[springer series on chemical sensors and biosensors] surface plasmon resonance based sensors volume...

Springer Ser Chem Sens Biosens (2006) 4: 191–206DOI 10.1007/5346_020© Springer-Verlag Berlin Heidelberg 2006Published online: 8 July 2006

SPR Biosensors for Environmental Monitoring

Jakub Dostálek · Jirí Homola (�)

Institute of Radio Engineering and Electronics, Prague, Czech [email protected]

1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 191

2 Organic Contaminants . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1922.1 Pesticides . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1922.2 Polycyclic Aromatic Hydrocarbons . . . . . . . . . . . . . . . . . . . . . . . 1952.3 Polychlorinated Biphenyls . . . . . . . . . . . . . . . . . . . . . . . . . . . 1962.4 Phenolic Contaminants . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1972.5 Dioxins . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1992.6 Trinitrotoluene . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 199

3 Inorganic Contaminants . . . . . . . . . . . . . . . . . . . . . . . . . . . . 200

4 Microbial Pathogens and Toxins . . . . . . . . . . . . . . . . . . . . . . . . 201

5 Summary and Outlook . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 202

References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 205

Keywords Biosensor · Dioxins · Environmental monitoring · Heavy metals ·Inorganic contaminants · Microbial pathogens · Organic contaminants · Pesticides ·Phenols · Polycyclic aromatic hydrocarbons · Polychlorinated biphenyls · Sensor ·Surface plasmon resonance · Toxins

1Introduction

An increasing number of chemical and biological substances are released intothe environment every year as a result of industrial and agricultural activity.Numerous substances have been identified as harmful and subjected to reg-ulatory measures (e.g., polycyclic aromatic hydrocarbons, pesticides, heavymetals, polychlorinated biphenyls, dioxins), risks to human and wildlife or-ganisms of others are still being assessed (e.g., surfactants, pharmaceuticals,and nanoparticles) [1–6]. Harmful substances can be discharged into variousenvironments including air, soil, and water through which they can interferewith human and wildlife organisms as endocrine disrupters, carcinogens, or(geno)toxicants. In order to protect public health and the local ecosystemsfrom the harmful effects of these compounds, efficient tools for their rapiddetection are urgently needed.

192 J. Dostálek · J. Homola

Currently, detection of harmful contaminants is performed using estab-lished analytical techniques, such as gas chromatography (GC), liquid chro-matography (LC) and mass spectrometry (MS) (detection of small organicpollutants [7, 8]), culturing and polymerase chain reaction (PCR) combinedwith DNA arrays (detection of microbial pathogens [9]), and immunoassays(detection of small organic pollutants and microbial pathogens [10, 11]).However, these methods require sophisticated equipment and laborious sam-ple preparation and are therefore performed by highly trained personnel inspecialized laboratories.

Chemical sensors and biosensors for environmental monitoring present aninteresting alternative to these conventional methods and offer numerous at-tractive features such as ease of use, low cost, portability, and the ability toperform detection in the field [12–16]. Optical biosensors based on surfaceplasmon resonance (SPR) show potential for rapid and sensitive detectionof chemical and biological contaminants in the environment. SPR sensorsprovide a generic platform which, in conjunction with appropriate biorecog-nition elements, can be tailored for detection of numerous compounds relatedto environmental protection [17–19].

This chapter reviews applications of SPR biosensors for detection of chem-ical and biological contaminants that present environmental risks, includingorganic chemicals, inorganic chemicals, microbial pathogens, and toxins.

2Organic Contaminants

Organic contaminants that present a concern to environmental protectioninclude pesticides (used in agriculture), polycyclic aromatic hydrocarbons(PAHs, a by-product of incomplete combustion), polychlorinated biphenyls(PCBs, components of coolants and lubricants), phenols (used in the pro-duction of plastics and pesticides), dioxins (unwanted by-products of manyindustrial processes including incineration and chemical manufacturing ofphenols, PCBs, and herbicides) and alkyphenols (surfactants in agrochemi-cals and household cleaning products).

