Skip to main content
Log in

Investigations into Salmonella contamination in feed production chain in Karst rural areas of China

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

In order to understand the status of Salmonella contamination of feed production chain in Karst rural areas, southwest of China, a total of 1077 feed samples including animal feed materials and feed products were randomly collected from different sectors of feed chain covering feed mills, farms, and feed sales in nine regions of Karst rural areas between 2009 and 2012, to conduct Salmonella test. The different positive rates with Salmonella contamination were detected, the highest was 4.7 % in 2009, the lowest was 0.66 % in 2011, while 4.3 % in 2010, 2.8 % in 2012, respectively. Twelve types of feed including concentrate, complete, self-made, and feed ingredients were inspected. Salmonella contamination mainly concentrated on animal protein material such as meat meal, meat and bone meal, feather meal, blood meal, and fish meal. No Salmonella contamination was detected in feed yeast, microbial protein, rapeseed, and soybean meal. Salmonella contamination existed in each sector of feed production chain. This investigation provided a basic reference for feed production management and quality control in feed production chain in Karst rural areas of China.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

References

  • Andrés-Barranco S, Vico JP, Marín CM, Herrera-León S, Mainar-Jaime RC (2016) Characterization of Salmonella enterica serovar Typhimurium isolates from pigs and pig environment–related sources and evidence of new circulating monophasic strains in Spain. J Food Prot 3:352–512

    Google Scholar 

  • Anon (2003) Evaluation of the measures to control Salmonella in the feed sector 2003. Quality series No. 98. Product Board Animal Feed 2004. http://www.pdv.nl

  • Ashbolt R, Kirk MD (2006) Salmonella Mississippi infections in Tasmania: the role of native Australian animals and untreated drinking water. Epidemiol Infect 134(6):1257–1265

    Article  CAS  Google Scholar 

  • Aude NN, Khanh DV, Nicolas D, Monique L (2013) Effect of combination of essential oils and bacteriocins on the efficacy of gamma radiation against Salmonella Typhimurium and Listeria monocytogenes. Int J Radiat Biol 89(10):794–800

    Article  Google Scholar 

  • Brendan AN (2012) Cold plasma reduction of Salmonella and Escherichia coli O157:H7 on almonds using ambient pressure gases. J Food Sci 77(3):171–175

    Article  Google Scholar 

  • CFIA (China Feed Industry Association) (2013) Feed production situations of China in 2013

  • Chunhong Z, Haorong B, Shuhua W (2004) Evaluation of CHROMagar vibrio colored medium in detection of Salmonella to animal feed. Veterinry Pharmaceuticals & Feed Additives (Chinese) 9(5):25–27

    Google Scholar 

  • Clavero MR, Monk JD, Beuchat LR, Doyle MP, Brackett RE (1994) Inactivation of Escherichia coli O157:H7, salmonellae, and campylobacter jejuni in raw ground beef by gamma irradiation. Appl Environ Microbiol 60:2069–2075

    CAS  Google Scholar 

  • Compton JA, Baney JA, Donaldson SC, Houser BA, San Julian GJ, Yahner RH (2008) Salmonella infections in the common raccoon (Procyon lotor) in western Pennsylvania. J Clin Microbiol 46(9):3084–3086

    Article  Google Scholar 

  • Crump JA, Griffin PA, Angulo FJ (2002) Bacterial contamination of animal feed and its relationship to human foodborne illness. Clin Infect Dis 35:859–865

    Article  Google Scholar 

  • D’Aoust JY (1997) Salmonella species. In: Doyle MP (ed) Food microbiology: fundamentals and frontiers. ASM Press, Washington, DC, pp. 129–157

    Google Scholar 

  • Davies RH, Wales AD (2010) Investigations into Salmonella contamination in poultry feed mills in the United Kingdom. J Appl Microbiol 109:1430–1440

    Article  CAS  Google Scholar 

  • Davies R, Breslin M, Corry JE, Hudson W, Allen VM (2001) Observations on the distribution and control of Salmonella species in two integrated broiler companies. Vet Rec 149:227–232

    Article  CAS  Google Scholar 

  • Duffy L, Barlow R, Fegan N, Vanderlinde P (2009) Prevalence and serotypes of Salmonella associated with prevalence and serotypes of Salmonella associated with goats at two Australian abattoirs. Lett Appl Microbiol 48:193–197

    Article  CAS  Google Scholar 

  • EFSA (2008) Microbiological risk assessment in feedingstuffs for food producing animals–scientific opinion of the panel on biological hazards. EFSA J 720:84. doi:10.2903/j.efsa.2008.720

    Google Scholar 

  • EFSA (2009) The community summary report on trends and sources of zoonoses and zoonotic agents in the European Union in 2007. The EFSA Journal 223:1–232

    Google Scholar 

  • EFSA (2014) European Centre for Disease Prevention and Control: the European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2012. The EFSA Journal 3547:75–78

    Google Scholar 

  • Fay JP, Farias RN (1975) The inhibitory action of fatty acids on the growth of Escherichia coli. J Gen Microbiol 91:233–240

