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  • Review Article
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Paper-based sensors for bacteria detection

Abstract

The detection of pathogenic bacteria is essential to prevent and treat infections and to provide food security. Current gold-standard detection techniques, such as culture-based assays and polymerase chain reaction, are time-consuming and require centralized laboratories. Therefore, efforts have focused on developing point-of-care devices that are fast, cheap, portable and do not require specialized training. Paper-based analytical devices meet these criteria and are particularly suitable to deployment in low-resource settings. In this Review, we highlight paper-based analytical devices with substantial point-of-care applicability for bacteria detection and discuss challenges and opportunities for future development.

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Fig. 1: Timeline of paper-based sensors.
Fig. 2: Commercial paper-based sensors.
Fig. 3: Operational process of paper-based sensors.

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References

  1. Gupta, A., Gupta, R. & Singh, R. L. in Principles and Applications of Environmental Biotechnology for a Sustainable Future (ed. Singh, R. L.) 43–84 (Springer, 2017).

  2. Doron, S. & Gorbach, S. L. in International Encyclopedia of Public Health (ed. Heggenhougen, H. K.) 273–282 (Academic, 2008).

  3. Thompson, T. et al. The staggering death toll of drug-resistant bacteria. https://doi.org/10.1038/d41586-022-00228-x (2022).

  4. Vos, T. et al. Global burden of 369 diseases and injuries in 204 countries and territories, 1990–2019: a systematic analysis for the Global Burden of Disease Study 2019. Lancet 396, 1204–1222 (2020).

    Article  Google Scholar 

  5. Murray, C. J. L. et al. Global burden of bacterial antimicrobial resistance in 2019: a systematic analysis. Lancet 399, 629–655 (2022).

    Article  Google Scholar 

  6. Baryeh, K., Takalkar, S., Lund, M. & Liu, G. in Medical Biosensors for Point of Care (POC) Applications (ed. Narayan, R. J.) 3–25 (Woodhead, 2017).

  7. Mabey, D., Peeling, R. W., Ustianowski, A. & Perkins, M. D. Diagnostics for the developing world. Nat. Rev. Microbiol. 2, 231–240 (2004).

    Article  Google Scholar 

  8. Nagaraj, S., Ramlal, S., Kingston, J. & Batra, H. V. Development of IgY based sandwich ELISA for the detection of staphylococcal enterotoxin G (SEG), an egc toxin. Int. J. Food Microbiol. 237, 136–141 (2016).

    Article  Google Scholar 

  9. Saravanan, A. et al. Methods of detection of food-borne pathogens: a review. Environ. Chem. Lett. 19, 189–207 (2021).

    Article  Google Scholar 

  10. Bordbar, M. M., Sheini, A., Hashemi, P., Hajian, A. & Bagheri, H. Disposable paper-based biosensors for the point-of-care detection of hazardous contaminations — a review. Biosensors 11, 316 (2021).

    Article  Google Scholar 

  11. Iwase, T. et al. A simple assay for measuring catalase activity: a visual approach. Sci. Rep. 3, 3081–3081 (2013).

    Article  Google Scholar 

  12. Saptalena, L. G., Kuklya, A. & Telgheder, U. Gas chromatography–differential mobility spectrometry and gas chromatography–mass spectrometry for the detection of coliform bacteria. Int. J. Mass. Spectrom. 388, 17–25 (2015).

    Article  Google Scholar 

  13. Aebisher, D., Bartusik, D. & Tabarkiewicz, J. Laser flow cytometry as a tool for the advancement of clinical medicine. Biomed. Pharmacother. 85, 434–443 (2017).

    Article  Google Scholar 

  14. Cheng, J. H. & Sun, D. W. Recent applications of spectroscopic and hyperspectral imaging techniques with chemometric analysis for rapid inspection of microbial spoilage in muscle foods. Compr. Rev. Food Sci. Food Saf. 14, 478–490 (2015).

    Article  Google Scholar 

  15. Pahlow, S. et al. Isolation and identification of bacteria by means of Raman spectroscopy. Adv. Drug Deliv. Rev. 89, 105–120 (2015).

    Article  Google Scholar 

  16. Dietvorst, J. et al. Bacteria detection at a single-cell level through a cyanotype-based photochemical reaction. Anal. Chem. 94, 787–792 (2022).

    Article  Google Scholar 

  17. Urdea, M. et al. Requirements for high impact diagnostics in the developing world. Nature 444, 73–79 (2006).

    Article  Google Scholar 

  18. Land, K. J., Boeras, D. I., Chen, X.-S., Ramsay, A. R. & Peeling, R. W. REASSURED diagnostics to inform disease control strategies, strengthen health systems and improve patient outcomes. Nat. Microbiol. 4, 46–54 (2019).

    Article  Google Scholar 

  19. Lee, W. G., Kim, Y.-G., Chung, B. G., Demirci, U. & Khademhosseini, A. Nano/microfluidics for diagnosis of infectious diseases in developing countries. Adv. Drug Deliv. Rev. 62, 449–457 (2010).

    Article  Google Scholar 

  20. Bradbury, D. W. et al. Automation of biomarker preconcentration, capture, and nanozyme signal enhancement on paper-based devices. Anal. Chem. 91, 12046–12054 (2019).

    Article  Google Scholar 

  21. Ruecha, N., Yamada, K., Suzuki, K. & Citterio, D. in Materials for Chemical Sensing (eds Paixão, T. R. L. C. & Reddy, S. M.) 29–74 (Springer, 2017).

  22. Han, S., Chopra, M., Rubino, I. & Choi, H.-J. in Paper-based Medical Diagnostic Devices: As a Part of Bioanalysis-advanced Materials, Methods, and Devices (ed. Lee, J. H.) 137–153 (Springer, 2021).

  23. Snyder, S. A. et al. Lysis and direct detection of coliforms on printed paper-based microfluidic devices. Lab Chip 20, 4413–4419 (2020).

