Skip to main content

Advertisement

SpringerLink
Log in

Loop-Mediated Isothermal Amplification (LAMP) for the Detection of Salmonella in Food

  • Published:
Food Analytical Methods Aims and scope Submit manuscript

Abstract

Salmonella infection represents a considerable global burden, with significant health and economic impacts. Salmonellosis is most often attributed to the consumption of contaminated foods such as poultry, beef, pork, eggs, milk, seafood, nut products, and fresh produce. Increased public awareness related to food-borne contamination resulted in greater efforts to develop more sensitive, rapid, and inexpensive methods of pathogens detection. Loop-mediated isothermal amplification (LAMP) constitutes a promising solution for rapid diagnosis of food-borne pathogens and is increasingly been applied for the specific diagnosis of different pathogens, Salmonella included. We have reviewed the application of LAMP for the specific detection of Salmonella in food matrices, compared with conventional culture techniques, and in terms of applicability, food matrices, type of assays, target genes, assay temperature, time and equipment, specificity, sensitivity, and robustness. The pros and cons of Salmonella LAMP assays are presented. The potential of LAMP for the development of new on-site diagnostics for the food and agricultural industries and its use as a routine Salmonella screening tool are discussed. Salmonella-specific LAMP assays are expected to provide a very robust, innovative, and powerful molecular diagnostic method for food safety testing services and public health authorities.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  • Ahn Y-C, Cho M-H, Yoon I-K, Jung D-H, Lee E-Y, Kim J-H, Jang W-C (2010) Detection of Salmonella using the loop mediated isothermal amplification and real-time PCR. J Korean Chem Soc 54(2):215–221

    Article  CAS  Google Scholar 

  • Aricind A, Bhagwat AA (2003) Simultaneous detection of Escherichia coli O157:H7, Listeria monocytogenes and Salmonella strains by real-time PCR. Int J Food Microbiol 84(2):217–224

    Article  Google Scholar 

  • Chen H, Zhang J, Sun D, Ma L, Liu X, Cai X, Liu Y (2008) Development of reverse transcription loop-mediated isothermal amplification for rapid detection of H9 avian influenza virus. J Virol Methods 151(2):200–203

    Article  CAS  Google Scholar 

  • Chen S, Wang F, Beaulieu JC, Stein RE, Ge B (2011) Rapid detection of viable salmonellae in produce by coupling propidium monoazide with loop-mediated isothermal amplification. Appl Environ Microbiol 77(12):4008–4016

    Article  CAS  Google Scholar 

  • Cocolin L, Rajkovic A, Rantsiou K, Uyttendaele M (2011) The challenge of merging food safety diagnostic needs with quantitative PCR platforms. Trends Food Sci Technol 22(S1):S30–S38

    Article  CAS  Google Scholar 

  • Elizaquivel P, Aznar R (2008) A multiplex RTi-PCR reaction for simultaneous detection of Escherichia coli O157:H7, Salmonella spp. and Staphylococcus aureus on fresh, minimally processed vegetables. Food Microbiol 25(5):705–713

    Article  CAS  Google Scholar 

  • Enosawa M, Kageyama S, Sawai K, Wanatabe K, Notomi T, Onoe S, Mori Y, Yokomizo Y (2003) Use of loop-mediated isothermal amplification of the IS900 sequence for rapid detection of cultured Mycobacterium avium subsp. paratuberculosis. J Clin Microbiol 41(9):4359–4365

    Article  CAS  Google Scholar 

  • Foley SL, Lynne AM (2008) Food animal-associated Salmonella challenges: pathogenicity and antimicrobial resistance. J Anim Sci 86(14):E173–E187

    Article  CAS  Google Scholar 

  • Francois P, Tangomo M, Hibbs J, Bonetti EJ, Boehme CC, Notomi T, Perkins MD, Schrenzel J (2011) Robustness of a loop-mediated isothermal amplification reaction for diagnostic applications. FEMS Immunol Med Microbiol 62(1):41–48