    Article  CAS  Google Scholar 

  • Furuta K, Morimoto S, Sato S (1980) Bacterial contamination in feed ingredients, formulated chicken feed and reduction of viable bacteria by pelleting. Lab Anim 14:221–224

    Article  CAS  Google Scholar 

  • Glickman LT, McDonough PL, Shin SJ, Fairbrother JM, LaDue RL, King SE (1981) Bovine Salmonellosis attributed to Salmonella anatum-contaminated haylage and dietary stress. J Am Vet Med Assoc 178:1268–1272

    CAS  Google Scholar 

  • Grimont PAD and Weill FX (2007) Antigenic formulae fort the Salmonella serovars, 9th edn. Paris, France: WHO Collaborating Centre for Reference and Research on Salmonella.

  • Hacking WC, Mitchell WRD, Carlson HC (1978) Salmonella investigation in an Ontario feed mill. Canadian Journal of Comparative Medicine 42:400–406

    CAS  Google Scholar 

  • Halls NA, Tallentire A (1978) Effects of processing and gamma irradiation on the microbiological contaminants of a laboratory animal diet. Lab Anim 12:5–10

    Article  CAS  Google Scholar 

  • Handeland K, Nesse LL, Lillehaug A, Vikoren T, Djonne B, Bergsjo B (2008) Natural and experimental Salmonella Typhimurium infections in foxes (Vulpes vulpes). Vet Microbiol 132(1–2):129–134

    Article  CAS  Google Scholar 

  • Harris IT, Fedorka-cray PJ, Gray JT, Thomas LA Ferris K (1997) Prevalence of Salmonella organisms in swine feed. Journal of Applied Veterinary Medicine Association 210:382–385

    CAS  Google Scholar 

  • Havelaar AH, Haagsma JA, Mangen MJJ, Kemmeren JM, Verhoef LPB (2009) Disease burden of foodborne pathogens in the Netherlands. Int J Food Microbiol 156:231–238

    Article  Google Scholar 

  • Hernandez SM, Keel K, Sanchez S, Trees E, Gerner-Smidt P, Adams JK (2012) Epidemiology of a Salmonella enterica subsp. enterica serovar Typhimurium strain associated with a songbird outbreak. Appl Environ Microbiol 78(20):7290–7298

    Article  CAS  Google Scholar 

  • Himathonkham S, Gracas DA, Pereira M, Riemann H (1996) Heat destruction of Salmonella in poultry feed: effect of time, temperature, and moisture. Avian Dis 40:72–77

    Article  Google Scholar 

  • Hoszowski A, Osek J, Kwiatek K, Wasyl D, Wieczorek K, Kukier E, Skarzynska M, Szwarc M, Wnuk D, Lalak A, Goldsztejn M (2008) Monitoring of foodstuff of animal origin and animal feedingstuff for Salmonella presence. Monograpgy issued by NVRI, Pulawy

    Google Scholar 

  • Jaquette CB, Beuchat LR, Mahon BE (1996) Efficacy of chlorine and heat treatment in killing Salmonella stanley inoculated onto alfalfa seeds and growth and survival of the pathogen during sprouting and storage. Appl Environ Microbiol 62:2212–2215

    CAS  Google Scholar 

  • Jijun H, Biao W (2009) Isolation and identification of Salmonella from animal feed. Journal of Agricultural Science and Technology (Chinese) 11(S1):56–58

    Google Scholar 

  • Jinghui Z, Yeru W, Xiaoyu S, Shenghui C, Haibin X, Baowei Y, Jinlin H, Guihua L, Qian C, Gang Z, Qiuxia C, Fengqin L (2014) Prevalence and quantification of Salmonella contamination in raw chicken carcasses at the retail in China. Food Control 44:198–202

    Article  Google Scholar 

  • Joost S, Rob de J, Arie HH, Annemarie P (2013) Variability and uncertainty analysis of the cross-contamination ratios of salmonella during pork cutting. Risk Anal 33:1100–1115

    Article  Google Scholar 

  • Khan M, Atamy M (1969) Antagonistic effect of fatty acids against Salmonella in meat and bone meal. Appl Microbiol 17:402–404

    CAS  Google Scholar 

  • Kwiatek K, Kukier E, Wasyl D, Hoszowski A (2008) Microbial quality of feed in Poland. Medycyna Weterynaryjna 64:183–188 In Polish with an English summary

    Google Scholar 

  • Leeson S, Marcotte M (1993) Irradiation of poultry feed. I. Microbial status and bird response. World’s Poultry Science Journal 49:19–33

    Article  Google Scholar 

  • Mao X, Hu J, Liu X (2011) Estimation on disease burden of foodborne nontyphoid salmonellosis in China using literature review method. Chinese Journal of Disease Control & Prevention 15(7):622–625

    Google Scholar 

  • Martin W, Per H (2010) An assessment of soybeans and other vegetable proteins as source of Salmonella contamination in pig production. Acta Vet Scand 52:15

    Article  Google Scholar 

  • Mattlho G, Himathongkham S, Riemann H, Kass P (1997) Destruction of Salmonella enteritidis in poultry feed by combination of heat and propionic acid. Avian Dis 41:58–61

