Probing and Quantifying the Food-Borne Pathogens and Toxins: From

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Probing and Quantifying the Food-Borne Pathogens and Toxins: From in vitro to in vivo Jing-Min Liu, Zhi-Hao Wang, Hui Ma, and Shuo Wang J. Agric. Food Chem., Just Accepted Manuscript • DOI: 10.1021/acs.jafc.7b05225 • Publication Date (Web): 17 Jan 2018 Downloaded from http://pubs.acs.org on January 17, 2018

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Journal of Agricultural and Food Chemistry

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Probing and Quantifying the Food-Borne Pathogens and

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Toxins: From in vitro to in vivo

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Jing-Min Liu, Zhi-Hao Wang, Hui Ma, and Shuo Wang*

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Tianjin Key Laboratory of Food Science and Health, School of Medicine,

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Nankai University, Tianjin 300071, China

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*Corresponding author

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(Shuo Wang) Mail to: No.94 Weijin Road, Tianjin, 300071, China.

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Email: [email protected]; Tel: +86-22-85358445

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ABSTRACT

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Development of real-time and in situ analytical methods for determination of

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food-borne pathogens and toxins ingested into human body would be a promising

13

research direction in the food safety area. The present review starts with

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summarization of the up-to-date progress of the nanomaterial-assisted in vitro

15

detection methods for pathogens and toxins, and finally focused on application of

16

animal bioimaging to in vivo study, including prospective strategies for in vivo

17

quantification of target pathogens or toxins and in vivo investigation of their behaviors

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inside the living body, with the assistance of real-time and non-invasive optical

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bioimaging. This review provides the advisory direction for food-safety research,

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from in vitro to in vivo, along with a prospective discussion of the further

21

development roadmap of the food-safety detection techniques, especially the

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bioimaging-guided methods for investigation and mediation of food contamination

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effect to human health.

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KEYWORDS: food-borne toxins, pathogens, in vivo detection, nanomaterials,

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bioimaging

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INTRODUCTION

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In recent years, food safety has become a challenging field and emerged as a major

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threat to public health world-widely, with the increasing demand of minimizing the

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occurrence of food-borne diseases.1 With the globalization of economy, rapid

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movement of people and international trade have increased the risk of food-borne

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diseases, generally caused by the consumption of contaminated food or water.2

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Therein, food contamination could be partly ascribed to the exposure to pathogens

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through water, air, and contact with soil, fertilizer, and the food processing

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environment, from raw material production to final consumption.

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As a global priority, efficient identification and quantification of food-borne

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pathogens and toxins (sterigmatocystin, aflatoxin, ochratoxin, etc.) has come to be a

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general research topic. Great effort has been made on the fabrication of rapid,

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sensitive, and selective analytical methods to quantify harmful substances in food

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products, including the fluorescence sensing, colorimetric detection, electrochemical

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sensing, chromatographic separation, and immunoassays.3 With the increase of

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diversity and complexity of the food-borne toxins, researchers are urged to know the

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specific actions of pathogens and toxins when ingested into the living body. Purely

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quantifying the concentrations or levels of pathogens or toxins in a certain sample

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provides limited information in vivo.

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Development of real-time and in situ analytical methods for sensitive and selective

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determination of food-borne pathogens and toxins ingested into human body would be

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the promising research direction in the food safety area, so as to clarify the harmful 3 ACS Paragon Plus Environment


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action mechanism inside the human body. Real-time and in situ analytical methods

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could not only improve business efficiency owing to the faster release of products

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without waiting for the results of time-consuming tests, but also clarify the harmful

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action mechanism inside the human body through in situ collecting the information of

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pathogen behaviors. Compared with the conventional in vitro detection methods

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mentioned as determination of the target analytes in certain food or biological samples,

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optical imaging technology with real-time monitoring and non-damage detection

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ability appears as the advanced methodology for probing the toxins. Nanophosphors

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with excellent optical property and biocompatibility, such as persistent luminescence

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nanophosphors (PLNPs),4 quantum dots (QDs),5 carbon nanodots (CDs),6 and

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upconversion nanoparticles (UCNPs),7 were introduced as ideal contrast agents for in

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vivo bioimaging and the functional nanoprobes to specific recognition of the target

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pathogens or toxins inside the living body with the assistance of antibody or aptamer.

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Nanomaterial-involved bioimaging would open up a new way for probing the

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food-borne toxins via the involvement of bioimaging, and broaden the methodology

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development for food safety investigation based on the advanced functional

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nanomaterials.