    Article  CAS  Google Scholar 

  • Fukuda S, Takao S, Kuwayama M, Shimazu Y, Miyazaki K (2006) Rapid detection of norovirus from fecal specimens by real-time reverse transcription-loop-mediated isothermal amplification assay. J Clin Mircobiol 44(4):1376–1381

    Article  CAS  Google Scholar 

  • Furuhata K, Annaka T, Ikedo M, Fukuyama M, Yoshida S (2005) Comparison of loop-mediated isothermal amplification (LAMP) and conventional culture for the detection of Legionella species in hot spring water samples in Japan. Biocontrol Sci 10(3):117–120

    Article  Google Scholar 

  • Gandelman OA, Church VL, Moore CA, Kiddle G, Carne CA, Parmar S, Jalal H, Tisi LC, Murray JAH (2010) Novel bioluminescent quantitative detection of nucleic acid amplification in real-time. PLoS ONE 5(11):e14155

    Article  CAS  Google Scholar 

  • Goto M, Hayashidani H, Takatori K, Hara-Kudo Y (2007) Rapid detection of enterotoxigenic Staphylococcus aureus harbouring genes for four classical enterotoxins, SEA, SEB, SEC and SED, by loop-mediated isothermal amplification assay. Lett Appl Microbiol 45(1):100–107

    Article  CAS  Google Scholar 

  • Hara-Kudo Y, Yoshino M, Kojima T, Ikedo M (2005) Loop-mediated isothermal amplification for the rapid detection of Salmonella. FEMS Microbiol Lett 253(1):155–161

    Article  CAS  Google Scholar 

  • He C, Liu Z, Wang D, Sun Q, Huang J (2010) Application of LAMP to detect Salmonella in animal derived foods. Chin J Food Hyg 5:411–414 (in Chinese with English abstract)

    Google Scholar 

  • Hendriksen RS, Vieira AR, Karlsmose S, Lo Fo Wong DM, Jensen AB, Wegener HC, Aarestrup FM (2011) Global monitoring of Salmonella serovar distribution from the world health organization global foodborne infections network country data bank: results of quality assured laboratories from 2001 to 2007. Foodborne Pathog Dis 8(8):887–900

    Article  Google Scholar 

  • Hsieh K, Patterson AS, Ferguson BS, Plaxco KW, Soh HT (2012) Rapid, sensitive, and quantitative detection of pathogenic DNA at the point of care through microfluidic electrochemical quantitative loop-mediated isothermal amplification. Angew Chem Int Ed 51(20):4896–4900

    Article  CAS  Google Scholar 

  • Jenkins DM, Kubota R, Dong J, Li Y, Higashiguchi D (2011) Handheld device for real-time, quantitative, LAMP-based detection of Salmonella enterica using assimilating probes. Biosens Bioelectron 30(1):255–260

    Article  CAS  Google Scholar 

  • Jiang K, Lv Q, Zhang D, Gao X, Zhao Y, Li M, Liu L, Wu J, Lu X, Luo C (2012) A novel, sensitive, accurate multiplex loop-mediated isothermal amplification method for detection of Salmonella spp., Shigella spp. and Staphylococcus aureus in food. J Food Agric Environ 10(3&4):252–256

    CAS  Google Scholar 

  • Karanis P, Thekisoe O, Kiouptsi K, Ongerth J, Igarashi I, Inoue N (2007) Development and preliminary evaluation of a loop-mediated isothermal amplification procedure for sensitive detection of cryptosporidium oocysts in fecal and water samples. Appl Environ Microbiol 73(17):5660–5662

    Article  CAS  Google Scholar 

  • Klerks MM, Zijlstra C, van Bruggen AH (2004) Comparison of real-time PCR methods for detection of Salmonella enterica and Escherichia coli O157:H7, and introduction of a general internal amplification control. J Microbiol Methods 59(3):337–349

    Article  CAS  Google Scholar 

  • Kothary MH, Babu US (2001) Infective dose of foodborne pathogens in volunteers: a review. J Food Saf 21(1):49–73