    Article  Google Scholar 

  • Mccapes RH, Ekperigin HE, Cameron WJ, Ritchie WL, Slagter J, Stanheland V, Nagaraja KV (1989) Effect of a new pelleting process on the level of contamination of poultry mash by Escherichia coli and Salmonella. Avian Dis 33:103–111

    Article  CAS  Google Scholar 

  • Min L, Sasidhar M, H Scott H, Timothy JG, Dayna MB-H, Guy HL (2014) Salmonella spp. in lymph nodes of fed and cull cattle: relative assessment of risk to ground beef. Food Control 50:423–434

    Google Scholar 

  • Nabbut NH (1978) Salmonella serotypes encountered in animal feed additives in Lebanon. Am J Vet Res 39:893–895

    CAS  Google Scholar 

  • Nayak R, Kenney PB, Keswani J, Ritz C (2003) Isolation and characterisation of Salmonella in a turkey production facility. Br Poult Sci 44:192–202

    Article  CAS  Google Scholar 

  • Newell K, McClarin R, Murdock CR, MacDonald WN, Hutchinson HL (1959) Salmonellosis in Northern Ireland, with special reference to pigs and Salmonella contaminated pig meal. J Hyg (Lond) 57:92–105

    Article  CAS  Google Scholar 

  • Niemira BA, Gutsol A (2010) Nonthermal plasma as a novel food processing technology. In: Zhang HQ, Barbosa-Cánovas G, Balasubramaniam VM, Dunne P, Farkas D, Yuan J (eds) Nonthermal processing technologies for food. Blackwell Publishing, Ames, IA, pp. 271–288

    Google Scholar 

  • Pao S, Hagens BE, Kim C, Wildeus S, Ettinger MR, Wilsond MD, Watts BD, Whitley NC, Porto-Fettf ACS, Schwarz JG, Kaseloo P, Ren S, Long W III, Li H, Luchansky JB (2014) Prevalence and molecular analyses of Campylobacter jejuni and Salmonella spp. in co-grazing small ruminants and wild-living birds. Livest Sci 160:163–171

    Article  Google Scholar 

  • Qiong C, Fande K, Haibing P, Yuhua L, Yongfeng C, Shufei X (2006) Investigation into animal feed contaminated with Salmonella in Xiameng district, China. Fujian Animal and Veterinary Science (Chinese) 28(2):7–9

    Google Scholar 

  • SAPRC (2001) Hygienical Standard for Feeds (GB13078–2001), Standardization Administration of The People’s Republic of China(SAPRC)

  • Smith KE, Anderson F, Medus C, Leano F, Adams J (2005) Outbreaks of salmonellosis at elementary schools associated with dissection of owl pellets. Vector Borne Zoonotic Dis 5(2):133–136

    Article  Google Scholar 

  • van den Brandhof WE, De Wit GA, de Wit MAS, van Duynhoven YTHP (2004) Costs of gastroenteritis in the Netherlands. Epidemiol Infect 132:211–221

    Article  Google Scholar 

  • Voetsch AC, Van Gilder TJ, Angulo FJ, Farley MM, Shallow S, Marcus R, Cieslak PR, Deneen VC, Auxe RV (2004) FoodNet estimate of the burden of illness caused by nontyphoidal Salmonella infections in the United States. Clin Infect Dis 38(Suppl. 3):S127–S134

    Article  Google Scholar 

  • Wierup M, Häggblom P (2010) An assessment of soybeans and other vegetable proteins as source of Salmonella contamination in pig production. Acta Vet Scand 52:15

    Article  Google Scholar 

  • Wierup M, Kristoffersen T (2014) Prevention of Salmonella contamination of finished soybean meal used for animal feed by a Norwegian production plant despite frequent Salmonella contamination of raw soy beans, 1994–2012. Acta Vet Scand 56:41

    Article  Google Scholar 

  • Yuanran D, Peng D, Jinlei L, Yanling G, Funa Q (2013) Jine. Determination of Salmonella in animal feed and feed additives. Shanghai Animal and Veterinary Science Conmunication (Chinese) 2:10–11

    Google Scholar 

  • Zecha BC, McCapes RH, Dungan WM, Holte RJ, Worcester WW, Williams JE (1977) The Dillon Beach project—a five-year epidemiological study of naturally occurring Salmonella infection in turkeys and their environment. Avian Dis 21:141–159

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We would like to thank The Feed Industrial Management Department of nine regions of Guizhou province of China for the help in sample collection for this research. This work were supported by the Agricultural Major Special Project of Guzhou province (No.[2011]6021), (No.[2012]6004].

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Shenglin Yang.

Additional information

Responsible editor: Philippe Garrigues

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yang, S., Wu, Z., Lin, W. et al. Investigations into Salmonella contamination in feed production chain in Karst rural areas of China. Environ Sci Pollut Res 24, 1372–1379 (2017). https://doi.org/10.1007/s11356-016-7868-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-016-7868-6

Keywords

Navigation