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. 2023 Feb 9;102(5):102566. doi: 10.1016/j.psj.2023.102566

A systematic review and meta-analysis of the sources of Salmonella in poultry production (pre-harvest) and their relative contributions to the microbial risk of poultry meat

J Wang *, S Vaddu *, S Bhumanapalli *, A Mishra †, T Applegate *, M Singh †, H Thippareddi *,1
PMCID: PMC10074252  PMID: 36996513

Abstract

Salmonella is a major foodborne pathogen associated with poultry and poultry products and a leading cause for human salmonellosis. Salmonella is known to transmit in poultry flocks both vertically and horizontally. However, there is a lack of knowledge on relative contribution of the factors on Salmonella prevalence in poultry live production system including hatchery, feed, water, environment-interior, and -exterior. Therefore, a systematic review and meta-analysis was conducted to quantify the potential sources of Salmonella during preharvest and their relative contributions to the microbial risk of poultry meat. A total of 16,800 studies identified from Google Scholar and 37 relevant studies were included in the meta-analysis for relative contributions to Salmonella positivity on broilers after applying exclusion criteria. A generalized linear mixed model approach combined with logit transformation was used in the current study to stabilize the variance. The analysis revealed that the hatchery is the most significant contributor of Salmonella with a prevalence of 48.5%. Litter, feces, and poultry house internal environment were the other 3 major contributing factors with a prevalence of 25.4, 16.3, and 7.9%, respectively. Moreover, poultry house external environment (4.7%), feed (4.8%), chicks (4.7%), and drinker water also contributed to the Salmonella positivity. Results from this meta-analysis informed the urgent need for controls in live production to further reduce Salmonella in fresh, processed poultry. The control strategies can include eliminating the sources of Salmonella and incorporating interventions in live production to reduce Salmonella concentrations in broilers.

Key words: preharvest, broiler chicken, Salmonella, contributing factors, meta-analysis

INTRODUCTION

Poultry meat, specifically chicken meat has gained significant market share in the United States (US) compared to beef and pork (USDA, 2021) and the consumption is gradually increasing worldwide. Several factors have contributed to this increase in market share, including the significant progress in knowledge on the genetics of the bird, nutritional requirements and production practices, resulting in significant reduction in production costs, consequently making chicken meat more affordable for the population. While this is true, poultry has been recognized as a major source of foodborne pathogens, specifically Salmonella and Campylobacter and causes significant morbidity in the US and worldwide. In 2018, FoodNet identified 25,606 infections, 5,893 hospitalizations, and 120 deaths due to foodborne sources (Tack et al., 2019). Salmonella and Campylobacter continue to be major foodborne pathogens resulting in majority of the foodborne illnesses and are reported to contribute approximately 73.4% of foodborne infections, 71.7% of hospitalizations, and 55% of the total number of deaths due to foodborne illnesses in the US (Figure 1; Tack et al., 2019).

Figure 1.

Figure 1

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Percentage of foodborne outbreaks caused by Salmonella and Campylobacter by food category.

These microorganisms can gain entry into the ecosystem of the bird's gut through a variety of sources, including feed, water, litter (fresh vs. reused), pests (including darkling beetles), rodents, surrounding environment (wild birds) and colonize the gastrointestinal tract of the bird. Once the colonization occurs, it is not practically possible to eliminate these microorganisms from the bird gut and microorganisms eventually contaminate the poultry meat during processing due to cross-contamination at multiple steps of poultry processing. The only opportunity to reduce the risk from these foodborne pathogens is to reduce their population on the bird (surface) and in its gut.

In spite of the numerous antimicrobial interventions that the poultry processors have incorporated during processing, Salmonella and Campylobacter prevalence on the whole carcasses as well as chicken parts remains an issue. Thus, there is a need to reduce the concentrations and prevalence of these microorganisms in the poultry gut to further reduce their prevalence in the poultry meat. While numerous preharvest strategies (nutritional, immunologic [vaccines], competitive inhibition, etc.) have been evaluated and implemented, a comprehensive solution to eliminate these microorganisms or prevent their colonization of the gut remains elusive. Regardless, poultry producers have incorporated numerous strategies at preharvest stage, although these strategies are not highly effective on their own. Collectively, they have been relatively successful in reducing the prevalence of the microorganisms.

Poultry production has gone through significant changes, for example the increase in the no antibiotics ever (NAE) market, requires producers to reduce and/or eliminate inclusion of sub-therapeutic levels of antibiotics placing pressure on the production system to find alternative methods to control microorganisms (such as Eimeria and Clostridium perfringens) in the ecosystem of the bird's gut during production. These changes include improvements in management practices such as biosecurity and hygienic measures at the production farms, litter management, use of nutritional strategies to include organic acids, botanicals, bacteriocins, bacteriophages, novel compounds and feed additives, pre- and probiotics, immunization through oral or vaccination, etc.