    Article  Google Scholar 

  24. Liana, D. D., Raguse, B., Gooding, J. J. & Chow, E. Recent advances in paper-based sensors. Sensors 12, 11505–11526 (2012).

    Article  Google Scholar 

  25. Yao, Z. et al. Paper-based sensors for diagnostics, human activity monitoring, food safety and environmental detection. Sens. Diagn. 1, 312–342 (2022).

    Article  Google Scholar 

  26. Gooding, J. J. What Is a “real sample”? ACS Sens. 3, 1609–1609 (2018).

    Article  Google Scholar 

  27. Cate, D. M., Adkins, J. A., Mettakoonpitak, J. & Henry, C. S. Recent developments in paper-based microfluidic devices. Anal. Chem. 87, 19–41 (2015).

    Article  Google Scholar 

  28. Morbioli, G. G., Mazzu-Nascimento, T., Stockton, A. M. & Carrilho, E. Technical aspects and challenges of colorimetric detection with microfluidic paper-based analytical devices (μPADs) — a review. Anal. Chim. Acta 970, 1–22 (2017).

    Article  Google Scholar 

  29. Akyazi, T., Basabe-Desmonts, L. & Benito-Lopez, F. Review on microfluidic paper-based analytical devices towards commercialisation. Anal. Chim. Acta 1001, 1–17 (2018).

    Article  Google Scholar 

  30. Zhu, G. et al. Paper-based immunosensors: current trends in the types and applied detection techniques. Trends Anal. Chem. 111, 100–117 (2019).

    Article  Google Scholar 

  31. Wang, K., Wang, Z., Zeng, H., Luo, X. & Yang, T. Advances in portable visual detection of pathogenic bacteria. ACS Appl. Bio Mater. 3, 7291–7305 (2020).

    Article  Google Scholar 

  32. Cho, I.-H., Bhunia, A. & Irudayaraj, J. Rapid pathogen detection by lateral-flow immunochromatographic assay with gold nanoparticle-assisted enzyme signal amplification. Int. J. Food Microbiol. 206, 60–66 (2015).

    Article  Google Scholar 

  33. Yan, J. et al. Effect of physiochemical property of Fe3O4 particle on magnetic lateral flow immunochromatographic assay. Sens. Actuators B 197, 129–136 (2014).

    Article  Google Scholar 

  34. Song, C. et al. Development of a lateral flow colloidal gold immunoassay strip for the simultaneous detection of Shigella boydii and Escherichia coli O157:H7 in bread, milk and jelly samples. Food Control. 59, 345–351 (2016).

    Article  Google Scholar 

  35. Shin, J. H. et al. Multiplexed detection of foodborne pathogens from contaminated lettuces using a handheld multistep lateral flow assay device. J. Agric. Food Chem. 66, 290–297 (2018).

    Article  Google Scholar 

  36. Funes-Huacca, M. et al. Portable self-contained cultures for phage and bacteria made of paper and tape. Lab Chip 12, 4269–4278 (2012).

    Article  Google Scholar 

  37. Liu, H. et al. Visual and sensitive detection of viable pathogenic bacteria by sensing of RNA markers in gold nanoparticles based paper platform. Biosens. Bioelectron. 62, 38–46 (2014).

    Article  Google Scholar 

  38. Zhao, Y. et al. Rapid multiplex detection of 10 foodborne pathogens with an up-converting phosphor technology-based 10-channel lateral flow assay. Sci. Rep. 6, 21342 (2016).

    Article  Google Scholar 

  39. He, D., Wu, Z., Cui, B., Xu, E. & Jin, Z. Establishment of a dual mode immunochromatographic assay for Campylobacter jejuni detection. Food Chem. 289, 708–713 (2019).

    Article  Google Scholar 

  40. Zhang, H. et al. Rapid detection of methicillin-resistant Staphylococcus aureus in pork using a nucleic acid-based lateral flow immunoassay. Int. J. Food Microbiol. 243, 64–69 (2017).

    Article  Google Scholar 

  41. Liu, H.-b, Du, X.-j, Zang, Y.-X., Li, P. & Wang, S. SERS-based lateral flow strip biosensor for simultaneous detection of Listeria monocytogenes and Salmonella enterica serotype Enteritidis. J. Agric. Food Chem. 65, 10290–10299 (2017).

    Article  Google Scholar 

  42. Cui, X., Xiong, Q.-R., Xiong, Y.-H., Shan, S. & Lai, W.-H. Establishing of a method combined immunomagnetic separation with colloidal gold lateral flow assay and its application in rapid detection of Escherichia coli O157:H7. Chin. J. Anal. Chem. 41, 1812–1816 (2013).

    Article  Google Scholar 

  43. Liu, Y. et al. A highly sensitive and flexible magnetic nanoprobe labeled immunochromatographic assay platform for pathogen Vibrio parahaemolyticus. Int. J. Food Microbiol. 211, 109–116 (2015).

    Article  Google Scholar 

  44. Shi, L. et al. A novel method to detect Listeria monocytogenes via superparamagnetic lateral flow immunoassay. Anal. Bioanal. Chem. 407, 529–535 (2015).

    Article  Google Scholar 

  45. Pang, B. et al. Development of a low-cost paper-based ELISA method for rapid Escherichia coli O157:H7 detection. Anal. Biochem. 542, 58–62 (2018).

    Article  Google Scholar 

  46. Zhao, Y. et al. Rapid and accurate detection of Escherichia coli O157:H7 in beef using microfluidic wax-printed paper-based ELISA. Analyst 145, 3106–3115 (2020).

    Article  Google Scholar 

  47. Trinh, T. N. D., Thai, D. A. & Lee, N. Y. Pop-up paper-based and fully integrated microdevice for point-of-care testing of vancomycin-resistant Enterococcus. Sens. Actuators B 345, 130362 (2021).