2.1Pesticides

In agriculture, several hundreds of different pesticides have been used world-wide over the last few decades. Owing to their widespread applications andpersistence in the environment, pesticides are accumulating in media such assoil and ground water. Many pesticides exhibit endocrine-disrupting activity,which poses a threat to public health and local ecosystems, and are thereforeregulated. In the European Union, the maximum allowable concentrations in

SPR Biosensors for Environmental Monitoring 193

drinking water for individual pesticides and pesticides in total are 0.1 ng mL–1

and 0.5 ng mL–1, respectively [20]. In the United States, for drinking water theUS Environmental Protection Agency (EPA) sets the maximum allowed con-centrations for the most common pesticides such as atrazine and simazine to3 ng mL–1 and 4 ng mL–1, respectively [21].

As pesticides are rather small molecules (e.g., the molecular weight ofatrazine is 216 Da), their detection is usually performed using the inhibitionassay (see Chap. 7 in this volume [54]). In this type of sensor, the analyzedsample is pre-incubated with an antibody for the targeted analyte. Subse-quently, the mixture is injected into the SPR sensor with an analyte derivativeimmobilized on the sensor surface, and the binding of the unreacted antibodyto the analyte derivative is measured. The presence of the targeted analytein the sample is detected as a decrease of antibody binding to the analytederivative. Figure 1 shows a typical sensorgram and calibration curve for aninhibition assay-based SPR biosensor for detection of pesticides developed atthe Institute of Radio Engineering and Electronics, Prague.

The first SPR immunosensor for detection of pesticides was developed byMinunni et al. [22] in the early 1990s. They used an SPR sensor developed byBiacore AB, Sweden, with the atrazine derivative bound to dextran matrix onthe sensor chip. The detection of atrazine was performed using the inhibitionassay and monoclonal antibodies. The sensor response was subsequently am-plified by secondary antibody, which was bound to the antibody captured bythe atrazine derivative (sandwich assay, see Chap. 7 in this volume [54]). Thisbiosensor was demonstrated to measure atrazine in distilled and tap waterwithin the range 0.05–1 ng mL–1 in 15 min and exhibited relatively low cross-reactivity with simazine and tetrabutyl atrazine (20%). The sensor surfacewas regenerated with 100 mM sodium hydroxide in 20% acetonitrile.

Mouvet et al. developed an integrated optical (IO) SPR sensor forsimazine [23]. A triazine derivative was immobilized on the sensor using the

Fig. 1 Inhibition assay for detection of atrazine: a SPR sensorgram obtained while flowingover the sensor surface aqueous samples with atrazine at the concentrations 0, 0.1, 1, 10,and 100 ng mL–1 incubated with antibody; b calibration curve of the sensor


dextran chemistry. Using inhibition assay this system allowed detection ofsimazine in the range 0.11–1.1 ng mL–1 within 20 min. The sensor surfacewas shown to be regenerable allowing up to 200 detection cycles on a sin-gle chip. The regeneration was performed by the sequential incubation inpepsin (2 mg mL–1) and solution of 50% acetonitrile and 1% proprionic acid.The sensor exhibited relatively high cross reactivity with atrazine and tetra-butyl atrazine (approximately 60%). Detection in natural surface and groundwater samples without any sample preparation other than sample filtrationwas demonstrated. Harris et al. [24] combined this sensor with two types ofantibody receptors (IgG and their Fab fragments) for detection of simazine;calibration curves achieved for these two biorecognition elements are shownin Fig. 2.

Another widely used pesticide, 2-4 dichlorophenoxyacetic acid (2,4-D),was detected with an SPR immunosensor by Gobi et al. [25]. They used in-hibition assay and a sensor chip on which the conjugate of BSA and 2,4-Dderivative was physisorbed. The detection was performed with monoclonalantibodies in phosphate buffer saline (PBS) using a commercial SPR-20instrument (from DKK-TOA, Japan). A detection range of 0.5 ng mL–1 to1 µg mL–1 and a detection time of 20 min were achieved. Regeneration of thesensor for up to 20 detection cycles was performed using pepsin (10 µg mL–1).

