information from the individual studies it contains (Shapiro 1994).

Although there are major drawbacks to conducting a systematic review, such as the considerable amount of time and labour required, there are proven advantages of conducting a systematic review as opposed to a traditional narrative review. This is the first systematic review of the major risk factors and sources of Campylobacter infection in broilers. The findings of this review are being used to assist the development of practical control measures for Campylobacter in GB broiler flocks.


The authors wish to thank staff of the Veterinary Laboratories Agency Library for their invaluable help in retrieving references. This work was funded by the Department of the Environment, Food and Rural Affairs.