Advances in airborne microorganisms detection using biosensors: A critical review

doi:10.1007/s11783-021-1420-8

Frontiers of Environmental Science & Engineering

2021, Vol. 15

Issue (3): 47 https://doi.org/10.1007/s11783-021-1420-8

本期目录

Advances in airborne microorganisms detection using biosensors: A critical review

Jinbiao Ma^1,², Manman Du^1,², Can Wang^1,²(

), Xinwu Xie^3,⁴(

), Hao Wang^3,⁵, Qian Zhang⁶

¹. School of Environmental Science and Engineering, Tianjin University, Tianjin 300072, China
². Tianjin Key Laboratory of Indoor Air Environmental Quality Control, Tianjin 300072, China
³. Institute of Medical Support Technology, Academy of Military Science, Tianjin 300161, China
⁴. National Bio-Protection Engineering Center, Tianjin 300161, China
⁵. School of Electronic Information and Automation, Tianjin University of Science and Technology, Tianjin 300222, China
⁶. School of Mechanical Engineering and Safety Engineering, Institute of Particle Technology, University of Wuppertal, Wuppertal D-42119, Germany

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Abstract：

• Airborne microorganism detection methods are summarized.

• Biosensors play an important role in detecting airborne microorganisms.

• The principle of biosensor detection of airborne microorganisms is introduced.

• The application and progress of biosensor in recent years is summarized.

• The future perspectives of biosensor are identified.

Humanity has been facing the threat of a variety of infectious diseases. Airborne microorganisms can cause airborne infectious diseases, which spread rapidly and extensively, causing huge losses to human society on a global scale. In recent years, the detection technology for airborne microorganisms has developed rapidly; it can be roughly divided into biochemical, immune, and molecular technologies. However, these technologies still have some shortcomings; they are time-consuming and have low sensitivity and poor stability. Most of them need to be used in the ideal environment of a laboratory, which limits their applications. A biosensor is a device that converts biological signals into detectable signals. As an interdisciplinary field, biosensors have successfully introduced a variety of technologies for bio-detection. Given their fast analysis speed, high sensitivity, good portability, strong specificity, and low cost, biosensors have been widely used in environmental monitoring, medical research, food and agricultural safety, military medicine and other fields. In recent years, the performance of biosensors has greatly improved, becoming a promising technology for airborne microorganism detection. This review introduces the detection principle of biosensors from the three aspects of component identification, energy conversion principle, and signal amplification. It also summarizes its research and application in airborne microorganism detection. The new progress and future development trend of the biosensor detection of airborne microorganisms are analyzed.

Key words： Biosensor Airborne microorganisms Microbiological detection technology

收稿日期: 2020-10-28 出版日期: 2021-04-12

Corresponding Author(s): Can Wang,Xinwu Xie

引用本文:

. [J]. Frontiers of Environmental Science & Engineering, 2021, 15(3): 47.
Jinbiao Ma, Manman Du, Can Wang, Xinwu Xie, Hao Wang, Qian Zhang. Advances in airborne microorganisms detection using biosensors: A critical review. Front. Environ. Sci. Eng., 2021, 15(3): 47.

链接本文:

https://academic.hep.com.cn/fese/CN/10.1007/s11783-021-1420-8
https://academic.hep.com.cn/fese/CN/Y2021/V15/I3/47

Tab.1

Detection method	Advantage	Disadvantage	Reference
Culture	1. Relatively simple operation 2. Low cost, and less equipment investment 3. Used for strain typing and drug resistance detection	1. Large workload, and long detection time 2. Low sensitivity 3. Difficult to cultivate some microorganisms or require high biological safety	Hudu et al., 2016; Gupta and Kakkar, 2018
Medical imaging	1. Short detection time 2. fast analysis speed	1. Need professional equipment 2. Low specificity 3. Invasive 4. Not suitable for early-stage patients	Brenner and Hall, 2007; Seibel et al., 2020
Immune technology	1. Medium sensitivity, capable of determining small or limited amounts of enzymes in samples 2. Medium specificity, not easily affected by impurities 3. Medium detection time, suitable for large number of samples	1. Prone to “false positives” affecting the results 2. Many measurement steps and complicated operation 3. High measurement cost	Phunpae et al., 2014; Fronczek and Yoon, 2015; Mekonnen et al., 2020
Polymerase chain reaction	1. High sensitivity 2. High specificity, low sample purity requirements 3. Used for strain typing and drug resistance detection 4. Medium detection time	1. High measurement cost 2. Complex cyclic process, high technical requirements, and professional equipment 3. Unable to distinguish between living and dead microorganisms	Weile and knabbe, 2009; Paolucci et al., 2010; Eddabra and Ait Benhassou, 2018
Gene Sequencing	1. Good stability, and specificity 2. High detection accuracy	1. Large workload, and long detection time 2. High measurement cost	Schlaberg et al., 2017
Biosensor	1. High sensitivity, and high specificity 2. Short detection time, and fast analysis speed 3. Flexible and portable, suitable for on-site testing 4. Low cost	1. High sample purity requirements, weak anti-interference ability 2. Poor detection stability 3. Poor repeatability	Nidzworski et al., 2014; Cui and Zhou, 2020