Regardless, the sources of foodborne pathogens and their relative contribution to the prevalence and concentrations of these foodborne pathogens on the bird and in the gut should be understood to better target intervention strategies. This systematic review and meta-analysis will evaluate the role of each of those contributing factors: chicks (from hatchery), biosecurity, feed, water, litter (fresh vs. reused), pests (including darkling beetles), rodents and the surrounding environment (wild birds) on Salmonella prevalence and concentrations in birds presented for harvest.

MATERIALS AND METHODS

Literature Search

A systemic review process adapted from Aiassa et al. (2015) was conducted to address the specific question:

  • •

    What are the contributing factors, in order of prominence for Salmonella colonization in broilers on the farm during grow-out?

A detailed literature search was performed in Google Scholar for studies published from 1970 to January 2022. The following keywords were used to address the research questions mentioned earlier: Salmonella, detection, prevalence, and broiler. There were 16,800 studies identified from Google Scholar. Additional studies (n = 3) were identified from the review articles. Peer-reviewed articles, governmental agency reports, master's thesis, and doctoral dissertations were also included.

Inclusion Criteria

Titles and abstracts of the studies identified through the keyword search were screened to determine whether they were appropriate for current research questions mentioned earlier. Articles had to include prevalence data on Salmonella in commercial broiler live production environment to pass the first criterion. Challenge studies or feed additive-related studies were excluded from the results. Studies were reviewed by full text if the title and abstract failed to present adequate information to include or exclude in the analysis. Full-text articles were obtained for all remaining studies and screened for whether the sample size and the prevalence and/or positive samples were reported. Additionally, this meta-analysis has a specific emphasis on risk factors that are present in the US. Therefore, regions of the studies were identified during the screen process and listed as US and non-US. Only studies with the reputable and replicable microbiological methods were determined appropriate for use in the meta-analysis. Thus, scores were not assigned to individual studies due to the problematic nature of incorporating study quality scores as factors in meta-analysis (Juni et al., 1999; Herbsion et al., 2006).

Data Extraction

Eligible articles that passed the screening were included in quantitative and qualitative analysis (n = 39). The quantitative variables included the number of positive samples and sample size. In cases where positive sample number was absent, and the prevalence was reported, the positive samples were calculated by multiplying the prevalence by the reported sample size and rounded off accordingly. Studies with inconsistent results through the text or figures were excluded.

Qualitative data included the regions where the study was performed, type of broiler production, sample source (contribution factor), and detection method were extracted from the studies. The regions were classified as US and non-US based on the materials and methods section in articles or inferred by address of authors. The type of broiler production is classified as conventional, NAE, and alternative. Unless the article specified that samples were collected from the alternative (including organic and pasture-raised) or NAE system, the system is marked as conventional. Samples source from broiler live production section was further divided into feces (e.g., feces or cecal samples, or cloacal swabs), litter (e.g., litter, boot socks, or drag swabs), chicks, hatchery, water, feed, interior environment (e.g., rodents, darkling beetles, fan surfaces, feed trough or mice), exterior environment (e.g., water puddles, wild birds, soil, grass, or poultry house outside surface swabs). Detection method, whether it was selective enrichment or direct plating was also noted for each study.

Data were grouped by sample source and regions after extraction. Each subgroup is required to have at least two independent studies to be considered for use in the meta-analysis. If there is only 1 usable study in the subgroup, then the specific prevalence or positive sample number is reported. All data are stored in Microsoft Excel Worksheet (Microsoft, Redmond, WA).

Quality Assessment of Data

Quality scores were not estimated for the studies included in this meta-analysis. Previous research has reported that these types of scores can affect the interpretation of meta-analyses and may create their own selection bias (Herbison et al., 2006; Stone et al., 2019).

Data Analysis

All data analysis was conducted using R version 4.0.2 (R Core Team 2019). The metafor package (Viechtbauer, 2010) was used to generate the meta-analysis statistics and forest plots. Due to the essence of prevalence results following a binomial distribution (positive or negative), a generalized linear mixed model approach combined with logit transformation was used in the current study to stabilize the variance (Freeman and Tukey, 1950). The prevalence of Salmonella was first transformed using the logit transformation:

logitp=ln(p1−p)

with variance

var(logitp)=1Np+11−Np

where p is the prevalence of Salmonella reported in a study and N is the sample size of that study.

To identify the most influential contribution factor or source of Salmonella positivity, data were grouped by the sample source. For our specific interests within the US, data for each sample source were partitioned based on regions to allow for subgroup analysis. A random intercept logistic regression model was then fitted to each subgroup to estimate the population prevalence and its 95% confidence interval (CI) as well as describe statistics between-study variance τ2 (Higgins et al., 2019) and heterogeneity I2. The I2 values of 25, 50, and 75% were considered as low, medium, and high measures of heterogeneity, respectively.