Nakamura et al. demonstrated direct detection of herbicides by usinga heavy-subunit-histidine-tagged photosynthesis reaction center (HHisRC)from bacterium Rhodobacter sphaerodies [26] (Fig. 3). They used a Biacore Xinstrument (from Biacore AB, Sweden) and a sensor chip with dextran matrix

Fig. 2 Calibration curve of integrated optical SPR immunosensor for detection of simazineusing inhibition assay and IgG antibodies and Fab fragments [24]


Fig. 3 Sensorgrams obtained from direct atrazine SPR biosensor for atrazine bindingto the heavy-subunit-histidine-tagged photosynthesis reaction center (HHisRC) immobi-lized on the sensor chip; atrazine concentrations 1–100 µg mL–1 [26]

into which HHisRC was immobilized by nickel chelation chemistry. Detectionof atrazine in buffer in the concentration range 1–100 µg mL–1 was demon-strated. Detection time in the order of minutes was achieved.

Chegel et al. reported an SPR biosensor based on displacement of plas-toquione from D1 protein interacting with photosynthesis-inhibiting pesti-cides [27]. They used an SPR biosensor system with angular modulation ofSPR and D1 protein attached to the sensor chip via phisisorption on thiol self-assembled monolayer. When exposed to atrazine, plastoquione was displacedfrom D1 protein producing a change in the SPR signal. This sensor alloweddetection of atrazine within the concentration range 50–5000 ng mL–1.

Detection of atrazine based on specifically expressed mRNA in Sac-charomyces cerevisiae bacteria exposed to atrazine was reported by Limet al. [28]. The cells were brought into contact with the analyzed sample, dis-rupted, and the amount of expressed P450 mRNA was measured using an SPRbiosensor Biacore 2000 (Biacore AB, Sweden) with complementary oligonu-cleotide probes. These probes were biotin-labeled and immobilized on thesensor surface using streptavidin–biotin chemistry. Detection of atrazine inthe range 1 pg mL–1 to 1 µg mL–1 was reported. The analysis, including bacte-ria incubation, disruption, and mRNA detection, was completed in 15 min.

2.2Polycyclic Aromatic Hydrocarbons

Polycyclic aromatic hydrocarbons (PAH) are a group of over 100 differ-ent chemicals that are formed during the incomplete combustion of coal,oil, gas, garbage, or other organic substances and can be found in air, wa-


Fig. 4 Sensorgram obtained for different concentrations of benzo(a)pyrene (BaP) and2-hydroxybiphenyl (HBP) detected in buffer by inhibition assay. Channel 1 and channel 2are modified with BSA–BaP and BSA–HBP conjugates, respectively [29]

ter, and sediments. PAHs are regulated due to their endocrine-disruptingand carcinogenic activity (e.g., US EPA sets a maximum concentration forbenzo[a]pyrene in drinking water at 0.2 ng mL–1 [21]).

A SPR immunosensor for detection of benzo(a)pyrene (BaP) and 2-hydroxy-biphenyl (HBP, metabolite of BaP) by an inhibition assay was reported byGobi et al. and Miura et al. [29–31]. They immobilized BaP and HBP con-jugates of bovine serum albumin (BSA) by physical adsorption on the SPRsensor chip, which was used in a two-channel SPR-20 sensor (DKK, Japan).Using monoclonal antibodies against BaP and HBP, simultaneous detectionof BaP and HBP in buffer was demonstrated with a detection limit as lowas 0.01 ng mL–1 [29]. The detection was performed in 15 min and the sen-sor was regenerated for repeated measurements by using pepsin and a pHchange. The sensor exhibited negligible cross-sensitivity between BaP andHBP (Fig. 4).

2.3Polychlorinated Biphenyls

Polychlorinated biphenyls (PCB) – currently banned compounds – were for-merly used in hydraulic fluids, plasticizers, adhesives, fire retardants, andpesticide extenders. These contaminants are persistent in the environmentand are present in sediments at the bottom of lakes, rivers, and seas. As theyexhibit carcinogenic and endocrine-disrupting activity, they are subject toregulation. For instance, in the United States, the maximum allowed concen-tration of PCBs in drinking water is 0.5 ng mL–1 [21].