Tab.2

Fig.1

Fig.2

Fig.3

Virus	Sensor type	Sample	Range	Detection limit	Response time	Detection target	Reference
SARS-CoV-2	FET biosensor	Culture medium; Nasopharyngeal swabs	Protein: 1 fg/mL – 100 pg/mL; SARS-CoV-2 in culture medium: 1.6 × 10¹ – 1.6 × 10⁴ PFU/mL; Clinical samples: 1 × 10¹- 1 × 10⁵ copies/mL	Protein: 1 fg/mL; SARS-CoV-2 in culture medium: 1.6 × 10¹ PFU/mL; Clinical samples: 2.42 × 10² copies/mL	50 s	SARS-CoV-2 antigen protein, cultured SARS-CoV-2, or SARS-CoV-2 from clinical samples	Seo et al., 2020
	Electrochemical biosensor	Cell-containing medium	10 fg/mL – 1 µg/mL	1 fg/mL	3 min	SARS-CoV-2 S1 spike protein	Mavrikou et al., 2020
	SPR biosensors	Oligonucleotide	0.1 pM – 1 μM	0.22±0.08 pM	–	RNA-dependent RNA polymerase-COVID sequences	Qiu et al., 2020
SARS-CoV	SPR biosensor	Rabbit anti- SARS coronaviral surface antigen (SCVme)	200 ng/mL – 100 μg/mL	200 ng/mL	10 min	Anti-SCVme	Park et al., 2009
	Nanowire FET biosensor	Nucleocapsid (N) protein	0.6 – 10 nM	0.6 nM	10 min	N protein	Ishikawa et al., 2009
H1N1 Influenza virus	Paired surface plasma waves biosensor	Throat swab	18 – 1.8 × 10⁶ PFU/mL	30 PFU/mL	20 min	Swine-origin influenza virus	Su et al., 2012
	FET biosensor	H1N1 HA	50 aM – 5 nM	50 aM	–	HA	Hideshima et al., 2013
	Electrochemical immunesensor	Throat swab	10 – 100 pg/mL	20 pg/mL (80 – 100 virions/μL)	30 min	Structural protein in the virion	Nidzworski et al., 2014
	SPR biosensor	Recombinant influenza virus A	10 pg/mL – 10 μg/mL	50.5 pg/mL	–	Anti-hemagglutinin (HA)	Ahmed et al., 2017
	Electrochemical biosensor	Nasal swab	10³ – 10⁸ PFU/sample	10² PFU/sample	15 min	H1N1 influenza virus	Cui et al., 2017