Test for Publication Bias Due to Small-Study Effects

There are limitations in using the funnel plots to statistically quantify the publication bias. The previous research (Ioannidis and Trikalinos, 2007) recommends to conduct such tests only when there is a sufficient number of studies (n ≥ 10) and low heterogeneity (I2 < 50%). Unfortunately, none of the analyses examined in this study met both these criteria, so publication bias could not be appropriately assessed.

RESULTS AND DISCUSSION

Several sources of Salmonella exist in the broiler production, including the environment (exterior to the poultry house), poultry feed, hatchery for the chicks, chicks, environment in the poultry house, drinker water, feces or bird droppings and litter in the poultry house (Figure 2). The prevalence of Salmonella from each of these sources was determined from literature. The systematic review process outline is presented in Figure 3. A total of 16,800 studies were identified on Google Scholar and 3 additional studies were retrieved from the manual search. A total of 16,312 studies were excluded from the search as they were either feed additive-related manuscripts or review papers, with no original data. Results on feed and water samples from the study of Rama et al. (2022) was retrieved from the PhD dissertation. A total of 44 studies were fully reviewed and 3 of them were missing the sample size whereas one of them was missing the prevalence or positive numbers.

Figure 2.

Figure 2

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Sources of Salmonella colonization of broilers in a poultry house.

Figure 3.

Figure 3

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Flow diagram of the systematic review process.

In total, there were 42,341 samples from 39 studies in the final meta-analysis. A brief summary of the 39 studies are listed in Table 1. The sample source from each study was further partitioned to different contribution factors shown in Table 2.

Table 1.

Summary of live production studies used in the meta-analysis.

Production Country Sample source Detection method No of positive samples Sample size Reference
NR Japan Cecal content, eggshell SE 338 2,372 Limawongpranee et al.,1999
NR Japan Cecal content, litter, floor swab, feed, chick papers, water, mouse SE 440 1,264 Limawongpranee et al.,1998
Organic US Feces, feed, water SE 13 300 Alali et al., 2010
Conv. US Feces, feed, water SE 115 400 Alali et al., 2010
NR US Droppings, intestinal content, cloacal swab DP 10 119 Craven et al., 2000
NR US Feces, paper pads, water line, mouses, litter, wall swab, fans, and environment sample SE 849 8,739 Bailey et al., 2001
NR US Feces, hatchery, eggshell, fluff, litter, water SE 236 519 Bailey et al., 2002
NR US Litter PCR 28 47 Liu et al., 2002
NR US Feces, hatchery, environment, litter, water SE 196 1302 Waltman et al., 1993
NR US Feed, hatchery DP 153 345 Davies et al., 1997
NR US Litter, feces SE 47 516 Corrier et al., 1999
NR US Litter, hatchery SE 167 896 Byrd et al., 1999
NR Australia Litter SE 17 288 Kingston, 1981
NR US Litter SE 110 300 Byrd et al., 1997
NR US Egg fragments from hatchery SE 132 175 Cox et al., 1990
NR US Egg fragments from hatchery SE 91 350 Cox et al., 1997
NR US Litter, feed, dust SE 13 77 Bhatia et al., 1979
NR US Hatchery SE 103 540 Bailey et al., 1994
NR US Boot socks, drag swab, feces, litter SE 13 77 Berghaus et al., 2013
Conv. US Litter SE 131 433 Siemon et al., 2007
Pasture US Litter SE 89 530 Siemon et al., 2007
Conv. US Feces, feed, water, swab inside, swab outside, grass SE 76 2,400 Thakur et al., 2013
Conv. US Drag swab SE 37 68 Higgins et al., 2008
Conv. US Drag swab, litter SE 33 136 De Rezende et al., 2001
Conv. S. Korea Cloacal swabs, cecal dropping, next boxes, wall dust, hatchery SE 24 49 Kim et al., 2007
NR Spain Dust, water, boots, beddings, feces, chicks SE 111 754 Marin et al., 2011
NR US Drag swab, feed, water, litter, dust, mice, chicks SE 255 2,320 Liljebjelke et al., 2005
Conv. Chad Droppings, litter, feed, water SE 9 16 Tabo et al., 2013
Conv. US Cloacal swabs, litter, feed, water SE 133 1,584 Shang et al., 2018
Conv. US Litter, drag swab SE 114 608 Volkova et al., 2009
Conv. US Rectal swabs, fresh feed, trough feed, soil, litter SE 19 3,200 Rodriguez et al., 2006
Conv. US Feed NA 38 121 Jones, 2008
Conv. US Feed SE 15 80 Whyte et al., 2003
Conv. US Cloacal swabs, litter, drag swabs SE 1,100 9,210 English, 2015
Conv. US Environmental swabs, diagnostic specimen SE 29 180 Roy et al., 2002
Conv. US Feces SE 11 40 Bailey et al., 2020
Organic US Feces SE 28 40 Bailey et al., 2020
Conv. US Litter SE 28 40 Gu et al., 2019
Conv. and Organic US Litter, feed, water SE 62 120 Sapkota et al., 2014
Pastured US Feces, litter SE 173 846 Hwang et al., 2020
NAE US Litter, water, feces, feed SE 100 492 Rama et al., 2021
NR Denmark Beetles, boots, fecal droppings SE 67 448 Skov et al., 2004
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Abbreviations: Conv., conventional; DP, directed plating; NAE, no antibiotics ever; NR, not reported; SE, selective enrichment; US, United States.