Shimomura et al. used a Biacore 2000 SPR sensor instrument (BiacoreAB, Sweden) for detection of PCB 3,3′,4,4′,5-pentachlorobiphenyl [32]. Theyemployed competition assay format and the sensor chip with polyclonal an-tibodies immobilized in the dextran matrix. The sample was mixed witha conjugate of PCB-horseradish peroxidase (HRP) and injected into the sen-sor. The presence of the analyte was detected as a decrease in binding ofPCB–HRP conjugate. The detection was performed in 15 min with a detectionlimit of 2.5 ng mL–1 in buffer. The sensor was demonstrated to be regenerableby 0.1 M hydrochloric acid.

2.4Phenolic Contaminants

Phenolic compounds relevant to environmental protection include bisphe-nol A, nonylhenol, 2,4-dichlorophenol, phenol, hydroquinone, resorcinol,phloroglucinol, and catechol.

Bisphenol A (BPA) is a compound which is currently not regulated, butas it exhibits weak estrogenic properties it is a suspected endocrine dis-rupter [33]. BPA is widely used as a plasticizer in plastics such as polycarbon-ate and epoxy resins and thus it is a concern for water quality. Soh et al. de-veloped an SPR immunosensor based on inhibition assay to detect BPA [34].They used a SPR-20 sensor instrument (DKK, Japan) with the sensor chipmodified with thiol monolayer on which BPA was immobilized through BPAsuccinimidyl ester. Using a monoclonal antibody, detection of BPA in bufferat concentrations as low as 10 ng mL–1 was achieved. Detection time was ap-proximately 30 min and the sensor was demonstrated to be regenerable using0.01 M hydrochloric acid.

Large amounts of polyethoxylated alkyphenol detergents are released intothe environment, where they degrade forming more toxic and dangerouscompounds such as alkyphenols. Alkylphenols are not yet regulated, however,for instance US EPA has recommended a maximum 1-h average concentra-tion (acute criterion) and maximum 4-day average concentration (chroniccriterion) of 27.9 and 5.9 ng mL–1, respectively, for nonylphenol in fresh-water [35]. Recently, Samsonova et al. reported an inhibition assay-basedSPR biosensor for detection of 4-nonylphenol [36]. They used a Biacore Qdevice (from Biacore AB, Sweden) and a sensor chip with dextran ma-trix on which 9-(p-hydroxyphenyl)nonanoic acid was immobilized usingamine coupling chemistry. Using monoclonal antibodies, a detection limitof 2 ng mL–1 in buffer was achieved. The detection was performed in lessthan 3 min including a 30-s regeneration step. The sensor was regeneratedby 100 mM sodium hydroxide in 10% acetonitrile. Furthermore, the sen-sor was applied for detection of 4-nonyphenol in shellfish with a detec-tion limit of 10 ng g–1 (Fig. 5) (time for sample preparation was approxi-mately 1 h).


Fig. 5 Calibration curve for SPR sensor-based detection of 4-nonylphenol in four differentshellfish samples by inhibition assay [36]

2,4-Dichlorophenol is the major dioxin precursor. Currently it is not regu-lated, but it is listed among the drinking water contaminant candidates whichthe US EPA intends to regulate in future [37]. Soh et al. developed an SPRbiosensor for detection of this compound based on a competition assay [38].They used a SPR-20 sensor instrument (DKK, Japan) and the sensor chipwith monoclonal antibodies against 2,4-dichlorophenol immobilized on thesensor surface via gold-binding peptide and protein G. The assay was basedon the competition between the binding of analyte present in a sample andadded conjugate of BSA–2,4-dichlorophenol. Detection of 2,4-dichlorophenolin buffer with a detection limit of 20 ng mL–1 was demonstrated.

Write et al. explored direct detection of various phenolic compounds (phe-nol, hydroquinone, resorcinol, phloroglucinol, and catechol) using an SPRsensor with intensity modulation and synthetic receptors loaded in a polymeror sol-gel layer [39]. Their preliminary experiments, consisting of the detec-tion of phenols in buffer, suggested that detection of phenols at millimolarconcentration levels (∼ 100 µg mL–1) is feasible using this approach.