	Electrochemical impedance aptasensor	Inactivated H1N1 viruses	9 – 900 ng/L	0.9 pg/uL	30 min	Inactivated influenza A virus subtype H1N1	Bai et al., 2018
	Electrochemical impedance sensor	Influenza virus DNA	1 pM – 10 nM	8.4 pM	–	Influenza virus DNA	Lee et al., 2018
	Electrochemical biosensor	Mini-HA protein and H1N1 viruses	0 – 10⁶ PFU/mL	3.7 PFU/mL	30 min	Mini-HA protein and H1N1 viruses	Bhardwaj et al., 2019
H7N9 Influenza virus	Upconversion luminescence resonance energy Biosensor	H7 oligonucleotide	1 pM – 10 nM	7 pM	2 h	H7 oligonucleotide	Ye et al., 2014
	Electrochemical DNA biosensor	Throat swab	1 pM – 100 nM	100 fM	100 s	HA gene sequence	Dong et al., 2015
	Electrochemical immunesensor	Inactivated H7N9 avian influenza virus (AIV)	0.01 – 20 ng/mL	6.8 pg/mL	–	H7N9 AIV	Wu et al., 2015
	Electrochemical biosensor	H7N9 virus DNA	50 fM – 100 pM	9.4 fM	150 min	H7N9 virus DNA	Yu et al., 2015
	Electrochemical immunesensor	AIV H7	1.6 pg/mL – 16 ng/mL	1.6 pg/mL	30 min	AIV H7	Huang et al., 2016
	Electrochemical immunesensor	AIV H7	1 – 25 ng/mL	0.43 ng/mL	20 min	AIV H7	Tian et al., 2017
	SPR biosensor	H7N9 virus mixed with nasal mucosa	2.3 × 10² – 2.3 × 10⁵ copies/mL	402 copies/mL	10 min	H7N9 virus	Chang et al., 2018
H5N1 Influenza virus	SPR biosensor	Poultry swab	0.128 – 12.8 HAU/50 μL	0.128 HAU/50 μL	1.5 h	H5N1 AIV	Bai et al., 2012
	Electrochemical immunesensor	Chicken red blood cells	10¹ – 10³ EID₅₀/mL	10³ EID₅₀/mL	2 h	H5N1 AIV	Lum et al., 2012
	Electrochemical DNA biosensor	H5N1 AIV HA and neuraminidase (NA)	8 – 100 nM	18 nM	–	HA and NA	Grabowska et al., 2013
	Fluorescence biosensor	H5N1 antibody	5.0 nM – 1.0 μM	1.6 nM	–	H5N1 antibody	Wei et al., 2013
	Electrochemical impedance aptasensor	H5N1 virus and chicken swab	0.125 – 16 HAU/50 μL	H5N1 virus: 0.125 HAU/50 μL chicken swab: 1 HAU/50 mL	–	H5N1 virus	Karash et al., 2016
	SPR biosensor	H5N1-infected feces	1 × 10⁴ – 1 × 10⁶ EID₅₀/mL	1000 EID₅₀/mL	–	H5N1 AIV	Nguyen et al., 2016

	FET biosensor	Chicken serum	10 pM – 10 nM	5.9 pM	–	HA protein	Kwon et al., 2020
Rotavirus	Photonic crystal biosensors	Culture/ Feces	0.02 × 10⁴ – 5.77 × 10⁴ FFU/mL	0.18 × 10⁴ FFU/mL	30 min	Rotavirus	Pineda et al., 2009
	Fluorescence biosensor	Rotavirus	10³ – 10⁵ PFU/mL	10⁵ PFU/mL	–	Rotavirus cell	Jung et al., 2010

	FET biosensor	Pure rotavirus stock and fecal sample	Pure rotavirus stock: 10 – 10⁵ PFU/mL fecal sample: 10 – 10⁴ PFU/mL	Pure rotavirus stock: 10² PFU/mL fecal sample: 10³ PFU/mL	50 min	Rotavirus	Liu et al., 2013
	3D photonic crystal biosensor	Rotavirus antigen	2.54 – 127 μg/mL	6.35 μg/mL	–	Rotavirus	Maeng et al., 2016
Dengue virus	Innovative silicon nanowire FET sensor	Viral RNA mini kit	1 – 100 fM	10 fM	30 min	RNA	Zhang et al., 2010
	Electrochemical impedance biosensor	Vero cells	5.5 × 10³ – 8.4 × 10⁵ TCID₅₀/mL	8.4 × 10² TCID₅₀/mL	–	Dengue virus	Wasik et al., 2017
	Optical DNA-based biosensor	Saliva and urine	0.1 fM – 0.1 nM	0.2 aM	90 min	DNA	Ariffin et al., 2018
	Solid-state optical DNA biosensor	Serum, Urine, and Saliva	1 fM – 1 × mM	0.121 fM	15 min	Dengue virus serotype 2 genome	Mazlan et al., 2019
Vaccinia virus	Evanescent wave biosensor Optic biosensor	Throat culture swab specimens	1.3 × 10¹ – 1.3 × 10⁸ PFU/mL	2.5 × 10⁵ pfu/ml	–	Variola virus	Donaldson et al., 2004
	Electrochemical impedance biosensor	Human blood cells	0 – 3500 PFU/50 μL	330 PFU/50 μL	–	Variola virus	Labib et al., 2012