Table 2.

Contribution factor of Salmonella of broiler live production.

Contributing factor Sample type from studies
Feces (Excreta, which includes feces and urine) Intestine content, cecal content, feces, droppings, and cloacal swabs
Litter Drag swab, litter, and boots
Hatchery Egg shells and fluffs inside hatcher, tray liner swab, eggs, and setter area swabs
Chicks Paper liners, meconium, boxes, and eggshells in trays
Feed Fresh feed
Drinker water Drinker water
Environment-exterior Soil, standing water, puddles, grass, and outside swabs
Environment-interior Mouse, flies, darkling beetles, fan swabs, inside swabs, floor swab, insect, wall swab
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Contributing Factors

Meta-analysis model was constructed to assess each contributing factor (Table 2). From the pooled Forest Plot (Figure 4), feces (excreta), litter, feed, water, hatchery, poultry house exterior and interior environment contributed to the overall predicted Salmonella prevalence (P < 0.01). Hatchery, litter, and feces rank top 3 contributing factors in broiler live production.

Figure 4.

Figure 4

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Summary forest plot for all sources of Salmonella colonization of broilers in a poultry house.

Meta-analysis models were constructed for each contribution factor by the location of study conducted, whether in the US or other countries (non-US; Table 3). A detailed discussion of each contributing factor and predicted Salmonella prevalence is provided below.

Table 3.

Meta-analysis results for Salmonella prevalence from different sources throughout broiler live production.

Source Region No. of reports Population prevalence (95% CI) τ2 I2
Feces US 14 0.125 (0.070–0.216)a 1.50 98.1
Non-US 7 0.251 (0.161–0.370)b 0.42 95.6
All regions 21 0.163 (0.106–0.243) 1.29 97.7
Litter US 20 0.254 (0.166–0.370) 1.48 97.0
Non-US 6 0.253 (0.097–0.518) 1.86 97.9
All regions 26 0.254 (0.172–0.358) 1.57 97.1
Hatchery US 5 0.488 (0.272–0.708) 1.93 97.7
Non-US 3 0.463 (0.311–0.622) 1.55 97.8
All regions 8 0.485 (0.328–0.645) 1.87 97.7
Chicks US 4 0.065 (0.039–0.105) 0.23 92.3
Non-US 1 0.074 (0.019–0.252) NA NA
All regions 5 0.047 (0.006–0.284) 0.21 89.7
Environment US 6 0.028 (0.017–0.157) 2.17 97.0
-interior Non-US 4 0.146 (0.046–0.379) 1.48 93.8
All regions 10 0.079 (0.032–0.181) 2.18 96.7
Environment US 4 0.017 (0.004–0.071)a 1.48 95.6
-exterior Non-US 1 0.530 (0.007–0.721)b NA NA
All regions 5 0.047 (0.006–0.284) 4.42 98.4
Feed US 9 0.067 (0.007–0.138) 4.66 92.8
Non-US 6 0.095 (0.020–0.352) 2.90 66.3
All regions 15 0.048 (0.014–0.147) 2.14 89.9
Water US 6 0.012 (0.002–0.056) 1.62 72.8
Non-US 3 0.031 (0.019–0.049) NA NA
All regions 9 0.020 (0.009–0.043) 0.58 61.1
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Abbreviations: CI, confidence interval; NA, not available; US, United States.

a,b

Different superscripts-mean the estimated pooled prevalence significantly different for regions (P < 0.1).

Poultry House Environment—Exterior

The poultry house external environment and upkeep can play a significant role in the effectiveness of biosecurity measures to minimize the risk of Salmonella entry into the poultry house environment. These measures can include personnel/visitor requirements, presence and contact with other farm and domestic animals, cleaning and sanitation of the poultry house environment, as well as equipment used within or outside of the poultry house and vehicles visiting the farm. Strict implementation of biosecurity measures can limit the introduction and spread of disease as well as microorganisms such as Salmonella and Campylobacter within and across the flocks on a farm.

Poultry house environment (external) can be a source of Salmonella, including the soil, standing water or puddles, presence of grass and agricultural lands in the vicinity of the poultry house as well as farm animals such as beef or dairy cattle, sheep, goats and other ruminants, wild birds, etc. are known reservoirs of the foodborne pathogens Salmonella and Campylobacter. Further, Salmonella can persist in soil for extended periods of time based on the soil properties, sun light, temperature fluctuations, presence of organic material, etc.