    Article  Google Scholar 

  • Kubota R, Labarre P, Weigl BH, Li Y, Haydock P, Jenkins DM (2013) Molecular diagnostics in a teacup: non-instrumented nucleic acid amplification (NINA) for rapid, low cost detection of Salmonella enterica. Chin Sci Bull 58(10):1162–1168

    Article  CAS  Google Scholar 

  • Kurosaki Y, Sakuma T, Fukuma A, Fujinami Y, Kawamoto K, Kamo N, Makino S-I, Yasuda J (2009) A simple and sensitive method for detection of Bacillus anthracis by loop-mediated isothermal amplification. J Appl Microbiol 107(6):1947–1956

    Article  CAS  Google Scholar 

  • Lee S-Y, Huang J-G, Chuang T-L, Sheu J-C, Chuang Y-K, Holl M, Meldrum DR, Lee C-N, Lin C-W (2008) Compact optical diagnostic device for isothermal nucleic acids amplification. Sensors Actuators B Chem 133(2):493–501

    Article  CAS  Google Scholar 

  • Lee K, Iwata T, Shimizu M, Taniguchi T, Nakadai A, Hirota Y, Hayashidani H (2009) A novel multiplex PCR assay for Salmonella subspecies identification. J Appl Microbiol 107(3):805–811

    Article  CAS  Google Scholar 

  • Li XF, Zhang S, Zhang HW, Zhang LH, Tao HT, Yu J, Zheng WJ, Liu CH, Lü D, Xiang R, Liu Y (2009) A loop-mediated isothermal amplification method targets the phoP gene for the detection of Salmonella in food samples. Int J Food Microbiol 13(3):252–258

    Article  Google Scholar 

  • Liu B, Zhang L, Zhu X, Shi C, Chen J, Liu W, He X, Shi X (2011) PCR identification of Salmonella serogroups based on specific targets obtained by comparative genomics. Int J Food Microbiol 144(3):511–508

    Article  CAS  Google Scholar 

  • Lu Y, Yang W, Shi L, Li L, Alam MJ, Guo S, Miyoshi S (2009) Specific detection of viable Salmonella cells by an ethidium monoazide-loop mediated isothermal amplification (EMA-LAMP) method. J Health Sci 55(5):820–824

    Article  CAS  Google Scholar 

  • Majowicz SE, Musto J, Scallan E, Angulo FJ, Kirk M, O'Brien SJ, Jones TF, Fazil A, Hoekstra RM (2010) The global burden of nontyphoidal Salmonella gastroenteritis. Clin Infect Dis 50(6):882–889

    Article  Google Scholar 

  • Malorny B, Paccassoni E, Fach P, Bunge C, Martin A, Helmuth R (2004) Diagnostic real-time PCR for detection of Salmonella in food. Appl Environ Microbiol 70(12):7046–7052

    Article  CAS  Google Scholar 

  • Malorny B, Bunge C, Helmuth R (2007) A real-time PCR for the detection of Salmonella enteritidis in poultry meat and consumption eggs. J Microbiol Methods 70(2):245–251

    Article  CAS  Google Scholar 

  • Malorny B, Lofstrom C, Wagner M, Kramer N, Hoorfar J (2008) Enumeration of Salmonella bacteria in food and feed samples by real-time PCR for quantitative microbial risk assessment. Appl Environ Microbiol 74(5):1299–1304

    Article  CAS  Google Scholar 

  • Mori Y, Nagamine K, Tomita N, Notomi T (2001) Detection of loop-mediated isothermal amplification reaction by turbidity derived from magnesium pyrophosphate formation. Biochem Biophys Res Commun 289(1):150–154

    Article  CAS  Google Scholar 

  • Nagamine K, Hase T, Notomi T (2002) Accelerated reaction by loop-mediated isothermal amplification using loop primers. Mol Cell Probes 16(3):223–229

    Article  CAS  Google Scholar 

  • Naravaneni R, Jamil K (2005) Rapid detection of food-borne pathogens by using molecular techniques. J Med Microbiol 54(1):51–54