    Article  Google Scholar 

  48. Zhuang, J. et al. SERS-based CRISPR/Cas assay on microfluidic paper analytical devices for supersensitive detection of pathogenic bacteria in foods. Biosens. Bioelectron. 207, 114167 (2022).

    Article  Google Scholar 

  49. Zhou, B. et al. CRISPR/Cas12a based fluorescence-enhanced lateral flow biosensor for detection of Staphylococcus aureus. Sens. Actuators B 351, 130906 (2022).

    Article  Google Scholar 

  50. Foo, P. C. et al. Loop-mediated isothermal amplification (LAMP) reaction as viable PCR substitute for diagnostic applications: a comparative analysis study of LAMP, conventional PCR, nested PCR (nPCR) and real-time PCR (qPCR) based on Entamoeba histolytica DNA derived from faecal sample. BMC Biotechnol. 20, 34 (2020).

    Article  Google Scholar 

  51. Qiu, E. M. et al. CRISPR-based detection of Helicobacter pylori in stool samples. Helicobacter 26, e12828 (2021).

    Article  Google Scholar 

  52. Seo, J. H. et al. Development of a high-throughput centrifugal loop-mediated isothermal amplification microdevice for multiplex foodborne pathogenic bacteria detection. Sens. Actuators B 246, 146–153 (2017).

    Article  Google Scholar 

  53. Chen, S. et al. A novel AuNPs colorimetric sensor for sensitively detecting viable Salmonella typhimurium based on dual aptamers. Food Control. 115, 107281 (2020).

    Article  Google Scholar 

  54. Yang, X., Zhou, X., Zhu, M. & Xing, D. Sensitive detection of Listeria monocytogenes based on highly efficient enrichment with vancomycin-conjugated brush-like magnetic nano-platforms. Biosens. Bioelectron. 91, 238–245 (2017).

    Article  Google Scholar 

  55. Pang, B. et al. Colorimetric detection of Staphylococcus aureus using gold nanorods labeled with yolk immunoglobulin and urease, magnetic beads, and a phenolphthalein impregnated test paper. Microchim. Acta 186, 611 (2019).

    Article  Google Scholar 

  56. You, S.-M. et al. Paper-based colorimetric detection of pathogenic bacteria in food through magnetic separation and enzyme-mediated signal amplification on paper disc. Anal. Chim. Acta 1151, 338252 (2021).

    Article  Google Scholar 

  57. Mazur, F., Tran, H., Kuchel, R. P. & Chandrawati, R. Rapid detection of listeriolysin O toxin based on a nanoscale liposome–gold nanoparticle platform. ACS Appl. Nano Mater. 3, 7270–7280 (2020).

    Article  Google Scholar 

  58. Alhogail, S., Suaifan, G. A. R. Y. & Zourob, M. Rapid colorimetric sensing platform for the detection of Listeria monocytogenes foodborne pathogen. Biosens. Bioelectron. 86, 1061–1066 (2016).

    Article  Google Scholar 

  59. Suaifan, G. A. R. Y., Alhogail, S. & Zourob, M. Rapid and low-cost biosensor for the detection of Staphylococcus aureus. Biosens. Bioelectron. 90, 230–237 (2017).

    Article  Google Scholar 

  60. Suaifan, G. A. R. Y., Alhogail, S. & Zourob, M. Paper-based magnetic nanoparticle-peptide probe for rapid and quantitative colorimetric detection of Escherichia coli O157:H7. Biosens. Bioelectron. 92, 702–708 (2017).

    Article  Google Scholar 

  61. Janzen, M. C., Ponder, J. B., Bailey, D. P., Ingison, C. K. & Suslick, K. S. Colorimetric sensor arrays for volatile organic compounds. Anal. Chem. 78, 3591–3600 (2006).

    Article  Google Scholar 

  62. Carey, J. R. et al. Rapid identification of bacteria with a disposable colorimetric sensing array. J. Am. Chem. Soc. 133, 7571–7576 (2011).

    Article  Google Scholar 

  63. Chen, Q., Li, H., Ouyang, Q. & Zhao, J. Identification of spoilage bacteria using a simple colorimetric sensor array. Sens. Actuators B 205, 1–8 (2014).

    Article  Google Scholar 

  64. Yang, M. et al. Machine learning-enabled non-destructive paper chromogenic array detection of multiplexed viable pathogens on food. Nat. Food 2, 110–117 (2021).

    Article  Google Scholar 

  65. Jia, Z. et al. Nondestructive multiplex detection of foodborne pathogens with background microflora and symbiosis using a paper chromogenic array and advanced neural network. Biosens. Bioelectron. 183, 113209 (2021).

    Article  Google Scholar 

  66. Ali, M. M. et al. A DNAzyme-based colorimetric paper sensor for Helicobacter pylori. Angew. Chem. Int. Ed. 58, 9907–9911 (2019).

    Article  Google Scholar 

  67. Song, C., Liu, J., Li, J. & Liu, Q. Dual FITC lateral flow immunoassay for sensitive detection of Escherichia coli O157:H7 in food samples. Biosens. Bioelectron. 85, 734–739 (2016).

    Article  Google Scholar 

  68. Pang, B. et al. Development of a self-priming PDMS/paper hybrid microfluidic chip using mixed-dye-loaded loop-mediated isothermal amplification assay for multiplex foodborne pathogens detection. Anal. Chim. Acta 1040, 81–89 (2018).

    Article  Google Scholar 

  69. Pisamayarom, K., Suriyasomboon, A. & Chaumpluk, P. Simple screening of Listeria monocytogenes based on a fluorescence assay via a laminated lab-on-paper chip. Biosensors 7, 56 (2017).

    Article  Google Scholar 

  70. Wang, Y., Ping, J., Ye, Z., Wu, J. & Ying, Y. Impedimetric immunosensor based on gold nanoparticles modified graphene paper for label-free detection of Escherichia coli O157:H7. Biosens. Bioelectron. 49, 492–498 (2013).