The predicted Salmonella prevalence in the poultry house environment (external environment, e.g., water puddles, wild birds, soil, grass, or poultry house outside surface swabs) was 4.7% (95% CI: 0.6–28.4%), with an overall heterogeneity of 98.4%, indicating differences Salmonella prevalence between studies (Figure 5).

Figure 5.

Figure 5

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Forest plot for environment-exterior as a source of Salmonella colonization of broilers in a poultry house.

Poultry Feed

Poultry feed has been implicated in several cross-continental spread of Salmonella over the years. Poultry feed ingredients are sourced from various locations and if there has been an exposure to livestock or wildlife fecal material, these ingredients can be sources of Salmonella in the finished poultry feed. Poultry feed contains ingredients, grain, milling byproducts, rendered animal byproducts, vitamin and mineral supplements and fats and oils (Food Drug, 2019). While the risk of Salmonella from these sources can vary significantly, with vitamin and mineral supplements being free of Salmonella due to the manufacturing process, others such as animal byproducts, grains, and occasionally fats and oils can be sources of Salmonella to varying degrees.

Depending on the type of feed (mash vs. pellet) and the processing conditions such as conditioning and pelleting temperatures, the manufacturing process can contribute to reducing the Salmonella populations or prevalence based on the concentrations in the ingredients. Salmonella can persist for extended periods, over years in poultry feed processing environment such as in feed mills, grain stores, feed bins, etc. and once it gets established in such environment can be difficult to eradicate (Davies and Wray, 1997).

Parker et al. (2022) reported a combined prevalence of Salmonella in raw feed components to be 18%, with finished feed at 9% and milling equipment to be 8%. This indicates that the raw materials were the main source of Salmonella, with the manufacturing process reducing the prevalence although it cannot be concluded whether the Salmonella prevalence in the finished feed was due to survival during the manufacturing process or recontamination from the feed mill environment. Further, the authors reported that the risk of Salmonella prevalence in animal-based byproducts was 3.9 times greater than plant-based raw feed components (cereal feed such as soy, corn, and dried forage and meals, etc.). The Salmonella prevalence in precook equipment was 1.5 times greater than the risk of detection in post-cook equipment, indicating that the post-cook equipment is more sanitary, although not free of Salmonella—an important risk for recontamination of the animal feed (Parker et al., 2022).

The Salmonella prevalence in poultry feed ranged from 0 to 100% across all the studies, with feed from US studies ranging from 0 to 40% and non-US studies ranging from 0 to 100% (the 100% prevalence was reported in 1 study with only 2 samples analyzed). The predicted Salmonella prevalence in the poultry feed across the regions was 4.8% (95% CI: 1.4–14.7%), with an overall heterogeneity of 89.9%, indicating significant differences between the studies (Figure 6).

Figure 6.

Figure 6

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Forest plot for feed as a source of Salmonella colonization of broilers in a poultry house.

Hatchery

Hatcheries today are highly automated and have high throughput of eggs and chicks and can contribute to the spread of Salmonella through the chicks. Introduction of large amounts of airborne fluff and dust generated during hatching process was shown to be the primary source of Salmonella contamination of broilers (Bailey et al., 1992). As a consequence, the hatcher air subsequent to hatching probably carries Salmonella to the immediate environment and consequently the rest of the hatchery. Carpenter et al. (1986) demonstrated the importance of dust in poultry areas as a transport mechanism for potential disease-causing organisms. They showed that reducing airborne dust in a poultry room by a factor of two reduced airborne bacteria by a factor of 100.

Salmonella has been recovered from several surfaces and the air in hatcheries, including hatchers, chick handling areas, cleaning equipment, setters, egg transfer areas, and service areas. Withenshaw et al. (2021) reported Salmonella prevalence of 6% in all samples tested (6,990 total samples) in 22 hatcheries in Great Britain, with at least 1 sample positive for Salmonella in 77% of the hatcheries. The positive samples per hatchery varied from 0 to 33.3%, indicating that proper cleaning and sanitation and probably design of the hatchery should address Salmonella contamination of surfaces. In addition, the positive samples varied by hatchery area, with 0.3% positive in egg areas to 18.7% in waste areas. The hatchery characteristics and practices that contribute to a higher risk of Salmonella contamination include: 1) greater number of hatchers in regular use, 2) storing trays in the process room, 3) drying set-up trolleys in the corridor, and 4) skips located in an enclosed area (Withenshaw et al., 2021).

The prevalence of Salmonella in hatcheries ranged from 19 to 75%, with samples being eggshells and fluff inside the hatcher, tray liners, eggs, and setter areas. The predicted prevalence of Salmonella in hatchery equipment surfaces, eggs, tray liners, eggshells, and the fluff was 48.5% (95% CI: 32.8–64.5%) with a heterogeneity of 97.7%, indicating differences between hatcheries and studies (Figure 7). These differences could be due to difference in the surfaces and equipment sampled or true differences in Salmonella prevalence between hatcheries as reported by Withenshaw et al. (2021).