    Article  CAS  Google Scholar 

  • Niessen L, Luo J, Denschlag C, Vogel RF (2013) The application of loop-mediated isothermal applification (LAMP) in food testing for bacterial pathogens and fungal contaminants. Food Microbiol 36(2):191–206

    Article  CAS  Google Scholar 

  • Notomi T, Okayama H, Masubuchi H, Yonekawa T, Watanabe K, Amino N, Hase T (2000) Loop-mediated isothermal amplification of DNA. Nucleic Acids Res 28(12):e63

    Article  CAS  Google Scholar 

  • Ohtsuka K, Yanagawa K, Takatori K, Hara-Kudo Y (2005) Detection of Salmonella enterica in naturally contaminated liquid eggs by loop-mediated isothermal amplification, and characterization of Salmonella isolates. Appl Environ Microbiol 71(11):6730–6735

    Article  CAS  Google Scholar 

  • Ohtsuki R, Kawamoto K, Kato Y, Shah MM, Ezaki T, Makino S-I (2008) Rapid detection of Brucella spp. by the loop-mediated isothermal amplification method. J Appl Microbiol 104(6):1815–1823

    Article  CAS  Google Scholar 

  • Okamura M, Ohba Y, Kikuchi S, Suzuki A, Tachizaki H, Takehara K, Ikedo M, Kojima T, Nakamura M (2008) Loop-mediated isothermal amplification for the rapid, sensitive, and specific detection of the O9 group of Salmonella in chickens. Vet Microbiol 132(1–2):197–204

    Article  CAS  Google Scholar 

  • Okamura M, Ohba Y, Kikuchi S, Takehara K, Ikedo M, Kojima T, Nakamura M (2009) Rapid, sensitive, and specific detection of the O4 group of Salmonella enterica by loop-mediated isothermal amplification. Avian Dis 53(2):216–221

    Article  Google Scholar 

  • Oliveira SD, Santos LR, Schuch DMT, Silva AB, Salle CTP, Canal CW (2002) Detection and identification of salmonellas from poultry-related samples by PCR. Vet Microbiol 87(1):25–35

    Article  CAS  Google Scholar 

  • Parida M, Posadas G, Inoue S, Hasebe F, Morita K (2004) Real time reverse transcription loop-mediated isothermal amplification for rapid detection of West Nile virus. J Clin Microbiol 42(1):257–263

    Article  CAS  Google Scholar 

  • Parida M, Horioke K, Ishida H, Dash PK, Saxena P, Jana AM, Islam MA, Inoue S, Hosaka N, Morita K (2005) Rapid detection and differentiation of dengue virus serotypes by a real-time reverse transcription-loop-mediated isothermal amplification assay. J Clin Microbiol 43(6):2895–2903

    Article  CAS  Google Scholar 

  • Parida M, Sannarangaiah S, Dash PK, Rao PV, Morita K (2008) Loop mediated isothermal amplification (LAMP): a new generation of innovative gene amplification technique; perspectives in clinical diagnosis of infectious diseases. Rev Med Virol 18(6):407–421

    Article  CAS  Google Scholar 

  • Ravan H, Yazdanparast R (2012a) Development and evaluation of a loop-mediated isothermal amplification method in conjunction with an enzyme-linked immunosorbent assay for specific detection of Salmonella serogroup D. Anal Chim Acta 733:64–70

    Article  CAS  Google Scholar 

  • Ravan H, Yazdanparast R (2012b) Development of a new loop-mediated isothermal amplification assay for prt (rfbS) gene to improve the identification of Salmonella serogroup D. World J Microbiol Biotechnol 28(5):2101–2106

    Article  CAS  Google Scholar 

  • Seo KH, Valentin-Bon IE, Brackett RE (2006) Detection and enumeration of Salmonella enteritidis in homemade ice cream associated with outbreak: comparison of conventional and real-time PCR methods. J Food Prot 69(3):639–643

    CAS  Google Scholar 

  • Shao Y, Zhu S, Jin C, Chen F (2011) Development of multiplex loop-mediated isothermal amplification-RFLP (mLAMP-RFLP) to detect Salmonella spp. and Shigella spp. in milk. Int J Food Microbiol 148(2):75–79