    Article  Google Scholar 

  71. Vizzini, P. et al. Highly sensitive detection of Campylobacter spp. in chicken meat using a silica nanoparticle enhanced dot blot DNA biosensor. Biosens. Bioelectron. 171, 112689 (2021).

    Article  Google Scholar 

  72. Preechakasedkit, P. et al. Development of a one-step immunochromatographic strip test using gold nanoparticles for the rapid detection of Salmonella Typhi in human serum. Biosens. Bioelectron. 31, 562–566 (2012).

    Article  Google Scholar 

  73. Cho, I.-H. & Irudayaraj, J. Lateral-flow enzyme immunoconcentration for rapid detection of Listeria monocytogenes. Anal. Bioanal. Chem. 405, 3313–3319 (2013).

    Article  Google Scholar 

  74. Bisha, B. et al. Colorimetric paper-based detection of Escherichia coli, Salmonella spp., and Listeria monocytogenes from large volumes of agricultural water. J. Vis. Exp. 88, 51414 (2014).

    Google Scholar 

  75. Singh, J., Sharma, S. & Nara, S. Nanogold based lateral flow assay for the detection of Salmonella Typhi in environmental water samples. Anal. Methods 7, 9281–9288 (2015).

    Article  Google Scholar 

  76. Hossain, S. M. Z. et al. Multiplexed paper test strip for quantitative bacterial detection. Anal. Bioanal. Chem. 403, 1567–1576 (2012).

    Article  Google Scholar 

  77. Zhang, L. et al. Ultrasensitive detection of viable Enterobacter sakazakii by a continual cascade nanozyme biosensor. Anal. Chem. 89, 10194–10200 (2017).

    Article  Google Scholar 

  78. Pan, R. et al. Gold nanoparticle-based enhanced lateral flow immunoassay for detection of Cronobacter sakazakii in powdered infant formula. J. Dairy Sci. 101, 3835–3843 (2018).

    Article  Google Scholar 

  79. Choi, J. R. et al. An integrated paper-based sample-to-answer biosensor for nucleic acid testing at the point of care. Lab Chip 16, 611–621 (2016).

    Article  Google Scholar 

  80. Han, J. et al. Nanozyme-based lateral flow assay for the sensitive detection of Escherichia coli O157:H7 in milk. J. Dairy Sci. 101, 5770–5779 (2018).

    Article  Google Scholar 

  81. Fu, J. et al. Dramatically enhanced immunochromatographic assay using cascade signal amplification for ultrasensitive detection of Escherichia coli O157:H7 in milk. J. Agric. Food Chem. 68, 1118–1125 (2020).

    Article  Google Scholar 

  82. Chen, M. et al. Dual gold nanoparticle lateflow immunoassay for sensitive detection of Escherichia coli O157:H7. Anal. Chim. Acta 876, 71–76 (2015).

    Article  Google Scholar 

  83. Wang, J.-Y. et al. Development of colloidal gold immunochromatographic signal-amplifying system for ultrasensitive detection of Escherichia coli O157:H7 in milk. RSC Adv. 5, 62300–62305 (2015).

    Article  Google Scholar 

  84. Lu, C., Gao, X., Chen, Y., Ren, J. & Liu, C. Aptamer-based lateral flow test strip for the simultaneous detection of Salmonella Typhimurium, Escherichia coli O157:H7 and Staphylococcus aureus. Anal. Lett. 53, 646–659 (2020).

    Article  Google Scholar 

  85. Ren, W., Cho, I.-H., Zhou, Z. & Irudayaraj, J. Ultrasensitive detection of microbial cells using magnetic focus enhanced lateral flow sensors. Chem. Commun. 52, 4930–4933 (2016).

    Article  Google Scholar 

  86. Wu, W. et al. A sensitive lateral flow biosensor for Escherichia coli O157:H7 detection based on aptamer mediated strand displacement amplification. Anal. Chim. Acta 861, 62–68 (2015).

    Article  Google Scholar 

  87. Hwang, J., Kwon, D., Lee, S. & Jeon, S. Detection of Salmonella bacteria in milk using gold-coated magnetic nanoparticle clusters and lateral flow filters. RSC Adv. 6, 48445–48448 (2016).

    Article  Google Scholar 

  88. Xia, S., Yu, Z., Liu, D., Xu, C. & Lai, W. Developing a novel immunochromatographic test strip with gold magnetic bifunctional nanobeads (GMBN) for efficient detection of Salmonella Choleraesuis in milk. Food Control. 59, 507–512 (2016).

    Article  Google Scholar 

  89. Xu, B. et al. Simultaneous identification and antimicrobial susceptibility testing of multiple uropathogens on a microfluidic chip with paper-supported cell culture arrays. Anal. Chem. 88, 11593–11600 (2016).

    Article  Google Scholar 

  90. Kim, H. J., Kwon, C. & Noh, H. Paper-based diagnostic system facilitating Escherichia coli assessments by duplex coloration. ACS Sens. 4, 2435–2441 (2019).

    Article  Google Scholar 

  91. Kim, H. J., Kwon, C., Lee, B. S. & Noh, H. One-step sensing of foodborne pathogenic bacteria using a 3D paper-based device. Analyst 144, 2248–2255 (2019).

    Article  Google Scholar 

  92. Wang, C., Gao, X., Wang, S. & Liu, Y. A smartphone-integrated paper sensing system for fluorescent and colorimetric dual-channel detection of foodborne pathogenic bacteria. Anal. Bioanal. Chem. 412, 611–620 (2020).

    Article  Google Scholar 

  93. Kim, J.-Y. & Yeo, M.-K. A fabricated microfluidic paper-based analytical device (μPAD) for in situ rapid colorimetric detection of microorganisms in environmental water samples. Mol. Cell. Toxicol. 12, 101–109 (2016).

    Article  Google Scholar 

  94. Ren, W., Liu, W. & Irudayaraj, J. A net fishing enrichment strategy for colorimetric detection of E. coli O157:H7. Sens. Actuators B 247, 923–929 (2017).

