The Sensitivity and Specificity of Loop-Mediated Isothermal Amplification and PCR Methods in Detection of Foodborne Microorganisms: A Systematic Review and Meta-Analysis
-
Yasaman Sadeghi
,
Pegah Kananizadeh
,
Solmaz Ohadian Moghadam
,
Ahad Alizadeh
,
Mohammad Reza Pourmand
,
Neda Mohammadi
,
Davoud Afshar
,
Reza Ranjbar
Abstract
Background: The loop-mediated isothermal amplification (LAMP) method is frequently used for identifying many microorganisms. The present review aimed to evaluate the sensitivity and specificity of LAMP method for detection of food-borne bacteria and to compare these features with those of polymerase chain reaction (PCR), as an alternative molecular diagnostic procedure, and with cultivation method, as the gold standard method.
Methods: The literature was searched in electronic databases (PubMed, Scopus, Web of Science, and EMBASE) for recruiting publications within Jan 2000 to Jul 2021. We used the combinations of keywords including foodborne disease, LAMP, PCR, Loop-mediated isothermal amplification, and polymerase chain reaction. Meta-analysis was used to adjust the correlation and heterogeneity between the studies. The efficiency of the methods was presented by negative likelihood ratio, positive likelihood ratio, sensitivity, specificity, and odds ratio using forest plots. A P-value less than 0.05 was considered as statistical significance cut off. The confidence intervals were presented at the 95% interval.
Results: Overall, 23 relevant studies were analyzed. The sensitivities of LAMP and PCR methods were estimated to be 96.6% (95% CI: 95.0-97.7) and 95.6% (95%CI: 91.5-97.8), respectively. The specificities of LAMP and PCR were also estimated to be 97.6% (95%CI: 92.6-99.3) and 98.7% (95%CI: 96.5-99.5), respectively.
Conclusion: The specificities of LAMP and PCR assays were determined by comparing their results with cultivation method as the gold standard. Overall, the specificity of both PCR and LAMP methods was low for detection of fastidious bacteria. Nevertheless, LAMP and PCR methods have acceptable specificities and sensitivities, and their application in clinical practice necessitates more studies.
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2. Ranjbar R, Afshar D (2015). Development of a loop-mediated isothermal amplification assay for rapid detection of Yersinia enterocolitica via targeting a conserved locus. Iran J Microbiol, 7(4):185-90.
3. Notomi T, Okayama H, Masubuchi H, et al (2000). Loop-mediated isothermal amplification of DNA. Nucleic Acids Res, 28(12):E63.
4. Ushikubo H (2004). [Principle of LAMP method--a simple and rapid gene amplification method]. Uirusu, 54:107-112.
5. N Muhammad, M A Hossain, A K Musa, et al (2010). Seroepidemiological study of human brucellosis among the population at risk. Mymensingh Med J, 19(1):1-4.
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11. Khan M, Wang R, Li B, et al (2018). Comparative evaluation of the LAMP assay and PCR-based assays for the rapid detection of Alternaria solani. Front Microbiol, 9:2089.
12. Lakshmi BA, Kim S (2021). Recent trends in the utilization of LAMP for the diagnosis of viruses, bacteria, and allergens in food. Recent Developments in Applied Microbiology and Biochemistry, 2021: 291-297.
13. Mandal P, Biswas A, Choi K, Pal U (2011). Methods for rapid detection of foodborne pathogens: an overview. Am J Food Technol, 6:87-102.
14. Ailenberg M, Silverman M (2000). Controlled hot start and improved specificity in carrying out PCR utilizing touch-up and loop incorporated primers (TULIPS). Biotechniques, 29:1018-20, 1022-4.
15. Pöschl B, Waneesorn J, Thekisoe O, et al (2010). Comparative diagnosis of malaria infections by microscopy, nested PCR, and LAMP in northern Thailand. Am J Trop Med Hyg, 83:56-60.
16. Zhao H-B, Yin G-Y, Zhao G-P, et al (2014). Development of loop-mediated isothermal amplification (LAMP) for universal detection of enteroviruses. Indian J Microbiol, 54:80-86.
17. Sails AD, Fox AJ, Bolton FJ, et al (2003). A real-time PCR assay for the detection of Campylobacter jejuni in foods after enrichment culture. Appl Environ Microbiol, 69(3):1383-90.
18. Li X, Zhang S, Zhang H, et al (2009). A loop-mediated isothermal amplification method targets the phoP gene for the detection of Salmonella in food samples. Int J Food Microbiol, 133:252-258.