    Article  CAS  Google Scholar 

  • Song T, Toma C, Nakasone N, Iwanaga M (2005) Sensitive and rapid detection of Shigella and enteroinvasive Escherichia coli by a loop-mediated isothermal amplification method. FEMS Microbiol Lett 243(1):259–263

    Article  CAS  Google Scholar 

  • Tang T, Cheng A, Wang M, Li X, He Q, Jia R, Zhu D, Chen X (2012) Development and clinical verification of a loop-mediated isothermal amplification method for detection of Salmonella species in suspect infected ducks. Poult Sci 91(4):979–986

    Article  CAS  Google Scholar 

  • Tebbs RS, Wong LY, Brzoska P and Petrauskene OV (2012) Molecular technologies for Salmonella detection. In: Annous BA and Gurtler JB (eds). Salmonella—distribution, adaptation, control measures and molecular technologies. ISBN 978-953-51-0661-6. InTech. DOI: 10.5772/2470

  • Techathuvanan C, D'Souza DH (2012) Reverse-transcriptase loop-mediated isothermal amplification as a rapid screening/monitoring tool for Salmonella enterica detection in liquid whole eggs. J Food Sci 77(4):M200–M205

    Article  CAS  Google Scholar 

  • Techathuvanan C, Draughon FA, D'Souza DH (2010a) Loop-mediated isothermal amplification (LAMP) for the rapid and sensitive detection of Salmonella typhimurium from pork. J Food Sci 75(3):M165–M172

    Article  CAS  Google Scholar 

  • Techathuvanan C, Draughon FA, D'Souza DH (2010b) Real-time reverse transcriptase PCR for the rapid and sensitive detection of Salmonella typhimurium from pork. J Food Prot 73(3):507–514

    CAS  Google Scholar 

  • Techathuvanan C, Draughon FA, D'Souza DH (2011) Comparison of reverse transcriptase PCR, reverse transcriptase loop-mediated isothermal amplification, and culture-based assays for Salmonella detection from pork processing environments. J Food Prot 74(2):294–301

    Article  CAS  Google Scholar 

  • Tirado C, Schmidt K (2001) WHO surveillance programme for control of foodborne infections and intoxications: results and trends across greater Europe. J Infect 43(1):80–84

    CAS  Google Scholar 

  • Tourlousse DM, Ahmad F, Stedtfeld RD, Seyrig G, Tiedje JM, Hashsham SA (2012) A polymer microfluidic chip for quantitative detection of multiple water- and foodborne pathogens using real-time fluorogenic loop-mediated isothermal amplification. Biomed Microdevices 14(4):769–778

    Article  CAS  Google Scholar 

  • Ueda S, Kuwabara Y (2009) The rapid detection of Salmonella from food samples by loop-mediated isothermal amplification (LAMP). Biocontrol Sci 14(2):73–76

    Article  CAS  Google Scholar 

  • Wang Y-Z, Wang D-G (2013) Development and evaluation of a loop-mediated isothermal amplification (LAMP) method for detecting foodborne Salmonella in raw milk. Adv Mater Res 647:577–582

    Article  CAS  Google Scholar 

  • Wang D, Huo G, Wang F, Li Y, Ren D (2008a) Drawback of loop-mediated isothermal amplification. Afr J Food Sci 2:83–86

    Google Scholar 

  • Wang L, Shi L, Alam MJ, Geng Y, Li L (2008b) Specific and rapid detection of foodborne Salmonella by loop-mediated isothermal amplification method. Food Res Int 41(1):69–74

    Article  Google Scholar 

  • Wang Y, Zhang W, Yuan Y, Ma X, Zhang H, Su X, Wang Z, Ma B (2009) Study on loop-mediated isothermal amplification assay for detection of Salmonella in meat products. 3rd International Conference on Bioinformatics and Biomedical Engineering (ICBBE 2009): 1–6