Figure 7.

Figure 7

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Forest plot for hatchery as a source of Salmonella colonization of broilers in a poultry house.

Chicks

Whereas vertical transmission of Salmonella from the egg to the progeny is possible, the majority of the infection and subsequent colonization probably occurs on exposure to the Salmonella in the air during incubation and hatching or through the oral route via ingestion of Salmonella contaminated membranes and other egg material. Wilding and Baxter-Jones (1985) isolated salmonellae from 1 out of approximately 10,000 commercial hatching eggs examined over several years and estimated 1 Salmonella-positive egg out of every 1,000 or 2,000 based on recovery from small groups of newly hatched chicks.

Contamination (experimental) of the egg shell surfaces with Salmonella-inoculated feces resulted in majority of the chicks being positive for Salmonella, indicating the respiratory system as the primary pathway for entry. Further, day-old chicks are more susceptible to Salmonella colonization compared to 3-day old chicks by either oral or cloacal inoculation (Cox et al., 1990). Cason et al. (1994) reported 85% of the chicks were positive for Salmonella when the eggs were inoculated prior to incubation (by immersing in Salmonella inoculum of ca. 8 log CFU/mL), and 77% of the chicks were positive for Salmonella that contained both inoculated eggs and noninoculated eggs. The Salmonella incidence in the chicks was 81% and 80% from the noninoculated eggs that were placed in a tray above and below the mixed tray that contained both inoculated and noninoculated eggs. From control eggs, 44% of digestive tracts of hatched chicks were positive, indicating that Salmonella in a contaminated hatcher can reach the gut of chicks hatching from Salmonella-free eggs before they are removed from the hatcher.

Thus, chicks can be contaminated with Salmonella, either on the surface, the respiratory tract or the gastrointestinal tract. Whereas the rate of contamination of the chicks may not be as dramatic as demonstrated by Cason et al. (1994) resulting from lower concentrations of Salmonella on the egg shell surface due to natural contamination of the egg shells, the probability of chicks with Salmonella in their systems is relatively high. It is possible that these Salmonella-positive chicks further spread the microorganism when they are placed in poultry house and act as seeder birds.

The prevalence of Salmonella in chicks ranged from 7 to 12%, with very few studies (5; 4 from US and 1 from non-US) reporting Salmonella prevalence in a commercial setting. The discrepancy between the high Salmonella prevalence in hatcheries and the hatchery environment, specifically the hatching cabinet being the primary source, is probably due to the low concentrations of Salmonella in the chicks when sampled (d-0). Bailey et al. (1994) showed that while only 4.8% of the chicks were positive by sampling the intestines, 29.4 and 23.2% of the birds (cecal samples) were positive by d 7, indicating that the chicks have greater Salmonella positive rates than is evident through intestinal sampling.

The predicted prevalence of Salmonella in chicks was 4.7% (95% CI: 0.6–28.4%), with a heterogeneity of 89.7% (Figure 8). The number of studies and data were inadequate to evaluate differences in Salmonella prevalence between chicks hatched in the US and non-US locations.

Figure 8.

Figure 8

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Forest plot for chicks as a source of Salmonella colonization of broilers in a poultry house.

Poultry House Environment—Interior

Poultry production environment is replete with vectors for Salmonella including rodents, pests (darkling beetles), flies and other environmental surfaces such as fan blades, floors and walls and those that are exposed to dust containing Salmonella. While each can be a source of Salmonella and its colonization of the birds, literature on each of the specific sources and prevalence of Salmonella is limited. Thus, in the current meta-analysis, the sources of Salmonella were grouped and considered together in evaluating the risks for Salmonella colonization of the birds during grow-out.

Darkling beetles: Alphitobius diaperinus, known as the lesser mealworm beetle, darkling beetle, black beetle, or litter beetle is common in poultry production environments, including turkey and broiler operations (Axtell, 1994; Lambkin, 2001). The open floor housing and deep litter provide optimal habitat for the insects to establish, reproduce and develop (Axtell and Arends, 1990).

Salmonella-infected darkling beetles ingested by broiler chicks can colonize the gastrointestinal tract and spread Salmonella to other non-exposed chicks (Roche et al., 2009). The darkling beetles present in broiler environment can present a significant risk of colonization by the chicks and the birds during grow-out. Moraes et al. (2016) reported Salmonella prevalence of 25% in darkling beetles in layer farms using qPCR method but Chernaki-Leffer et al. (2002) failed to isolate Salmonella from darkling beetles using conventional isolation method in broiler farms. However, Segabinazi et al. (2005) and Hald et al. (1998) reported Salmonella prevalence of 0.37% (54 samples) and 45% in mealworm samples, collected from broiler farms during placement of the chicks and subsequent to transportation of the birds to the processing plant, confirming the potential risk of Salmonella exposure to future flocks raised on the same litter.