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The present review starts with the up-to-date progress of the nanomaterial-assisted

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in vitro detection methods for food-borne pathogens and toxins, and finally focused

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on application of animal bioimaging to in vivo probing the target pathogens or toxins.

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This review provides the advisory direction for food-safety research, from in vitro to

71

in vivo, along with a prospective discussion of the further development roadmap of 4 ACS Paragon Plus Environment

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the food-safety detection techniques, especially the bioimaging-guided methods for

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investigation and mediation of food contamination effect to human health. (Figure 1)

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IN VITRO DETERMINATION OF FOOD-BORNE PATHOGENS AND TOXINS

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Detection of food-borne pathogens by conventional approaches generally involves

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microorganism identification by morphological evaluation through selective

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enrichment, biochemical analysis, and serological confirmation. Common methods

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for detection of pathogens or toxins are mainly polymerase chain reaction (PCR),

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enzyme

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chromatography (HPLC), mass spectrometry (MS), and morphological and

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biochemical characterization.8, 9 In a typical assay, a simple and specific primer-probe

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system based on a real-time polymerase chain reaction assay was fabricated to detect

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Anisakis simplex parasite in seafood, realizing selective and sensitive determination of

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trace parasite in marine products with a detection limit of 40 ppm.10 Reverse phase

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liquid chromatography coupled to electrospray ionization mass spectrometry (LC–

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ESI/MS) was applied to identify and quantify enterotoxins A and B from complex

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food samples with achieved detection limit of 0.5 g and 0.2 g, respectively.11

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Combination of intact cell immune-capture with liquid chromatography−tandem mass

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spectrometry has been proved to be effective for detecting Yersinia pestis in milk

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samples, of which the sensitivity was better than that of ELISA analysis.12

linked

immunosorbent

assay

(ELISA),

high

performance

liquid

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Although the above conventional analytical methods have been extensively studied

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and widely applied in food-safety inspection, these classical analytical approaches, to

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some extent, were limited by the insufficient sensitivity and reproducibility, 5 ACS Paragon Plus Environment


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time-consuming steps, the requirements of highly qualified staff and complex

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operation, and huge economic investment. In recent years, functional nanomaterials

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with submicron-sized dimensions and unique physiochemical properties have opened

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up new horizons for food safety inspection and generated a large number of detection

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methods with improved analytical performance.9, 13 The functional nanomaterials for

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the detection of food contamination are at the heart of the effective sensing in terms of

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signal-readout because they impact the sensitivity of quantification, recognition

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selectivity and specificity, simplicity and speed, as well as overall quality and

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robustness of the detection performance.

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QDs are typical small semiconductor particles with size ranging from 2 to 10 nm

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that can emit light ranging from ultraviolet to infrared.14 Quantum confinement effect

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originated from the nanometer size has endowed QDs with outstanding electro-optical

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properties, such as high quantum yields, long fluorescence lifetimes, large extinction

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coefficients, broad absorption spectrum, narrow and symmetric size-tunable emission,

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pronounced photostability, and strong resistance to photobleaching, all of which make

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them advantageous over the traditional fluorophores for sensing applications.15

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Upconversion nanoparticles are tunable optical luminescence nanomaterials, which

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have many advantages over the traditional organic fluorophores, such as narrow

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emission bandwidths and large anti-Stokes shifts.16 The UCNPs also provides an

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antidote for the background effects of autofluorescence and light scattering, thereby

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greatly improving the signal-to-background ratio and sensitivity of detection.17 There

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is no obvious intensity loss in the long-term monitoring of the optical stability of 6 ACS Paragon Plus Environment

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UCNP-labeled targets, and low toxicity in vitro and in vivo makes them suitable for

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bio-applications.

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Plasmonic metal nanomaterials (PMNMs), typically gold nanoparticles (AuNPs)

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and silver nanoparticles (AgNPs), have particular physical and chemical properties as

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well as good biocompatibility. The most distinctive feature of PMNMs is localized

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surface plasmon resonance (SPR), arising from the resonant oscillation of their free

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electrons in the presence of light with a particular frequency.18 Due to their sensitive

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spectral response to the local environment of nanoparticle surface and high density of

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electromagnetic filed, PMNMs have great potential for the fabrication of sensing

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platform, especially via the colorimetric and surface enhanced raman scattering

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(SERS) methodology.19

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Persistent luminescence nanophosphors are born with distinctive features, such as

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long-lasting afterglow, low toxicity, and excellent biocompatibility, of which, most

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importantly, the super-long persistent luminescence enable the PLNPs applied for

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time-resolved fluorescence sensing in vitro as well as real-time bioimaging in vivo

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without requiring any external simultaneous excitation of light sources.20, 21 Therefore,

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PLNPs have attracted great attention as unique optical nanoprobes and opened up a

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new research direction in the field of biological and biomedical research.