  • Wattiau P, Weijers T, Andreoli P, Schliker C, Veken HV, Maas HM, Verbruggen AJ, Heck ME, Wannet WJ, Imberechts H, Vos P (2008) Evaluation of the Premi Test Salmonella, a commercial low-density DNA microarray system intended for routine identification and typing of Salmonella enterica. Int J Food Microbiol 123(3):293–298

    Article  CAS  Google Scholar 

  • Whyte P, Mc Gill K, Collins JD, Gormley E (2002) The prevalence and PCR detection of Salmonella contamination in raw poultry. Vet Microbiol 89(1):53–60

    Article  CAS  Google Scholar 

  • Yang JL, Ma GP, Yang R, Yang SQ, Fu LZ, Cheng AC, Wang MS, Zhang SH, Shen KF, Jia RY, Deng SX, Xu ZY (2010) Simple and rapid detection of Salmonella serovar Enteritidis under field conditions by loop-mediated isothermal amplification. J Appl Microbiol 109(5):1715–1723

    CAS  Google Scholar 

  • Ye Y, Wang B, Huang F, Song Y, Yan H, Alam MJ, Yamasaki S, Shi L (2011) Application of in situ loop-mediated isothermal amplification method for detection of Salmonella in foods. Food Control 22(2–3):438–444

    Article  CAS  Google Scholar 

  • Yoneyama T, Kiyohara T, Shimasaki N, Kobayashi G, Ota Y, Notomi T, Totsuka A, Wakita T (2007) Rapid and real-time detection of hepatitis A virus by reverse transcription loop-mediated isothermal amplification assay. J Virol Methods 145(2):162–168

    Article  CAS  Google Scholar 

  • Ye Y, Yamasaki S, Lei S (2009) In situ loop-mediated isothermal amplification technology for rapid detection of food-borne Salmonella. Food Ferment Ind 35:137–141

    CAS  Google Scholar 

  • Zhang G, Brown EW, González-Escalona N (2011) Comparison of real-time PCR, reverse transcriptase real-time PCR, loop-mediated isothermal amplification, and the FDA conventional microbiological method for the detection of Salmonella spp. in produce. Appl Environ Microbiol 77(18):6495–6501

    Article  CAS  Google Scholar 

  • Zhang L, Pan ZM, Geng SZ, Chen X, Liu ZY, Zhao F, Jiao XA (2012) A loop-mediated isothermal amplification method targets the HisJ gene for the detection of foodborne Salmonella. Eur Food Res Technol 234(6):1055–1062

    Article  CAS  Google Scholar 

  • Zhu SM, Wu JJ, Xu C, Qu J, Cheng W, Chen FS (2008) Rapid detection of Salmonella spp. by loop-mediated isothermal amplification method. Mod Food Sci Technol 24(7):725–730

    CAS  Google Scholar 

  • Ziros PG, Kokkinos PA, Papanotas K, Vantarakis A (2012) Loop-mediated isothermal amplification (LAMP) for the detection of Salmonella spp. isolated from different food types. J Microbiol Biotechnol Food Sci (JMBFS) 2(1):152–161

    CAS  Google Scholar 

Download references

Conflict of Interest

Kokkinos P.A. declares that he has no conflict of interest. Ziros P.G. declares that he has no conflict of interest. Bellou M. declares that she has no conflict of interest. Vantarakis A. declares that he has no conflict of interest. This article does not contain any studies with human or animal subjects.

Author information

Authors and Affiliations

  1. Environmental Microbiology Unit, Department of Public Health, School of Medicine, University of Patras, Patras, Greece

    P. A. Kokkinos, P. G. Ziros, M. Bellou & A. Vantarakis

Authors
  1. P. A. Kokkinos
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. P. G. Ziros
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. M. Bellou
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. A. Vantarakis
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to A. Vantarakis.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kokkinos, P.A., Ziros, P.G., Bellou, M. et al. Loop-Mediated Isothermal Amplification (LAMP) for the Detection of Salmonella in Food. Food Anal. Methods 7, 512–526 (2014). https://doi.org/10.1007/s12161-013-9748-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12161-013-9748-8

Keywords

Search

Navigation