The Intestinal Microbiota and Its Modulation for Salmonella Control in Chickens
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Food Research International 44 (2011) 3149–3159 Contents lists available at SciVerse ScienceDirect Food Research International journal homepage: www.elsevier.com/locate/foodres Review The intestinal microbiota and its modulation for Salmonella control in chickens James R. Chambers, Joshua Gong ⁎ Guelph Food Research Centre, Agriculture and Agri-Food Canada, 93 Stone Road West, Guelph, Ontario, Canada N1G 5C9 article info abstract Article history: Salmonella control has been one of the major tasks in poultry production to ensure poultry food safety. Effective Received 1 December 2010 control is difficult due to the numerous potential sources of Salmonella infection and product contamination in Accepted 29 August 2011 integrated poultry enterprises. In addition, the lack of clinical symptoms of infection in poultry further increases the challenge of achieving proper control. The chicken intestinal microbiota plays an important role in the host Keywords: health and its modulation has achieved considerable success in the past to reduce Salmonella contamination at Salmonella control the farm level. The use of pro/prebiotics has been the major approach in modulating the microbiota. There is in- Microbiota and modulation Pro/prebiotics creased consumer pressure demanding the reduction of antibiotics in feed and elimination of Salmonella from Essential oils poultry and their products. Modulation of the chicken intestinal microbiota continues to offer an attractive op- Phage therapy tion for natural control and sustainable chicken production. In this article, the role of intestinal microbiota in chicken health and the progress in microbiota modulation for Salmonella control have been reviewed. Major technologies for modulating intestinal microbiota, such as the use of probiotics, prebiotics, or phytobiotics (essential oils) and phage therapy that have either receivedmuchattentioninresearchandapplicationor demonstrated promise in the development of novel techniques for Salmonella control, are discussed. The potential and drawbacks of each of these are also critically reviewed. Crown Copyright © 2011 Published by Elsevier Ltd. All rights reserved. Contents 1. Introduction ............................................................. 3150 1.1. Salmonellosis .......................................................... 3150 1.2. Cause of salmonellosis ..................................................... 3150 1.3. Antimicrobial resistant Salmonella ................................................ 3150 2. Intestinal microbiota and its role in chicken health ........................................... 3151 2.1. Microbiota development .................................................... 3151 2.2. Microbiota functions ...................................................... 3151 2.2.1. Gut development ................................................... 3152 2.2.2. Competitive exclusion ................................................. 3152 2.2.3. Immune modulation .................................................. 3152 2.3. Factors affecting the intestinal microbiota ............................................ 3152 2.3.1. Age .......................................................... 3152 2.3.2. Diet .......................................................... 3152 2.3.3. Antibiotics ....................................................... 3153 2.3.4. Major stresses ..................................................... 3153 2.4. Methods for modulating microbiota ............................................... 3153 3. Probiotics ............................................................... 3153 3.1. Probiotic products for Salmonella control ............................................. 3154 3.2. Considerations for development and fabrication of probiotics ................................... 3154 4. Prebiotics ............................................................... 3155 4.1. Types and modes of action ................................................... 3155 4.2. Prebiotics for Salmonella control ................................................. 3155 5. Phytobiotics (essentail oils) ...................................................... 3155 ⁎ Corresponding author. Tel.: +1 519 780 8027; fax: +1 519 829 2400. E-mail addresses: [email protected] (J.R. Chambers), [email protected] (J. Gong). 0963-9969/$ – see front matter Crown Copyright © 2011 Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.foodres.2011.08.017 3150 J.R. Chambers, J. Gong / Food Research International 44 (2011) 3149–3159 6. Bacteriophages ........................................................... 3156 6.1. Phage therapy by lytic phages ................................................. 