Rodents (Mice): Rodents are probably considered to be one of the most versatile pests. While majority of the broiler farms employ commercial pest control operations, some farms practice their own pest control measures. Literature indicates mice can be a significant source of Salmonella as they consume the same feed and defecate in the same environment (poultry litter) as the birds. Contaminated rodent feces can be ingested by the birds as they coprophagic, resulting in Salmonella colonization among the birds and subsequent spread.

Within poultry farms, infected rodents are often reported, with Salmonella prevalence of 5.3% (Jones et al., 1991). The risks of rodents regarding Salmonella persistence in poultry houses have been evaluated in only a few studies in broiler breeder and layer breeder houses in the UK (Davies and Wray, 1995). Camba et al. (2020) reported persistent prevalence of Salmonella in the gastro-intestinal tract of roof rats in a commercial layer farm in Japan, with rates ranging from 0 to 40%, over a 9-yr period. Bailey et al. (2001) reported Salmonella prevalence of 18.7% (of 150 samples) in flies within the poultry production environment, indicating the importance of this vector in transmission of Salmonella in poultry production.

Other interior environment: While other environmental surfaces in the poultry house have been positive for Salmonella such as fan blades, interior walls, floors and walls, these may be resulting from deposition of contaminated dust or a consequence of cross-contamination from other sources. While these surfaces may indicate prevalence of Salmonella, multiplication of the microorganism may not occur and may rather be an indicator of Salmonella prevalence in the poultry house and the birds.

Predicted Salmonella prevalence in the poultry production environment (interior) that included vectors such as mice, flies, darkling beetles and other insects and environment surfaces such as fan blades, poultry house inside surfaces such as floors and walls was 7.9% (95% CI: 3.0–18.0%, Figure 9). There were no differences between the Salmonella prevalence in the poultry production environment (interior) between US and non-US environment. High heterogeneity (I2≥96.7%) was observed between the US and non-US regions, indicating variability in Salmonella prevalence.

Figure 9.

Figure 9

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Forest plot for environment-interior as a source of Salmonella colonization of broilers in a poultry house.

Water

The water supply in poultry production operations is mostly through well water that is treated and the recommendation is to provide potable water for the birds. In majority of the cases, Salmonella contamination of well water is minimal and any treatment of the water further reduces the risk of foodborne pathogens in the water supply. However, water can get contaminated in the poultry house with birds drinking out of the drinking cups or the nipples and Salmonella and Campylobacter have been isolated from these sources.

A combination of optimal temperature (ca. 25°C), low flow rates and adequate nutrients make the drinking water in poultry houses ideal for microbial contamination and formation of biofilms, making disinfection less efficient. The prevalence of Salmonella in drinking water ranged from 0 to 11%, with the differences probably due to the location of sampling, whether the water was collected from the water main directly or at the drinker nipples or cups. Also, the method of sampling could introduce variability with regards to the prevalence, with larger volumes of collection resulting in higher prevalence. Bailey et al. (2001) collected the water samples using a sterile swab or cotton tipped applicators (4–5), by inserting the applicators into the water line at the ends of the line or by swabbing the drinking nipples or cups. While Salmonella contamination of water can spread the microorganism and consequently, colonization of the birds, it is probably not the primary source of Salmonella in a poultry house.

The prevalence of Salmonella in poultry water was 0 to 11% across all the regions, with predicted prevalence of 2.0% (95% CI: 0.9–4.3%) and an overall heterogeneity of 61.1% (Figure 10).

Figure 10.

Figure 10

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Forest plot for drinker water as a source of Salmonella colonization of broilers in a poultry house.

Feces (Excreta, a mixture of feces and urine)

Chicks are exposed to Salmonella at the hatchery, right after they pip from the shell (Bailey et al., 1994). The chicks can get colonized by Salmonella by respiratory (air or dust), oral (feed or water) or intracoacal routes (Cox et al., 1996). Once the chicks are colonized, they excrete high levels of Salmonella during grow-out. The excreta can be ingested by other birds, colonize the GIT and spread among the rest of the flock. Thus, excreta or feces are a good, non-destructive indicator of colonization of the bird and in extension, the flock. However, it is possible that not all the birds in a flock are colonized with Salmonella and hence, sampling of ceca may only be related to Salmonella colonization of the specific bird(s). However, Salmonella positive status of the flock can be observed by sampling of the feces of the birds across the poultry house using drag swabs or boot socks.