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The above advanced functional nanomaterials can be combined with suitable

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analytical methodologies and detection techniques to generate various advanced

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analytical methods for food-borne pathogen and toxin detection. The emerging

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nanomaterial-involved food-safety inspection methods include: sensitive and selective 7 ACS Paragon Plus Environment


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fluorescence sensing utilizing quantum dots (high quantum yields, narrow and

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symmetric size-tunable emission, pronounced photostability) and upconversion

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nanoparticles (high signal-to-background ratio and sensitivity due to large anti-Stokes

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shifts ),22,

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nanomaterials (localized surface plasmon resonance effect),24 and highly sensitive and

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in situ SERS methods using plasmonic metal nanomaterials,25 etc.

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simple and rapid colorimetric detection using plasmonic metal

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As the continuous increasing of food sample complexity and food contamination

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variety, there are great demands for further development of analytical methods with

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improvement on rapidness, sensitivity, specificity, robustness, and cost-effectiveness.

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As for the rapidness, the conventional culture-based methods always involve cell

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proliferation steps, which are usually carried out in laboratory conditions overnight.

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The prolonged period to obtain results reflects cost-ineffectiveness and inconvenience,

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especially for the food sample analysis that required high throughput and rapidness.

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While integrated with advanced functional nanomaterials, nanosensing techniques

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have demonstrated fast detection ability, and the target analytes can be detected within

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minutes to hours without the need of bacterial culture and concentrating. As fast and

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efficient detection of food-borne pathogens or toxins tends to be more practical that

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could better satisfy the need of current customers and market, future effort would be

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guided into generating portable, miniaturized, and high-throughput detection methods

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or devices.

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As for the sensitivity, because food-borne pathogens and toxins usually have a low

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infectious dose and high health risk, detection methods possessing extremely low 8 ACS Paragon Plus Environment

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detection limit along with good reproducibility are always popular in food-safety

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inspection. The use of nanoparticles will help to detect food-borne pathogens rapidly

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and accurately with a low detection limit. Plasmonic nanoparticle-assisted SERS

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detection is able to achieve extremely low detection limit, even to single molecule,

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and the sensitivity could be further improved via involvement of nano-composite

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materials.25-28 Nano-adsorbent based solid phase extraction coupled with optical or

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chromatographic detection is another effective method to obtain high sensitivity. Due

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to the high surface area of nanomaterials, like graphene,29 carbon nanotubes,30 and

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nano-MOFs (metal-organic frameworks),31 selective preconcentration of target

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analytes from complex food sample matrix was realizable and highly sensitive

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detection of food-borne pathogens or toxins was achieved. Besides, incorporating

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functional nanomaterials into the electrode or onto the electrode surface generated the

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highly-performed

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Nanomaterial modification would increase the surface area of electrode, in turn

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improve conjugation and catalyze redox reactions, which eventually improve the

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electric catalytic performance and sensitivity.

electrochemical

methods

for

food-safety

inspection.32-35

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As for the specificity, immunoassay based on specific antibody-antigen reaction is

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very popular in biosensing, including drugs, hormones, proteins and microorganisms.

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The basic principle is that soluble antigens and corresponding antibodies interact with

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each other, forming insoluble antigen-antibody complex precipitation. Immunoassay

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have been developed to detect food-borne toxins with fluorescence immunoassay,

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enzyme-linked immunosorbent assays, and magnetic bead-based ELISAs.36 9 ACS Paragon Plus Environment


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In addition to the antibody, aptamer has come to be an alternative specific probe,

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widely used in the nanosensing platforms for food-safety inspection. Aptamers are

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typical single stranded DNA or RNA molecules with high affinity and selectivity to

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bind targets.37 Unlike the complementary sequence base pairs, the high affinity of

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aptamers is related to the specific folding under the binding condition. Aptamers are

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short oligonucleotides generally less than or equal to 10 kDa, selected for various

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molecular ions, amino acids, proteins, virus and the pathogenic bacteria, plant or

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animal cells.38 Due to high selectivity, affinity and stability, aptamers have been

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utilized as effective recognition probe for fabrication of various sensing assays for

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food safety inspection.

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As for the robustness and cost-effectiveness, effort could be focused on the further

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integration of nanostructures via one-pot preparation or green synthesis, like the

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carbon nanomaterials (low cost and toxicity of the raw materials, green synthesis).