3156 6.2. Application for pathogen control (including Salmonella)..................................... 3156 6.3. Challenges in application ................................................... 3157 7. Conclusions ............................................................. 3157 Acknowledgments ............................................................ 3157 References ................................................................ 3157 1. Introduction specific lytic bacteriophage to lyse a particular serotype are used to dis- tinguish different strains of the same serotype. Of the 6 subspecies, only Non-typhoidal Salmonella represents a major cause of food poison- S. enterica subsp. enterica serotypes are routinely associated with dis- ing in humans around the world (Chimalizeni, Kawaza, & Molyneux, ease in warm-blooded animals (Uzzau et al., 2000). Serotypes of the 2010). It is caused by some serotypes of the bacterium, often ingested other Salmonella subspecies are usually found in poikilotherms in fecally contaminated food or water (Uzzau et al., 2000). Food of ani- (cold-blooded animals) and the environment and are less frequently mal origin represents one of the sources for this bacterium. The avian associated with human disease (CFSPH, 2005). Of the over 2500 se- species have been frequently implicated as a source of salmonellosis rotypes of Salmonella (WHO, 2005) only some cause salmonellosis (Revolledo, Ferreira, & Mead, 2006). Consequently, Salmonella control (Uzzau et al., 2000). The Centers for Disease Control and Prevention in food-animal production has become a high priority. (CDCP, USA) reported that in 2001, 360 different serotypes of the species, S. enterica, were observed in human cases of salmonellosis. Only three of these, Salmonella ser. Typhimurium, Salmonella ser. 1.1. Salmonellosis Enteritidis and Salmonella ser. Newport, were responsible for 50% of these cases (Porwollik et al., 2004). Of the top 10 serotypes of clin- In this review, salmonellosis refers to non-typhoidal salmonellosis ical Salmonella isolates from humans reported by the CDCP in 2005, which is most frequently associated with ‘food poisoning’. Salmonellosis six were among the top serotypes isolated from swine and poultry, is a gastrointestinal infection that often occurs following ingestion of se- namely Salmonella Typhimurium, Salmonella Enteritidis, Salmonella rotypes of the bacterial subspecies enterica of the species Salmonella ser. Heidelberg, Salmonella ser. Montevideo, Salmonella ser. Saintpaul enterica and is usually self limiting; however, through bacterial invasion and an unnamed serotype, Salmonella ser. I 4,[5],12:i:- (Foley, Lynne, it can progress to bacteremia. Common symptoms of the associated gas- & Nayak, 2008). troenteritis include: abdominal pain; diarrhea; nausea; vomiting; chills; Humans encounter S. enterica subsp. enterica serotypes from vari- and fever; while dehydration, headache and prostration also may occur ous sources. Generally, foodborne salmonellosis in humans originates (El-Gazzar & Marth, 1992). These usually appear about 12 to 36 h after from consumption of contaminated foods of animal origin although consumption of contaminated food. Those for the bacteremia are more other foods have also been implicated (Poppe, 2000; WHO, 2005). severe, possibly leading to death. Mortality from salmonellosis in well- Contamination with Salmonella often implies fecal contamination resourced countries, where invasive infection is rare (b5%), usually (Uzzau et al., 2000), be it direct or indirect. Consumption of contami- runs low (b2%); however, in resource-constrained countries with nated poultry products has frequently been associated with foodborne more frequent invasive disease, there is 18–24% mortality (Chimalizeni, salmonellosis, mainly owing to the ingestion of raw or undercooked Kawasa, & Molyneux, 2010). The annual incidence of non-typhoidal eggs or meat (Carter, Adams, Woodward, & La Ragione, 2009; Revolledo salmonellosis worldwide is 1.3 billion cases and approximately 3 million et al., 2006) although swine and their products have been implicated as of these die (Chimalizeni et al., 2010). well (Foley et al., 2008). Effective control is difficult due to the numer- Economic losses associated with foodborne salmonellosis are ous potential sources of Salmonella infection and product contamina- significant. Only a few countries have provided detailed estimates tion in integrated poultry enterprises (Poppe, 2000; Revolledo et al., of associated losses. In the United States of America (USA), it is es- 2006). timated that there are 1.4 million non-typhoidal salmonellosis cases annually with 168,000 visits to physicians, 15,000 hospitalizations, and 580 deaths (WHO, 2005) with a total cost of US$ 3 billion. In 1.3. Antimicrobial resistant Salmonella Denmark, the