    Article  Google Scholar 

  95. Sun, J., Huang, J., Li, Y., Lv, J. & Ding, X. A simple and rapid colorimetric bacteria detection method based on bacterial inhibition of glucose oxidase-catalyzed reaction. Talanta 197, 304–309 (2019).

    Article  Google Scholar 

  96. Li, D. et al. A multiplex PCR method to detect 14 Escherichia coli serogroups associated with urinary tract infections. J. Microbiol. Methods 82, 71–77 (2010).

    Article  Google Scholar 

  97. Lee, J. W., Nguyen, V. D. & Seo, T. S. Paper-based molecular diagnostics for the amplification and detection of pathogenic bacteria from human whole blood and milk without a sample preparation step. BioChip J. 13, 243–250 (2019).

    Article  Google Scholar 

  98. Mukama, O. et al. An ultrasensitive and specific point-of-care CRISPR/Cas12 based lateral flow biosensor for the rapid detection of nucleic acids. Biosens. Bioelectron. 159, 112143 (2020).

    Article  Google Scholar 

  99. Qian, J. et al. A portable CRISPR Cas12a based lateral flow platform for sensitive detection of Staphylococcus aureus with double insurance. Food Control. 132, 108485 (2022).

    Article  Google Scholar 

  100. Lafleur, L. K. et al. A rapid, instrument-free, sample-to-result nucleic acid amplification test. Lab Chip 16, 3777–3787 (2016).

    Article  Google Scholar 

  101. Tang, R. et al. A fully disposable and integrated paper-based device for nucleic acid extraction, amplification and detection. Lab Chip 17, 1270–1279 (2017).

    Article  Google Scholar 

  102. Noiphung, J. & Laiwattanapaisal, W. Multifunctional paper-based analytical device for in situ cultivation and screening of Escherichia coli infections. Sci. Rep. 9, 1555 (2019).

    Article  Google Scholar 

  103. Wang, W. et al. Gold nanoparticle-based paper sensor for multiple detection of 12 Listeria spp. by P60-mediated monoclonal antibody. Food Agric. Immunol. 28, 274–287 (2017).

    Article  Google Scholar 

  104. Wang, L. et al. A lateral flow strip combined with Cas9 nickase-triggered amplification reaction for dual food-borne pathogen detection. Biosens. Bioelectron. 165, 112364 (2020).

    Article  Google Scholar 

  105. Li, H. B. et al. High concentration of Cas12a effector tolerates more mismatches on ssDNA. FASEB J. 35, e21153 (2021).

    Google Scholar 

  106. You, Y. et al. Highly specific and sensitive detection of Yersinia pestis by portable Cas12a-UPTLFA platform. Front. Microbiol. 12, 700016 (2021).

    Article  Google Scholar 

  107. Wang, H. et al. CRISPR/Cas9 bridged recombinase polymerase amplification with lateral flow biosensor removing potential primer-dimer interference for robust Staphylococcus aureus assay. Sens. Actuators B 369, 132293 (2022).

    Article  Google Scholar 

  108. Wang, W. et al. Identification and quantification of eight Listeria monocytogene serotypes from Listeria spp. using a gold nanoparticle-based lateral flow assay. Microchim. Acta 184, 715–724 (2017).

    Article  Google Scholar 

  109. Rodriguez-Quijada, C. et al. Optimization of paper-based nanoparticle immunoassays for direct detection of the bacterial pathogen V. parahaemolyticus in oyster hemolymph. Anal. Methods 12, 3056–3063 (2020).

    Article  Google Scholar 

  110. Srisa-Art, M., Boehle, K. E., Geiss, B. J. & Henry, C. S. Highly sensitive detection of Salmonella Typhimurium using a colorimetric paper-based analytical device coupled with immunomagnetic separation. Anal. Chem. 90, 1035–1043 (2018).

    Article  Google Scholar 

  111. Carrell, C. S. et al. Rotary manifold for automating a paper-based Salmonella immunoassay. RSC Adv. 9, 29078–29086 (2019).

    Article  Google Scholar 

  112. Bordbar, M. M., Tashkhourian, J., Tavassoli, A., Bahramali, E. & Hemmateenejad, B. Ultrafast detection of infectious bacteria using optoelectronic nose based on metallic nanoparticles. Sens. Actuators B 319, 128262 (2020).

    Article  Google Scholar 

  113. Lim Sung, H. et al. Colorimetric sensor array allows fast detection and simultaneous identification of sepsis-causing bacteria in spiked blood culture. J. Clin. Microbiol. 52, 592–598 (2014).

    Article  Google Scholar 

  114. Bordbar, M. M., Tashkhourian, J. & Hemmateenejad, B. Structural elucidation and ultrasensitive analyses of volatile organic compounds by paper-based nano-optoelectronic noses. ACS Sens. 4, 1442–1451 (2019).

    Article  Google Scholar 

  115. Fronczek, C. F., Park, T. S., Harshman, D. K., Nicolini, A. M. & Yoon, J.-Y. Paper microfluidic extraction and direct smartphone-based identification of pathogenic nucleic acids from field and clinical samples. RSC Adv. 4, 11103–11110 (2014).

    Article  Google Scholar 

  116. Kang, D.-K. et al. Rapid detection of single bacteria in unprocessed blood using integrated comprehensive droplet digital detection. Nat. Commun. 5, 5427 (2014).

    Article  Google Scholar 

  117. Tram, K., Kanda, P., Salena, B. J., Huan, S. & Li, Y. Translating bacterial detection by DNAzymes into a litmus test. Angew. Chem. Int. Ed. 53, 12799–12802 (2014).

    Article  Google Scholar 

  118. Huang, Z., Cui, X., Xie, Q.-Y., Liu, D.-F. & Lai, W.-H. Short communication: a novel method using immunomagnetic separation with a fluorescent nanobeads lateral flow assay for the rapid detection of low-concentration Escherichia coli O157:H7 in raw milk. J. Dairy Sci. 99, 9581–9585 (2016).