Because Salmonella spread in broilers is primarily through fecal-oral route, Salmonella colonizes chicks when they are placed in the grow-out house can result in seeding or spreading Salmonella to other birds. The Salmonella positive status of chick feces is an indication of the colonization of the chicks at the hatchery, and even the noncolonized chicks and subsequently, the birds are exposed to Salmonella in the poultry house environment as discussed in other sources of Salmonella in this manuscript.

Salmonella prevalence between 0 and 56% has been reported in literature in poultry excreta, with a predicted prevalence of 16.3% (95% CI: 10.6–24.3%) in all the regions, US and non-US, with a heterogeneity of 97.7, indicating high degree of variability between the studies (Figure 11).

Figure 11.

Figure 11

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Forest plot for feces as a source of Salmonella colonization of broilers in a poultry house.

Litter

Broiler litter is a mixture of substrate, most often pine shavings, rice husk, cereal straw or other materials along with the feces (excreta) of the birds from previous flocks. In the US, the majority of the flocks are placed into grow-out houses within a day after hatch, directly on the litter (Volkova et al., 2009). If Salmonella is present in the litter, the chicks are exposed at a time when they are highly susceptible to colonization. Studies have shown that the presence of Salmonella in the litter prior to placement of a new flock was shown to be a precursor of high Salmonella frequencies in the new flock at later stages of production (Rose et al., 1999; Rose et al., 2003).

In addition to the type of litter material used, the soil composition and properties were shown to affect moisture retention and indirectly the water activity of the litter and thus, Salmonella survival. Volkova et al. (2009) reported that the probability of detecting Salmonella in the broiler litter were dependent on the soil texture (relative proportions of particles of different sizes) and the infiltration and drainage capabilities, that is, the properties defining the pattern of water movement through the soil profile.

In reused litter, uric acid accumulation occurs and presence of moisture results in conversion of uric acid to urea and ultimately, ammonia. Solubilization of ammonia in litter moisture raises the pH of the litter, and this higher pH was shown to decrease Salmonella populations in the litter. While specific relationships between the water activity of the litter, ammonia concentrations and inactivation rate of Salmonella have not been elucidated, this can be used as a strategy to reduce populations and possibly eliminate Salmonella between flocks. Mendonça et al. (2021) demonstrated destruction of Salmonella (>2.45 log CFU/g) in poultry litter in a poultry farm by injection and trapping ammonia (ca. 1,500 ppm) using tarps within 48 h.

Salmonella prevalence of 1 to 70% was reported in literature in poultry litter, with predicted prevalence of 25.4% (95% CI: 16.6–37.0%) in the US and 25.3% (95% CI: 9.7–51.8%) in non-US poultry houses, with a high heterogeneity of 97.7 indicating high degree of variability between the studies (Figure 12).

Figure 12.

Figure 12

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Forest plot for litter as a source of Salmonella colonization of broilers in a poultry house.

It is crucial to be aware of the method's inherent limitations when evaluating the findings of the meta-analyses. One of these limitations is the potential for publication bias, which is the increased chance of small studies to be published if they have a stronger effect. Several methods exist for determining publication bias, including the funnel plot evaluation, but research has shown that these statistical tests are misleading when the available data does not meet the criteria to conduct such analyses, that is, number of studies (n ≥ 10) and low heterogeneity (I2 < 50%). As such, we did not to include the publication bias in this study.

CONCLUSIONS

Salmonella colonization of broilers is primarily through the fecal-oral route, although other routes of colonization can occur such as respiratory and intracloacal. Several sources of Salmonella for such colonization have been evaluated from literature based on the prevalence of the microorganism in each of the sources. These sources of Salmonella in poultry production include, in the order of prevalence (higher to lower): 1) hatchery (48.5%), 2) litter (25.4%), 3) feces (16.3%), 4) poultry house internal environment (7.9%), 5) poultry house external environment (4.7%), 6) feed (4.8%), 7) chicks (4.7%), and 8) drinker water.

Whereas all of these sources play a significant role in colonization of the bird and subsequent spread, the primary sources of Salmonella include the chicks, feed and internal environment of the poultry house (including rodents and darkling beetles). Of these 3 primary sources of Salmonella, control of feed manufacturing process and/or additives to eliminate Salmonella from feed is a more feasible and effective strategy. Regardless, structural modifications to the poultry house need to be made to prevent infestation of the pests and rodents, and other sources of Salmonella to minimize the risk of Salmonella colonization and further spread within the flock.

Whereas significant progress has been made at the poultry processing stage to reduce concentrations and prevalence of Salmonella in processed poultry (fresh), controls at production need to be incorporated to achieve further reductions in Salmonella in fresh processed poultry. These controls at production include controlling the sources of Salmonella as well as incorporating interventions at preharvest to reduce Salmonella concentrations in and on the birds presented for harvest.

ACKNOWLEDGMENTS

The authors acknowledge the financial support from Anitox Corporation, 1055 Progress Circle Lawrenceville, GA for the conduct of this study.

DISCLOSURES

The authors declare no conflicts of interest.

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