Tab.3

Bacteria	Sensor type	Sample	Range		Response time	Detection target	Reference
Pneumococcus	Electrochemical biosensor	Serotype	10⁰ – 10⁴ CFU/sample	10² CFU/sample	15 min	S. pneumoniae	Cui et al., 2017
	Electrochemical impedance biosensor	Bacteria in Mueller-Hinton medium	10¹ – 10⁷ CFU/mL	10¹ CFU/mL	–	K. pneumoniae	Silva Junior et al., 2018
Yersinia pestis	Phosphor biosensor	Lung tissue homogenates infected Balb/c mice	10⁴ – 10⁸ CFU/mL	10⁴ CFU/mL	30 min	The whole cells of Y. pestis	Yan et al., 2006
	Fiber optic biosensor	Serum	0 – 10³ ng/mL	10 ng/mL	40 min	Anti-F1 antibodies	Wei et al., 2007
	Magnetic biosensor	Buffer and human blood serum	25 – 300 ng/mL	2.5 ng/mL	–	Y. pestis antigen F1	Meyer et al., 2007
Staphylococcus aureus	Electrochemical biosensor	Apple juice samples and water	2.0 – 2.0 × 10⁶ CFU/mL	2 CFU/mL	2 min	S. aureus	Bhardwaj et al., 2016
	Fluorescent MOF biosensor	Culture medium and cream pastry samples	40 – 4 × 10⁸ CFU/mL	31 CFU/mL	20 min	S. aureus	Bhardwaj et al., 2017
	Autoinducer peptide-based electrochemical biosensor	AIP-I isolated from S. aureus cultured	10 – 1000 nM	0.5 nM	4 h	Autoinducer peptide	Lubkowicz et al., 2018
	Love wave biosensor	Synthesis	0 – 10 nM	1.86 pM (12.4 pg/mL)	30 min	S. aureusgene sequences	Ji et al., 2020
Bacillus	Electrochemical immune biosensor	B. cereus, Bacillus megaterium, and Bacillus thuringiensis	10⁰ – 10⁷ CFU/mL	10¹ CFU/mL	–	Bacillus	Pal et al., 2007
	Electrochemical biosensor	Synthesis	0.1 fM – 20 fM	0.08 fM	120 min	DNA	Hu et al., 2014
	Single-walled carbon nanotubes-based electrochemical biosensor	B. subtilis KCCM 11316	10² – 10¹⁰ CFU/mL	10² CFU/mL	10 min	B. subtilis	Yoo et al., 2017
Corynebacterium diphtheriae	Array fluorescent biosensor	Human serum	5 – 20 mg/mL	100 fg	–	Human antibodies	Moreno-Bondi et al., 2006
	SPR biosensor	Monoclonal anti–diphtheria IgG sample	0 – 1000 ng/mL	10 ng/mL	1 h	Anti-diphtheria IgG	Zeinoddini et al., 2018
	Electrochemical immune biosensor	Human saliva	10^-⁴ – 10^-¹ Lf/mL	10^-⁴ Lf/mL	–	Diphtheria toxoid	Ziółkowski et al., 2019
Streptococcus	Electrochemical biosensor	Group B Streptococus nucleic acid detection kit	1 fM – 1 nM	0.4 fM	2 h	DNA	Yuan et al., 2016
	Electrochemical immune biosensor	S. agalactiae reference strain	10¹ – 10⁷ CFU/mL	10¹ CFU/mL	90 min	S. agalactiae	Vásquez et al., 2017
	Electrochemical biosensor	Human serum	50 – 5 × 10⁴ CFU/mL	50 CFU/mL	–	S. pneumoniae	Chang et al., 2020
Acinetobacter baumannii	Electrochemical DNA biosensor	Blood or sputum	27.5 – 8.25 × 10⁷ mg/mL	0.825 ng/mL (1.2 fM)	15 min	DNA	Yeh et al., 2010
	Lateral flow biosensor	Sputum	10 ng/uL – 1 fg/uL	100 fg/uL	1 h	DNA	Hu et al., 2019
	Optical DNA biosensor	Synthesis	1 μM – 1 zM	1 fM	–	Oligonucleotide sequences	Bahavarnia et al., 2020
Escherichia coli	Electrochemical biosensor	E. coli O157:H7	10 – 10⁵ CFU/mL	79 CFU/mL	10 min	E. coli O157:H7	Muhammad-Tahir and Alocilja, 2003
	Electrochemical impedance biosensor	E. coli strains ORN 178 and ORN 208	1.2 × 10² – 2.5 × 10³ CFU/mL	120 CFU/mL	–	E. coli	Guo et al., 2012
	FET biosensor	E. coli O157:H7	10 – 10⁴ CFU/mL	10 CFU/mL	100 s	E. coli cells	Chang et al., 2013