    Article  Google Scholar 

  119. Seok, Y. et al. A paper-based device for performing loop-mediated isothermal amplification with real-time simultaneous detection of multiple DNA targets. Theranostics 7, 2220–2230 (2017).

    Article  Google Scholar 

  120. Luo, K. et al. Comparison of 4 label-based immunochromatographic assays for the detection of Escherichia coli O157:H7 in milk. J. Dairy Sci. 100, 5176–5187 (2017).

    Article  Google Scholar 

  121. Ali, M. M. et al. A printed multicomponent paper sensor for bacterial detection. Sci. Rep. 7, 12335–12335 (2017).

    Article  Google Scholar 

  122. Trinh, T. N. D. & Lee, N. Y. A rapid and eco-friendly isothermal amplification microdevice for multiplex detection of foodborne pathogens. Lab Chip 18, 2369–2377 (2018).

    Article  Google Scholar 

  123. Xing, K.-Y. et al. Novel immunochromatographic assay based on Eu (III)-doped polystyrene nanoparticle-linker-monoclonal antibody for sensitive detection of Escherichia coli O157:H7. Anal. Chim. Acta 998, 52–59 (2018).

    Article  Google Scholar 

  124. Ahn, H., Batule, B. S., Seok, Y. & Kim, M.-G. Single-step recombinase polymerase amplification assay based on a paper chip for simultaneous detection of multiple foodborne pathogens. Anal. Chem. 90, 10211–10216 (2018).

    Article  Google Scholar 

  125. Na, M. et al. Determination of pathogenic bacteria–Bacillus anthrax spores in environmental samples by ratiometric fluorescence and test paper based on dual-emission fluorescent silicon nanoparticles. J. Hazard. Mater. 386, 121956 (2020).

    Article  Google Scholar 

  126. Zhang, M. et al. A newly developed paper embedded microchip based on LAMP for rapid multiple detections of foodborne pathogens. BMC Microbiol. 21, 197 (2021).

    Article  Google Scholar 

  127. Sheini, A. A point-of-care testing sensor based on fluorescent nanoclusters for rapid detection of septicemia in children. Sens. Actuators B 328, 129029 (2021).

    Article  Google Scholar 

  128. Adkins, J. A. et al. Colorimetric and electrochemical bacteria detection using printed paper- and transparency-based analytic devices. Anal. Chem. 89, 3613–3621 (2017).

    Article  Google Scholar 

  129. Jokerst, J. C. et al. Development of a paper-based analytical device for colorimetric detection of select foodborne pathogens. Anal. Chem. 84, 2900–2907 (2012).

    Article  Google Scholar 

  130. Sun, L. et al. A novel, simple and low-cost paper-based analytical device for colorimetric detection of Cronobacter spp. Anal. Chim. Acta 1036, 80–88 (2018).

    Article  Google Scholar 

  131. Ilhan, H. et al. The coupling of immunomagnetic enrichment of bacteria with paper-based platform. Talanta 201, 245–252 (2019).

    Article  Google Scholar 

  132. Schaumburg, F., Carrell, C. S. & Henry, C. S. Rapid bacteria detection at low concentrations using sequential immunomagnetic separation and paper-based isotachophoresis. Anal. Chem. 91, 9623–9630 (2019).

    Article  Google Scholar 

  133. Qiao, Z., Cai, Q., Fu, Y., Lei, C. & Yang, W. Visual and quantitative detection of E. coli O157:H7 by coupling immunomagnetic separation and quantum dot-based paper strip. Anal. Bioanal. Chem. 413, 4417–4426 (2021).

    Article  Google Scholar 

  134. Yu, J., Su, J., Zhang, J., Wei, X. & Guo, A. CdTe/CdS quantum dot-labeled fluorescent immunochromatography test strips for rapid detection of Escherichia coli O157:H7. RSC Adv. 7, 17819–17823 (2017).

    Article  Google Scholar 

  135. Hu, J. et al. Colorimetric-fluorescent-magnetic nanosphere-based multimodal assay platform for Salmonella detection. Anal. Chem. 91, 1178–1184 (2019).

    Article  Google Scholar 

  136. Bhardwaj, J., Devarakonda, S., Kumar, S. & Jang, J. Development of a paper-based electrochemical immunosensor using an antibody-single walled carbon nanotubes bio-conjugate modified electrode for label-free detection of foodborne pathogens. Sens. Actuators B 253, 115–123 (2017).

    Article  Google Scholar 

  137. Silva, N. F. D. et al. Development of a disposable paper-based potentiometric immunosensor for real-time detection of a foodborne pathogen. Biosens. Bioelectron. 141, 111317 (2019).

    Article  Google Scholar 

  138. Khan, M. S. et al. Electrically-receptive and thermally-responsive paper-based sensor chip for rapid detection of bacterial cells. Biosens. Bioelectron. 110, 132–140 (2018).

    Article  Google Scholar 

  139. Mondal, D., Binish, R., Samanta, S., Paul, D. & Mukherji, S. Detection of total bacterial load in water samples using a disposable impedimetric sensor. IEEE Sens. J. 20, 1712–1720 (2020).

    Article  Google Scholar 

  140. Muhammad-Tahir, Z. & Alocilja, E. C. Fabrication of a disposable biosensor for Escherichia coli O157:H7 detection. IEEE Sens. J. 3, 345–351 (2003).

    Article  Google Scholar 

  141. Lin, Y.-H. et al. Disposable amperometric immunosensing strips fabricated by Au nanoparticles-modified screen-printed carbon electrodes for the detection of foodborne pathogen Escherichia coli O157:H7. Biosens. Bioelectron. 23, 1832–1837 (2008).

    Article  Google Scholar 

  142. Karuppiah, S., Mishra, N. C., Tsai, W.-C., Liao, W.-S. & Chou, C.-F. Ultrasensitive and low-cost paper-based graphene oxide nanobiosensor for monitoring water-borne bacterial contamination. ACS Sens. 6, 3214–3223 (2021).