19. Yuan Y, Xu W, Zhai Z, et al (2009). Universal primer‐multiplex PCR approach for simultaneous detection of Escherichia coli, Listeria monocytogenes, and Salmonella spp. in food samples. J Food Sci, 74(8):M446-52.
20. Tavakoli HR, Najafi A, Ahmadi A (2010). Rapid, specific and concurrent detection of Listeria, Salmonella and Escherichia coli pathogens by multiplex PCR in Iranian food. Afr J Microbiol Res, 4:2503-2507.
21. Shalaby MA, Mohamed MS, Mansour MA, AS AE-H (2011). Comparison of polymerase chain reaction and conventional methods for diagnosis of Listeria monocytogenes isolated from different clinical specimens and food stuffs. Clin Lab, 57:919-924.
22. Tang M-J, Zhou S, Zhang X-Y, et al (2011). Rapid and sensitive detection of Listeria monocytogenes by loop-mediated isothermal amplification. Curr Microbiol, 63:511-516.
23. Wang F, Jiang L, Ge B (2012). Loop-mediated isothermal amplification assays for detecting Shiga toxin-producing Escherichia coli in ground beef and human stools. J Clin Microbiol, 50:91-97.
24. Nishimura N, Takaoka N, Baba Y, et al (2012). [Direct PCR detection of food-borne bacteria from mixed human feces]. Kansenshogaku Zasshi, 86(6):741-8.
25. Wang L, Li Y, Chu J, et al (2012). Development and application of a simple loop-mediated isothermal amplification method on rapid detection of Listeria monocytogenes strains. Mol Biol Rep, 39:445-449.
26. Xu Z, Li L, Chu J, et al (2012). Development and application of loop-mediated isothermal amplification assays on rapid detection of various types of staphylococci strains. Food Res Int, 47:166-173.
27. Delibato E, Anniballi F, Vallebona PS, et al (2013). Validation of a 1-day analytical diagnostic real-time PCR for the detection of Salmonella in different food meat categories. Food Anal Methods, 6:996–1003.
28. Vallières E, Saint-Jean M, Rallu F (2013). Comparison of three different methods for detection of Shiga toxin-producing Escherichia coli in a tertiary pediatric care center. J Clin Microbiol, 51:481-486.
29. Ishii S, Segawa T, Okabe S (2013). Simultaneous quantification of multiple food-and waterborne pathogens by use of microfluidic quantitative PCR. Appl Environ Microbiol, 79:2891-2898.
30. Wang L, Shi L, Su J, Ye Y, Zhong Q (2013). Detection of Vibrio parahaemolyticus in food samples using in situ loop-mediated isothermal amplification method. Gene, 515:421-425.
31. Wang YZ, Wang DG (2013). Development and evaluation of a loop-mediated isothermal amplification (LAMP) method for detecting foodborn Salmonella in raw milk. Advanced Materials Research, 647:577–582.
32. Hu Q, Lyu D, Shi X, et al (2014). A modified molecular beacons–based multiplex real-time PCR assay for simultaneous detection of eight foodborne pathogens in a single reaction and its application. Foodborne Pathog Dis, 11:207-214.
33. Rundell MS, Pingle M, Das S, et al (2014). A multiplex PCR/LDR assay for simultaneous detection and identification of the NIAID category B bacterial food and water-borne pathogens. Diagn Microbiol Infect Dis, 79(2):135-40.
34. Di H, Ye L, Neogi SB, et al (2015). Development and evaluation of a loop-mediated isothermal amplification assay combined with enrichment culture for rapid detection of very low numbers of Vibrio parahaemolyticus in seafood samples. Biol Pharm Bull, 38:82-87.
35. Yan M, Xu L, Jiang H, et al (2017). PMA-LAMP for rapid detection of Escherichia coli and shiga toxins from viable but non-culturable state. Microb Pathog, 105:245-250.
36. Han L, Wang K, Ma L, et al (2020). Viable but nonculturable Escherichia coli O157: H7 and Salmonella enterica in fresh produce: rapid determination by loop-mediated isothermal amplification coupled with a propidium monoazide treatment. Appl Environ Microbiol, 86:e02566-19.
37. Xu C, Luo H, Zhang Y (2020). Development of multiplex loop-mediated isothermal amplification for three foodborne pathogens. Food Science and Technology, 40(Suppl. 1): 205-210
38. Srimongkol G, Ditmangklo B, Choopara I, et al (2020). Rapid colorimetric loop-mediated isothermal amplification for hypersensitive point-of-care Staphylococcus aureus enterotoxin A gene detection in milk and pork products. Sci Rep, 10(1):7768.
39. Kreitlow A, Becker A, Schotte U, et al (2021). Establishment and validation of a loop-mediated isothermal amplification (LAMP) assay targeting the ttrRSBCA locus for rapid detection of Salmonella spp. in food. Food Control, 126:107973.