Detection of phenols based on toxicity measurement was carried out byChio et al. [40]. In their experiments, they used a Multiscope SPR sensor(Optrel, Germany) and Escherichia coli cells immobilized on an SPR sensorchip via synthetic cystein-terminated oligopeptides. When the immobilizedcells were exposed to phenol, a decrease in the SPR signal was observed due


to the damage of the cells. Using this approach, phenol in buffer was detectedat concentrations down to 5 µg mL–1.

2.5Dioxins

Dioxins are released in the environment in emissions from the incinera-tion of municipal refuse and certain chemical wastes and in exhaust fromautomobiles powered by leaded gasoline. Dioxins are highly persistent andaccumulate in the environment. They are highly toxic and exhibit endocrine-disrupting activity. Therefore, they are regulated by authorities, e.g., in theUnited States for the most toxic 2,3,7,8-TCDD the maximum allowed concen-tration in drinking water is 10–4 ng mL–1 [21].

Shimomura et al. developed an SPR biosensor for detection of 2,3,7,8-TCDD [32]. They used a Biacore 2000 instrument (Biacore AB, Sweden) andcompetition assay with monoclonal antibodies against 2,3,7,8-TCDD. The an-tibody was immobilized in the dextran matrix on the sensor chip by aminecoupling chemistry. The sample was mixed with a conjugate of 2,3,7,8-TCDD–horseradish peroxidase (HRP) and injected into the sensor. The assay wascompleted in 15 min. A detection limit of 0.1 ng mL–1 was achieved and thesensor was shown to be regenerable using 0.1 M hydrochloric acid.

2.6Trinitrotoluene

There is a demand for rapid detection of explosives, especially for environ-mental restoration and humanitarian demining. Among these compounds,trinitrotoluene (TNT) has attracted a great deal of attention as a main con-stituent of most of antipersonnel landmines and due to its toxic, mutagenic,and carcinogenic effects.

Strong et al. developed an SPR biosensor for detection of TNT [41]. Theyused a SPREETA sensor (from Texas Instruments, USA) with disposable sen-sor chip coated with BSA–trinitrobenzen conjugate. The detection of TNTwas performed by inhibition assay for TNT concentrations down to 1 µg g–1

for soil samples. The time needed for sample preparation (suspension fol-lowed by centrifugation) and analysis of the liquid supernatant were approxi-mately 10 and 6 min, respectively. The sensor was shown to be regenerableusing a solution with 0.1 M sodium chloride and 0.1% Triton X-100.

Sandakaran et al. reported another SPR immunosensor for TNT. For in-hibition assay-based detection, BSA–2,4,6 trinitrophenol conjugate was an-chored to the sensor surface by physical sorption. The detection was per-formed using the sensor instrument SPR-670 (Nippon Laser and Electronics,Japan). With polyclonal antibodies against BSA–TNP, a detection limit aslow as 0.09 ng mL–1 was achieved in buffer [42]. The sensor exhibited very


low cross-sensitivity to other similar compounds such as 1,4-DNT, 1,3-DNB,2A-4,6-DNT, and 4A-4,6-DNT. The sensor was demonstrated to be regenera-ble and a single detection cycle was performed in 22 min. The regenerationwas performed by pepsin.

3Inorganic Contaminants

Heavy metals belong to the group of harmful inorganic contaminants. Theyare released in the environment from factories and coal-burning power plantsand do not naturally decompose in the environment [43]. Currently, theyare regulated and, for instance, in freshwater US EPA sets maximum al-lowed concentrations for heavy metals such as cadmium (chronic criterion0.15 ng mL–1 [44]), copper (chronic criterion 9 ng mL–1 [45]), nickel (chroniccriterion 52 ng mL–1 [46]) and zinc (chronic criterion 120 ng mL–1 [47]).

Detection of heavy metals was demonstrated by Wu et al. who used a Bi-acore X instrument (Biacore AB, Sweden) with rabbit metallothinein coupledto dextran matrix on the sensor chip [48]. Metallothinein is a protein that canbe found in the cells of many organisms and is known to bind to metals (espe-cially cadmium and zinc). Model experiments in which metallothein was usedas a receptor demonstrated the potential of this sensor to directly detect Cd,Zn, and Ni in buffer at concentrations down to 0.1 µg mL–1.