    Article  Google Scholar 

  143. Morales-Narváez, E., Naghdi, T., Zor, E. & Merkoçi, A. Photoluminescent lateral-flow immunoassay revealed by graphene oxide: highly sensitive paper-based pathogen detection. Anal. Chem. 87, 8573–8577 (2015).

    Article  Google Scholar 

  144. Han, S.-M. et al. Performance characterization of two-dimensional paper chromatography-based biosensors for biodefense, exemplified by detection of Bacillus anthracis spores. BioChip J. 12, 59–68 (2018).

    Article  Google Scholar 

  145. Gumustas, A. et al. Paper based lateral flow immunoassay for the enumeration of Escherichia coli in urine. Anal. Methods 10, 1213–1218 (2018).

    Article  Google Scholar 

  146. Huang, F., Zhang, H., Wang, L., Lai, W. & Lin, J. A sensitive biosensor using double-layer capillary based immunomagnetic separation and invertase-nanocluster based signal amplification for rapid detection of foodborne pathogen. Biosens. Bioelectron. 100, 583–590 (2018).

    Article  Google Scholar 

  147. Choi, J. R., Nilghaz, A., Chen, L., Chou, K. C. & Lu, X. Modification of thread-based microfluidic device with polysiloxanes for the development of a sensitive and selective immunoassay. Sens. Actuators B 260, 1043–1051 (2018).

    Article  Google Scholar 

  148. Klug, K. E., Reynolds, K. A. & Yoon, J.-Y. A capillary flow dynamics-based sensing modality for direct environmental pathogen monitoring. Chem. A Eur. J. 24, 6025–6029 (2018).

    Article  Google Scholar 

  149. Weng, X., Kang, Y., Guo, Q., Peng, B. & Jiang, H. Recent advances in thread-based microfluidics for diagnostic applications. Biosens. Bioelectron. 132, 171–185 (2019).

    Article  Google Scholar 

  150. Alsaeed, B. & Mansour, F. R. Distance-based paper microfluidics; principle, technical aspects and applications. Microchem. J. 155, 104664 (2020).

    Article  Google Scholar 

  151. Kim, S. et al. Human sensor-inspired supervised machine learning of smartphone-based paper microfluidic analysis for bacterial species classification. Biosens. Bioelectron. 188, 113335 (2021).

    Article  Google Scholar 

  152. Cho, S., Park, T. S., Nahapetian, T. G. & Yoon, J.-Y. Smartphone-based, sensitive µPAD detection of urinary tract infection and gonorrhea. Biosens. Bioelectron. 74, 601–611 (2015).

    Article  Google Scholar 

  153. Sweeney, R. E., Budiman, E. & Yoon, J.-Y. Mie scatter spectra-based device for instant, contact-free, and specific diagnosis of bacterial skin infection. Sci. Rep. 7, 4801 (2017).

    Article  Google Scholar 

  154. Li, M., Wang, L., Qi, W., Liu, Y. & Lin, J. Challenges and perspectives for biosensing of bioaerosol containing pathogenic microorganisms. Micromachines 12, 798 (2021).

    Article  Google Scholar 

  155. Seok, Y., Lee, J. & Kim, M.-G. Paper-based airborne bacteria collection and DNA extraction kit. Biosensors 11, 375 (2021).

    Article  Google Scholar 

  156. Seok, Y., Jang, H., Oh, J., Joung, H.-A. & Kim, M.-G. A handheld lateral flow strip for rapid DNA extraction from Staphylococcus aureus cell spiked in various samples. Biomed. Phys. Eng. Express 5, 035035 (2019).

    Article  Google Scholar 

  157. Nguyen, D. T., Kim, H. R., Jung, J. H., Lee, K.-B. & Kim, B. C. The development of paper discs immobilized with luciferase/D-luciferin for the detection of ATP from airborne bacteria. Sens. Actuators B 260, 274–281 (2018).

    Article  Google Scholar 

  158. Park, C., Lee, J., Lee, D. & Jang, J. Paper-based electrochemical peptide sensor for label-free and rapid detection of airborne Bacillus anthracis simulant spores. Sens. Actuators B 355, 131321 (2022).

    Article  Google Scholar 

  159. Garland, T. Jr & Kelly, S. A. Phenotypic plasticity and experimental evolution. J. Exp. Biol. 209, 2344–2361 (2006).

    Article  Google Scholar 

  160. Matuła, K. et al. Phenotypic plasticity of Escherichia coli upon exposure to physical stress induced by ZnO nanorods. Sci. Rep. 9, 8575 (2019).

    Article  Google Scholar 

  161. Kumar, A. A. et al. From the bench to the field in low-cost diagnostics: two case studies. Angew. Chem. Int. Ed. 54, 5836–5853 (2015).

    Article  Google Scholar 

  162. Sena-Torralba, A. et al. Paper-based electrophoretic bioassay: biosensing in whole blood operating via smartphone. Anal. Chem. 93, 3112–3121 (2021).

    Article  Google Scholar 

  163. Pan, H. et al. Quantitative detection of viable but nonculturable state Escherichia coli O157:H7 by ddPCR combined with propidium monoazide. Food Control. 112, 107140 (2020).

    Article  Google Scholar 

  164. Gonzalez-Solino, C. & Lorenzo, M. D. Enzymatic fuel cells: towards self-powered implantable and wearable diagnostics. Biosensors 8, 11 (2018).

    Article  Google Scholar 

  165. Escalona-Villalpando, R. A. et al. Improving the performance of lactate/oxygen biofuel cells using a microfluidic design. J. Power Sources 342, 546–552 (2017).

    Article  Google Scholar 

  166. Fozouni, P. et al. Amplification-free detection of SARS-CoV-2 with CRISPR–Cas13a and mobile phone microscopy. Cell 184, 323–333 (2021).