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Besides, rapid detection assay based on the well-performed nanomaterials always

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gives good reproducibility and repeatability to further improve the robustness of the

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methodology.

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IN VIVO PROBING FOOD-BORNE PATHOGENS AND TOXINS

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In the past few decades, huge effort has been made on the research and development

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of in vitro identification and quantification of various food-borne pathogens and

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toxins, with continuous progress on the improved accuracy, sensitivity, selectivity, and

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speed. However, as the increase of diversity and complexity of the food-borne toxins,

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people are urged to know the specific actions of pathogens and toxins when ingested 10 ACS Paragon Plus Environment

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into the living body, not limited to purely quantifying the pathogens or toxins in a

205

certain sample. Therefore, development of real-time and in situ analytical methods for

206

sensitive and selective determination of food-borne pathogens and toxins ingested into

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human body would be the promising research direction in the food safety area.

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Real-time and in situ analytical methods could provide more intuitive information in

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vivo, in favor of clarifying the harmful action mechanism inside the human body and

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generating guideline for prevention and therapy of disease.

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Optical bioimaging technology, especially in vivo fluorescence imaging, have made

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tremendous advance in serving as the noninvasive and nonionizing tool for highly

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sensitive and real-time probing the life process inside the living body.39 In principle,

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bioimaging techniques are realized by equipment of a sensitive camera and

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appropriate filters to collect fluorescence emitted from the whole-body of living small

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animals. With the assistance of imaging contrast agents, the well-established

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fluorescence bioimaging is capable of visualizing biology in its intact and native

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physiological state, widely applied in cancer diagnosis and human disease treatment.

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However, there still existed some problems that hampered fluorescence bioimaging in

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terms of the tissue penetration depth and signal-readout resolution, caused by the high

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absorption, scattering, and intrinsic fluorescence by bio-entities or living tissues

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almost across the whole electromagnetic spectrum.40 To overcome these limitations,

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research efforts have been focused on development of advanced luminescent

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nanomaterials as efficient contrast agents, named as nano-imaging methodology.41

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Various nanophosphors with respective advantageous property have been introduced 11 ACS Paragon Plus Environment


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as nanoprobes for in vivo nano-imaging, of which the most attractive nanophosphors

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are QDs (high quantum yields, intense and tunable emission, ease of surface

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modification, etc.), carbon nanodots (low toxicity, green synthesis, high stability, good

229

biocompatibility, etc.), UCNPs (anti-Stokes and NIR-activable luminescence, narrow

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and intense emission, long lifetimes, low toxicity, superior photostability, etc.), and

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PLNPs (super-long afterglow, in vitro excitation allowable and in vivo re-excitable

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luminescence, superior structural stability and biocompatibility, low toxicity, ease of

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surface functionalization, etc.). All these nanophosphors have been extensively

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applied in in vivo bioimaging, including tumor targeting, molecule tracking, and drug

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delivery.4, 42-45 In a typical assay, a multi-functional core-shell nanostructure, which

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utilized Mn4+ and Ge4+ co-doped gadolinium aluminate PLNPs as the NIR

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luminescence center and employed the gold nanoshell to enhance the luminescence,

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was proposed for highly sensitive bioimaging of animal tumor, with excellent

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biocompatibility and improved resolution.4 Based on above, it is expectable that

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nanophosphor-assisted bioimaging with non-damage detection ability and real-time

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monitoring holds great potential for in vivo probing the target pathogens or toxins

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inside the living body, which would surely provide more reliable and in situ

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information of in vivo actions and distributions of food-borne harmful substance.

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The real-time and in situ bioimaging could be introduced to food-safety inspection,

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including in vivo quantification of the target pathogens and toxins inside the living

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body, probing their behaviors and distribution in vivo to further investigate the

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pathogenesis, and bioimaging-guided drug-delivery to target infarction site for therapy. 12 ACS Paragon Plus Environment

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As there have been few examples of utilization of bioimaging for in vivo probing the

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toxins or pathogens, herein we present several prospective research protocols of

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bioimaging-assisted food-safety inspection, which are believed to be universal for

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various food-borne pathogens or toxins investigation.