2. Ranjbar R, Afshar D (2015). Development of a loop-mediated isothermal amplification assay for rapid detection of Yersinia enterocolitica via targeting a conserved locus. Iran J Microbiol, 7(4):185-90.
3. Notomi T, Okayama H, Masubuchi H, et al (2000). Loop-mediated isothermal amplification of DNA. Nucleic Acids Res, 28(12):E63.
4. Ushikubo H (2004). [Principle of LAMP method--a simple and rapid gene amplification method]. Uirusu, 54:107-112.
5. N Muhammad, M A Hossain, A K Musa, et al (2010). Seroepidemiological study of human brucellosis among the population at risk. Mymensingh Med J, 19(1):1-4.
6. Keessen E, Hopman N, van Leengoed L, et al (2011). Evaluation of four different diagnostic tests to detect Clostridium difficile in piglets. J Clin Microbiol, 49(5):1816-21.
7. Panic N, Leoncini E, De Belvis G, et al (2013). Evaluation of the endorsement of the preferred reporting items for systematic reviews and meta-analysis (PRISMA) statement on the quality of published systematic review and meta-analyses. PLoS One, 8(12):e83138.
8. Asar S, Jalalpour S, Ayoubi F, et al (2016). PRISMA; Preferred Reporting Items for Systematic Reviews and Meta-Analyses. Journal of Rafsanjan University of Medical Sciences, 15(1): 68-80.
9. The R Development Core Team (2013). R: A language and environment for statistical computing.
http://softlibre.unizar.es/manuales/aplicaciones/r/fullrefman.pdf
10. Nliwasa M, MacPherson P, Chisala P, et al (2016). The sensitivity and specificity of loop-mediated isothermal amplification (LAMP) assay for tuberculosis diagnosis in adults with chronic cough in Malawi. PLoS One, 11:e0155101.
11. Khan M, Wang R, Li B, et al (2018). Comparative evaluation of the LAMP assay and PCR-based assays for the rapid detection of Alternaria solani. Front Microbiol, 9:2089.
12. Lakshmi BA, Kim S (2021). Recent trends in the utilization of LAMP for the diagnosis of viruses, bacteria, and allergens in food. Recent Developments in Applied Microbiology and Biochemistry, 2021: 291-297.
13. Mandal P, Biswas A, Choi K, Pal U (2011). Methods for rapid detection of foodborne pathogens: an overview. Am J Food Technol, 6:87-102.
14. Ailenberg M, Silverman M (2000). Controlled hot start and improved specificity in carrying out PCR utilizing touch-up and loop incorporated primers (TULIPS). Biotechniques, 29:1018-20, 1022-4.
15. Pöschl B, Waneesorn J, Thekisoe O, et al (2010). Comparative diagnosis of malaria infections by microscopy, nested PCR, and LAMP in northern Thailand. Am J Trop Med Hyg, 83:56-60.
16. Zhao H-B, Yin G-Y, Zhao G-P, et al (2014). Development of loop-mediated isothermal amplification (LAMP) for universal detection of enteroviruses. Indian J Microbiol, 54:80-86.
17. Sails AD, Fox AJ, Bolton FJ, et al (2003). A real-time PCR assay for the detection of Campylobacter jejuni in foods after enrichment culture. Appl Environ Microbiol, 69(3):1383-90.
18. Li X, Zhang S, Zhang H, et al (2009). A loop-mediated isothermal amplification method targets the phoP gene for the detection of Salmonella in food samples. Int J Food Microbiol, 133:252-258.
19. Yuan Y, Xu W, Zhai Z, et al (2009). Universal primer‐multiplex PCR approach for simultaneous detection of Escherichia coli, Listeria monocytogenes, and Salmonella spp. in food samples. J Food Sci, 74(8):M446-52.
20. Tavakoli HR, Najafi A, Ahmadi A (2010). Rapid, specific and concurrent detection of Listeria, Salmonella and Escherichia coli pathogens by multiplex PCR in Iranian food. Afr J Microbiol Res, 4:2503-2507.
21. Shalaby MA, Mohamed MS, Mansour MA, AS AE-H (2011). Comparison of polymerase chain reaction and conventional methods for diagnosis of Listeria monocytogenes isolated from different clinical specimens and food stuffs. Clin Lab, 57:919-924.
22. Tang M-J, Zhou S, Zhang X-Y, et al (2011). Rapid and sensitive detection of Listeria monocytogenes by loop-mediated isothermal amplification. Curr Microbiol, 63:511-516.