	Electrochemical immunesensor	E. coli O157:H7	30 – 3 × 10⁸ CFU/mL	30 CFU/mL	–	E. coli O157:H7	Güner et al., 2017
	Quartz crystal microbalance (QCM) sensor	Stock cultures of E. coli O157:H7	10² – 10⁷ CFU/ml	1.46 × 10³ CFU/mL	50 min	E. coli O157:H7	Yu et al., 2018
	Electrochemical biosensor	Urine	15 – 1.5 × 10⁸ CFU/mL,	1 CFU/mL	140 min	E. coli	Li et al., 2018
	Electrochemical biosensor	E. coli strain ATCC 11303 culture collection	313, 10, and 1 CFU/mL	1 CFU/mL	6 – 8 h	E. coli	Zuser et al., 2019
	Microfluidic colorimetric biosensor	Chicken E. coli O157:H7	50 – 5 × 10⁸ CFU/mL	50 CFU/mL	–	E. coli O157:H7	Zheng et al., 2019
Hemophilus influenzae	Electrochemical biosensor	Culture/urine	0.1 – 2500 nM	0.02 nM	–	Chloramphenicol	Yadav et al., 2014
	Electrochemical DNA biosensor	Synthesis	1 zM – 1 μM	1 zM	50 min	DNA	Mobed et al., 2019b
	Optical DNA biosensor	Synthesized H. influenza sequences	1 μM – 1 zM	1 zM	2 h	DNA	Hassanpour et al., 2020
Legionella pneumophila	Electrochemically biosensor	Synthesis	1 × 10^-¹⁴ – 1 × 10^-⁶ M	2.3 × 10^-¹⁴ M	30 min	DNA	Rai et al., 2012
	Electrochemical DNA biosensor	Synthesis	1 zM – 1 μM	1 zM	20 min	DNA	Mobed et al., 2019a
	Antimicrobial peptide biosensor	L. pneumophila	10³ – 10⁶ CFU/mL	10³ CFU/mL	2 h	L. pneumophila	Islam et al., 2020
Campylobacter jejuni	QCM sensor	Against C. jejuni	10⁴ – 10⁹ CFU/mL	150 CFU/mL		C. jejuni	Masdor et al., 2016
	Fluorescence immunosensor	C. jejuni in poultry liver	10 – 10⁶ CFU/mL	10 CFU/mL	1.5 h	C. jejuni	Dehghani et al., 2020
Salmonella	Electrochemical impedance biosensor	Culture	3 × 10³ – 3 × 10⁶ CFU/mL	3 × 10³ CFU/mL	3 h	Salmonella	Dastider et al., 2015
	Microfluidic nano-biosensoR	Culture/chicken	0 – 10⁶ CFU/mL	10³ CFU/mL	30 min	Salmonella	Kim et al., 2015
	Electrochemical biosensor	Culture/apple juice	10² – 10⁸ CFU/mL	3 CFU/mL	45 min	Salmonella	Sheikhzadeh et al., 2016
	Colorimetric biosensor	Culture/spiked Chicken carcass	10¹ – 10⁴ CFU/mL	11CFU/mL	2.5 h	Salmonella	Wang et al., 2020a
	Electrochemical aptasensor	Culture/spiked Chicken carcass	10² – 10⁶ CFU/mL	80CFU/mL	2 h	Salmonella	Wang et al., 2020b
	Electrochemical biosensor	Milk	1.5 × 10¹ – 1.5 × 10⁴ CFU/mL	150 CFU/mL	30 min	Salmonella	Malvano et al., 2020
Mycobacterium tuberculosis	Electrochemical DNA biosensor	Synthesis	1 pM – 10 nM	0.26 pM	100 s	DNA	Hong et al., 2012
	Electrochemical impedimetric immunosensor	Synthesis	100 fM – 1 nM	100 fM	–	16 kDa HSP	Gopinath et al., 2016
	Multichannel series piezoelectric quartz crystal (MSPQC) sensor	Culture /sputum	1 × 10³ – 1 × 10⁷CFU/mL	10² CFU/mL	70 min	H37Rv	Zhang et al., 2017
	Silicon photonic microring sensor	Sputum	5 fg/uL– 500 pg/uL	3.2 copies	1 h	DNA	Liu et al., 2018c
	MSPQC sensor	Culture /sputum	1 × 10² – 1 × 10⁸CFU/mL	20 CFU/mL	3 h	H37Ra	Zhang et al., 2019a
	Electrochemical Sensor	Culture	10² – 10⁷ CFU/mL	10² CFU/mL	2 h	H37Rv	Zhang et al., 2019b
	Electrochemical sensor	Synthesis	1 fg/mL – 1 ng/mL	0.33 fg/mL	–	Protein	Chen et al., 2019
	SPR biosensor	Sputum	2 – 125 ng/mL	0.63 ng/mL	35 – 40 min	Protein	Peláez et al., 2020

Tab.4

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