    Article  Google Scholar 

  167. Pang, Y. et al. CRISPR–Cas12a mediated SERS lateral flow assay for amplification-free detection of double-stranded DNA and single-base mutation. Chem. Eng. J. 429, 132109 (2022).

    Article  Google Scholar 

  168. Suea-Ngam, A., Howes, P. D. & deMello, A. J. An amplification-free ultra-sensitive electrochemical CRISPR/Cas biosensor for drug-resistant bacteria detection. Chem. Sci. 12, 12733–12743 (2021).

    Article  Google Scholar 

  169. Parolo, C. et al. Tutorial: design and fabrication of nanoparticle-based lateral-flow immunoassays. Nat. Protoc. 15, 3788–3816 (2020).

    Article  Google Scholar 

  170. Khanal, B., Pokhrel, P., Khanal, B. & Giri, B. Machine-learning-assisted analysis of colorimetric assays on paper analytical devices. ACS Omega 6, 33837–33845 (2021).

    Article  Google Scholar 

  171. Ding, X., Mauk, M. G., Yin, K., Kadimisetty, K. & Liu, C. Interfacing pathogen detection with smartphones for point-of-care applications. Anal. Chem. 91, 655–672 (2019).

    Article  Google Scholar 

  172. Estcourt, C. S. et al. The eSexual Health Clinic system for management, prevention, and control of sexually transmitted infections: exploratory studies in people testing for Chlamydia trachomatis. Lancet Public Health 2, e182–e190 (2017).

    Article  Google Scholar 

  173. Carlisle, R. Scientific American Inventions and Discoveries: All the Milestones in Ingenuity — From the Discovery of Fire to the Invention of the Microwave Oven (Wileys, 2004).

  174. Maumené, M. On a new reagent for ascertaining the presence of sugar in certain liquids. Phil. Mag. Ser. 36, 482–482 (1850).

    Google Scholar 

  175. Comer, J. P. Semiquantitative specific test paper for glucose in urine. Anal. Chem. 28, 1748–1750 (1956).

    Article  Google Scholar 

  176. Free, A. H., Adams, E. C., Kercher, M. L., Free, H. M. & Cook, M. H. Simple specific test for urine glucose. Clin. Chem. 3, 163–168 (1957).

    Article  Google Scholar 

  177. Hawkes, R., Niday, E. & Gordon, J. A dot-immunobinding assay for monoclonal and other antibodies. Anal. Biochem. 119, 142–147 (1982).

    Article  Google Scholar 

  178. Martinez, A. W., Phillips, S. T., Butte, M. J. & Whitesides, G. M. Patterned paper as a platform for inexpensive, low-volume, portable bioassays. Angew. Chem. Int. Ed. 46, 1318–1320 (2007).

    Article  Google Scholar 

  179. Dungchai, W., Chailapakul, O. & Henry, C. S. Electrochemical detection for paper-based microfluidics. Anal. Chem. 81, 5821–5826 (2009).

    Article  Google Scholar 

  180. Castro Arnold, R. et al. Novel point-of-care test for simultaneous detection of nontreponemal and treponemal antibodies in patients with syphilis. J. Clin. Microbiol. 48, 4615–4619 (2010).

    Article  Google Scholar 

  181. World Health Organization Regional Office for Europe. Circular economy and health: opportunities and risks (WHO, 2018).

  182. Corona, B., Shen, L., Reike, D., Rosales Carreón, J. & Worrell, E. Towards sustainable development through the circular economy — a review and critical assessment on current circularity metrics. Resour. Conserv. Recycl. 151, 104498 (2019).

    Article  Google Scholar 

  183. Arruda, E. H., Melatto, R. A. P. B., Levy, W. & Conti, D. D. M. Circular economy: a brief literature review (2015–2020). Sustain. Oper. Comput. 2, 79–86 (2021).

    Article  Google Scholar 

  184. Hofstetter, J. S. et al. From sustainable global value chains to circular economy — different silos, different perspectives, but many opportunities to build bridges. Circ. Econ. Sust. 1, 21–47 (2021).

    Article  Google Scholar 

  185. Street, A., Vernooij, E. & Rogers, M. H. Diagnostic waste: whose responsibility? Global. Health 18, 30 (2022).

    Article  Google Scholar 

  186. Parashar, N. & Hait, S. Plastics in the time of COVID-19 pandemic: protector or polluter? Sci. Total Environ. 759, 144274 (2021).

    Article  Google Scholar 

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Acknowledgements

R.C. acknowledges support from the National Health and Medical Research Council Emerging Leadership Investigator Grant (NHMRC APP1173428) and the UNSW Scientia Fellowship.

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F.M. conceptualized the content, investigated the literature, analysed the data, wrote and revised the manuscript and designed the figures. A.D.T. investigated the literature, analysed the data, wrote the manuscript and designed the figures. Y.Z. investigated the literature, analysed the data and wrote the manuscript. Y.G. investigated the literature, analysed the data and wrote the manuscript. R.C. conceptualized the content, investigated the literature, revised the manuscript and supervised the project.

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COVID-19 rapid antigen test: https://asm.org/Articles/2020/August/How-the-SARS-CoV-2-EUA-Antigen-Tests-Work

National policy targets: https://www.epa.nsw.gov.au/your-environment/recycling-and-reuse/response-to-china-national-sword/circular-economy-policy

SDG12: https://www.euro.who.int/__data/assets/pdf_file/0004/374917/Circular-Economy_EN_WHO_web_august-2018.pdf

Top 10 global causes of death in 2019: https://www.who.int/data/gho/data/themes/mortality-and-global-health-estimates

Unsafe food: https://www.who.int/NEWS-ROOM/FACT-SHEETS/DETAIL/FOOD-SAFETY

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Mazur, F., Tjandra, A.D., Zhou, Y. et al. Paper-based sensors for bacteria detection. Nat Rev Bioeng 1, 180–192 (2023). https://doi.org/10.1038/s44222-023-00024-w

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