23. Wang F, Jiang L, Ge B (2012). Loop-mediated isothermal amplification assays for detecting Shiga toxin-producing Escherichia coli in ground beef and human stools. J Clin Microbiol, 50:91-97.
24. Nishimura N, Takaoka N, Baba Y, et al (2012). [Direct PCR detection of food-borne bacteria from mixed human feces]. Kansenshogaku Zasshi, 86(6):741-8.
25. Wang L, Li Y, Chu J, et al (2012). Development and application of a simple loop-mediated isothermal amplification method on rapid detection of Listeria monocytogenes strains. Mol Biol Rep, 39:445-449.
26. Xu Z, Li L, Chu J, et al (2012). Development and application of loop-mediated isothermal amplification assays on rapid detection of various types of staphylococci strains. Food Res Int, 47:166-173.
27. Delibato E, Anniballi F, Vallebona PS, et al (2013). Validation of a 1-day analytical diagnostic real-time PCR for the detection of Salmonella in different food meat categories. Food Anal Methods, 6:996–1003.
28. Vallières E, Saint-Jean M, Rallu F (2013). Comparison of three different methods for detection of Shiga toxin-producing Escherichia coli in a tertiary pediatric care center. J Clin Microbiol, 51:481-486.
29. Ishii S, Segawa T, Okabe S (2013). Simultaneous quantification of multiple food-and waterborne pathogens by use of microfluidic quantitative PCR. Appl Environ Microbiol, 79:2891-2898.
30. Wang L, Shi L, Su J, Ye Y, Zhong Q (2013). Detection of Vibrio parahaemolyticus in food samples using in situ loop-mediated isothermal amplification method. Gene, 515:421-425.
31. Wang YZ, Wang DG (2013). Development and evaluation of a loop-mediated isothermal amplification (LAMP) method for detecting foodborn Salmonella in raw milk. Advanced Materials Research, 647:577–582.
32. Hu Q, Lyu D, Shi X, et al (2014). A modified molecular beacons–based multiplex real-time PCR assay for simultaneous detection of eight foodborne pathogens in a single reaction and its application. Foodborne Pathog Dis, 11:207-214.
33. Rundell MS, Pingle M, Das S, et al (2014). A multiplex PCR/LDR assay for simultaneous detection and identification of the NIAID category B bacterial food and water-borne pathogens. Diagn Microbiol Infect Dis, 79(2):135-40.
34. Di H, Ye L, Neogi SB, et al (2015). Development and evaluation of a loop-mediated isothermal amplification assay combined with enrichment culture for rapid detection of very low numbers of Vibrio parahaemolyticus in seafood samples. Biol Pharm Bull, 38:82-87.
35. Yan M, Xu L, Jiang H, et al (2017). PMA-LAMP for rapid detection of Escherichia coli and shiga toxins from viable but non-culturable state. Microb Pathog, 105:245-250.
36. Han L, Wang K, Ma L, et al (2020). Viable but nonculturable Escherichia coli O157: H7 and Salmonella enterica in fresh produce: rapid determination by loop-mediated isothermal amplification coupled with a propidium monoazide treatment. Appl Environ Microbiol, 86:e02566-19.
37. Xu C, Luo H, Zhang Y (2020). Development of multiplex loop-mediated isothermal amplification for three foodborne pathogens. Food Science and Technology, 40(Suppl. 1): 205-210
38. Srimongkol G, Ditmangklo B, Choopara I, et al (2020). Rapid colorimetric loop-mediated isothermal amplification for hypersensitive point-of-care Staphylococcus aureus enterotoxin A gene detection in milk and pork products. Sci Rep, 10(1):7768.
39. Kreitlow A, Becker A, Schotte U, et al (2021). Establishment and validation of a loop-mediated isothermal amplification (LAMP) assay targeting the ttrRSBCA locus for rapid detection of Salmonella spp. in food. Food Control, 126:107973.
| Files | ||
| Issue | Vol 50 No 11 (2021) | |
| Section | Review Article(s) | |
| DOI | https://doi.org/10.18502/ijph.v50i11.7571 | |
| Keywords | ||
| Food-Borne Pathogen Specificity Sensitivity Loop-mediated isothermal amplification (LAMP) Polymerase chain reaction | ||
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How to Cite
1.
Sadeghi Y, Kananizadeh P, Ohadian Moghadam S, Alizadeh A, Pourmand MR, Mohammadi N, Afshar D, Ranjbar R. The Sensitivity and Specificity of Loop-Mediated Isothermal Amplification and PCR Methods in Detection of Foodborne Microorganisms: A Systematic Review and Meta-Analysis. Iran J Public Health. 2021;50(11):2172-2182.