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First, for in vivo quantification of the target food-borne pathogens or toxins,

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fluorescence resonance energy transfer (FRET)-based fluorescence on-off switch that

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involving luminescent NPs as emission center and adsorption structure as quencher

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can be well-established. FRET is a typical non-radioactive process with the energy

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transferring from the fluorescent donor to the acceptor in a way of intermolecular

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dipole-dipole coupling, which only happens when the intermolecular distance in

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between is less than 10 nm and the overlap of emission spectrum of donor and

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absorption spectrum of acceptor is over 30%.46 In FRET-based fluorescence on-off

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switch, the energy acceptors (AuNPs, AuNRs, CuS, graphene, etc.) and donors (QDs,

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UCNPs, PLNPs, etc.) are brought to an appropriate distance exclusively through the

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specific recognition (antigen-antibody, DNA hybridization, biotin-avidin, etc.), then

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the fluorescence are quenched accordingly. Presence of target analytes would separate

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the emitter and quencher, and the FRET is inhibited to recover the fluorescence,

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through which process the target analytes are determined. This FRET-based

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fluorescence switch could be easily utilized in activable-bioimaging of target

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pathogens or toxins in vivo. (Figure 2)

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Second,

for in vivo probing

the

behaviors

of food-borne

pathogens,

nanophosphor-labelling would be an effective way. In the previous proof-of-concept 13 ACS Paragon Plus Environment


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study, Cr3+-doped zinc gallogermanate (ZGGO) PLNPs with ultra-brightness, super

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long afterglow, excellent biocompatibility, and low toxicity, was employed as targeted

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contrast agents and optical nanoprobes for selective tagging the food probiotics,

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Lactobacillus.42 Surface modification of PLNPs with antibody (Anti-Gram positive

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bacteria LTA (lipoteichoic acid) antibody) ensured the success of in vitro labeling the

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probiotics to form the PLNPs-probiotics conjugates, then treated with mice via oral

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administration. The in vitro excitation of PLNPs ensured the highly sensitive and

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long-term bioimaging in the living tissues, which eventually realized the tracing and

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behavior monitoring of labeled bacteria inside the living body and probing the

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bio-distribution in the gastrointestinal tract. The same procedure and methodology

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could be applied for study of pathogens as well, through which the in vivo probing the

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behaviors and tracking the distribution of pathogens would be achievable. (Figure 3)

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Third, for bioimaging-guided in vivo drug-delivery to target pathogens and

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infarction sites, nanophosphors integrated with specific layers that possess large

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surface area (mesoporous silica, TiO2, metal-organic frameworks, covalent-organic

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frameworks, carbon nanotubes, etc.) acted as the core-shell nanocarriers.

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Nanophosphors were utilized as the emission core that provided the luminescence for

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signal-readout during imaging, while drugs are loaded onto the nanocarrier surface via

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interaction with the functional layers. Nanoimaging-guided in vivo drug delivery are

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usually capable of effectively reducing the drug dosage, avoiding the possible damage

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to normal tissues, and increase the precision of therapy. More importantly, it is

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monitorable and controllable. (Figure 4) 14 ACS Paragon Plus Environment

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Taken together, in vivo probing methodology is believed to be the next-generation

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research roadmap for food-safety inspection and food science development, illustrated

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by the above three possible strategies for in vivo quantification of target pathogens or

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toxins and in vivo investigation of their behaviors inside the living body, with the

296

assistance of real-time and non-invasive optical bioimaging. The bioimaging-guided

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in vivo probing the target food-borne pathogens or toxins holds the great potential as

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the innovative methodology to clarify the harmful action mechanism inside the human

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body and reveal the scientific relationship between food science and human health,

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with the final goal of further promoting the development of prevention and therapy of

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food-borne diseases.

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ACKNOWLEDGMENTS

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This work was supported by Beijing Municipal Science and Technology Project

304

(No.Z171100004517013), State Key Program of National Natural Science Foundation

305

of China (No.31430068), and National Key Research and Development Program of

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China (No.2016YFD0401202).

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CONFLICT OF INTEREST

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The authors declare no competing financial interests.

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Figure 1. Schematic illustration of advanced nanomaterial-assisted analytical methods for

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food contamination: from in vitro detection to in vivo probing.

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Figure 2. Schematic illustration of FRET-based fluorescence on-off switch that involves

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luminescence NPs as emission center and adsorption structure as quencher for in vivo

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detection of food-borne pathogens or toxins.

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Figure 3. Schematic illustration of in vivo probing the behaviors and tracking the

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distribution of pathogens based on nanophosphor-tagging and fluorescence bioimaging.

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Figure 4. Schematic illustration of bioimaging-guided in vivo drug-delivery to target

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pathogens and infarction site for therapy.

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TOC Graphic

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Prospective of further development roadmap of food-safety research, from in vitro to

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in vivo, especially the bioimaging-guided method for investigation and mediation of

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food contamination effect to human health.


Probing and Quantifying the Food-Borne Pathogens and Toxins: From

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