Another approach to direct detection of Cu2+ ions was reported by Ocket al. [49]. They used a sensor based on attenuated total reflection and an-gular modulation of SPR with squarylium dye (SQ) loaded in a thin polymerlayer as a recognition element. This dye changes its absorption when it in-

Fig. 6 Calibration curve of direct Cu2+ SPR sensor with an SQ dye loaded in a polymerlayer deposited on the surface [49]


teracts with Cu2+ ions. Owing to anomalous dispersion accompanying thisabsorption, enhanced refractive index changes can be observed when SQ dyeis exposed to Cu2+ ions. By tuning the operating wavelength of the SPR sen-sor to the absorption wavelength of the dye, selective detection of Cu2+ in theconcentration range 1×10–12–1×10–4 M (0.063 pg mL–1 to 6.3 µg mL–1) wasdemonstrated (Fig. 6).

4Microbial Pathogens and Toxins

Besides anthropogenic contaminants, other harmful compounds such asbacterial pathogens and toxins can also be found in the environment. Forinstance, bacterial pathogens including Legionella pneumophila, Salmonellatyphimurium, Yersenia enterocolitica and Escherichia coli O157:H7 areknown to be able to outbreak via potable water systems, cooling towers,or heat exchanger systems. These bacteria cause significant threat to pop-ulations as they can cause various illnesses such as Legionnaire’s disease(Legionella pneumophila), gastroenteritis (Salmonella typhimurium) and di-arrhea (Yersinia enterocolitica, Escherichia coli O157:H7). In addition, varioustoxins can be released into the environment from natural sources such as al-gae. Among these, domoic acid (DA, a low molecular weight toxin producedby the marine diatom Pseudonitzshia pungens) is identified as posing a riskto human populations as it can accumulate in edible shellfish and exhibitsneurotoxic effects.

Recently, Oh et al. have developed an SPR immunosensor capable ofsimultaneous detection of Legionella pneumophila, Salmonella typhimurium,Yersinia enterocolitica and Escherichia coli O157:H7 [50, 51]. Monoclonalantibodies against these bacteria were immobilized in individual sensingchannels of the sensor chip of a Multiscope SPR sensor (Optrel, Germany) viaprotein G. For bacteria in buffer, the detection limit of 105 cfu mL–1 and goodspecificity were achieved. No special treatment of bacteria was performed.

Lotierzo et al. developed a photografted molecular imprinted polymer-based SPR sensor for detection of domoic acid [52]. They used a Biacore3000 sensor instrument (Biacore AB, Sweden) and the competition assay. Theconjugate of horseradish peroxidase and DA was added into analyzed sam-ple and the competition of binding of DA and the conjugate to the sensorchip was measured. As follows from the calibration curve (Fig. 7), a detectionlimit as low as 5 ng mL–1 was achieved. Recently, Yu et al. detected DA usinga two-channel sensor based on attenuated total reflection and wavelengthmodulation of SPR [53]. DA was immobilized on the sensor chip by thiolchemistry, and inhibition assay involving monoclonal antibodies was em-ployed. Detection of DA at concentrations as low as 0.1 ng mL–1 was achieved.The sensor was regenerated for up to 20 detection cycles using 50 mM hy-


Fig. 7 Calibration curve of SPR sensor with photografted molecular imprinted polymerand competition assay [52]

droxide solution and demonstrated an ability to maintain its activity evenafter two months of storage.

5Summary and Outlook

In recent years, we have witnessed an increasing research and developmentactivity aiming at introducing SPR biosensor technology to environmentalmonitoring. Numerous substances of environmental concern have been tar-geted and SPR biosensors for their rapid detection at practically relevantconcentrations have been demonstrated (Table 1). However, most of the re-ported biosensors for environmental contaminants have taken advantage ofcommercially available laboratory SPR sensor instruments not suitable for theuse in the field and dealt with rather pure samples (Table 1). In the future,we expect that advances in the development of mobile SPR sensor platforms,immobilization methods, and biorecognition elements will enable rapid de-tection and continuous monitoring of environmental contaminants in thefield and thus substantially contribute to the protection of local ecosystemsand public health.

Acknowledgements This work was supported by grants from the United States Food andDrug Administration (contract FD-U-002250) and the European Commission (contractQLK4-CT-2002-02323).


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