\r\n\tmolecular and imaging methods for detection and identification of plant diseases have many limitations that will be discussed in this book. This sparked interest in the development of minimally invasive and substrate general spectroscopic
\r\n\ttechniques that can be used directly in the field for confirmatory plant disease diagnostics.
\r\n\tThis book will also discuss recent progress in development of reflectance, infrared, Raman and surface-enhanced Raman
\r\n\tspectroscopy for detection and identification of plant diseases. It will also present advantages and disadvantages of these optical spectroscopy methods compared to the most common molecular and imaging techniques.
\r\n\tThe book also aims to discuss specific plant diseases, their symptoms and available methods of treatment.
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Venkateswarlu",coverURL:"https://cdn.intechopen.com/books/images_new/371.jpg",editedByType:"Edited by",editors:[{id:"58592",title:"Dr.",name:"Arun",surname:"Shanker",slug:"arun-shanker",fullName:"Arun Shanker"}],productType:{id:"1",chapterContentType:"chapter",authoredCaption:"Edited by"}},{type:"book",id:"878",title:"Phytochemicals",subtitle:"A Global Perspective of Their Role in Nutrition and Health",isOpenForSubmission:!1,hash:"ec77671f63975ef2d16192897deb6835",slug:"phytochemicals-a-global-perspective-of-their-role-in-nutrition-and-health",bookSignature:"Venketeshwer Rao",coverURL:"https://cdn.intechopen.com/books/images_new/878.jpg",editedByType:"Edited by",editors:[{id:"82663",title:"Dr.",name:"Venketeshwer",surname:"Rao",slug:"venketeshwer-rao",fullName:"Venketeshwer Rao"}],productType:{id:"1",chapterContentType:"chapter",authoredCaption:"Edited by"}}]},chapter:{item:{type:"chapter",id:"17823",title:"The Use of Magnetoencephalography to Evaluate Febrile Seizures and Epilepsy in Children",doi:"10.5772/18676",slug:"the-use-of-magnetoencephalography-to-evaluate-febrile-seizures-and-epilepsy-in-children",body:'The International League Against Epilepsy (ILAE) defined the febrile seizures as seizures occurring in childhood after one month of age, associated with a febrile illness not caused by an infection of the central nervous system, without previous neonatal seizures or a previous unprovoked seizure and not meeting the criteria for other acute symptomatic seizure (Østergaard, 2009). There is no evidence that electroencephalography (EEG) abnormalities help in the prediction of the development of subsequent epilepsy and are of limited value (American Academy of Pediatrics, 1996). Computed tomography (CT) and magnetic resonance imaging (MRI) is not indicated in children with simple febrile seizures, but may be useful in cases with prolonged or focal febrile seizures in order to reveal subtle underlying neurological diseases (Shinnar and Glauser, 2002).
The neuromagnetic field recordable outside of the head is a selective reflection of intracellular currents flowing in the apical dendrites of pyramidal cells parallel to the skull surface. The magnetic field generated by a single neuron is almost negligible. When several thousands of nearby cells are synchronously active, the summated extracranial magnetic field typically achieves a magnitude of a few hundred femto-Tesla (1fT=10-15) where the strongest neuromagnetic signals like those associated with epileptic spikes are a few thousands femto-Tesla (Rose et al., 1987,\n\t\t\t\tAnninos et al., 1987; 1989a,b; 1991;1997;\n\t\t\t\t2000a-c; 2003;\n\t\t\t\t2010;Anastasiadis et al., 1997, Kotini et al., 2007a-c). The magnetic activity of the brain is produced by cellular micro-currents, which emerge from ionic movements, due to the dynamical variations of the membrane potentials (Anninos and Raman, 1975; Anninos 1973).
The SQUID (Superconductive Quantum Interference Device) has the ability to detect magnetic fields of the order of 10-12T which are much smaller than the magnetic fields of the earth which are 5X10 -5 T. The SQUID is based on the Josephson effect of superconductivity (Josephson, 1962). Using multi-channel recordings the topography of the magnetic field can be recorded above the scalp with a temporal resolution of less than one millisecond (Braun, 2007). The signal measured by each channel of the SQUID is a time varying waveform voltage that reflects local changes in the magnetic flux as a function of time. This signal is called magnetoencephalography (MEG) if we measured the brain emitted magnetic fields and it is very similar to the EEG if we measured the brain emitted electric fields. MEG is a non-invasive method for the study of electro-magnetic brain activity.
The major advantage of MEG over EEG, is that MEG has higher localization accuracy. This is due to the fact, that the different structures of the head influence the magnetic fields less than the volume current flow, that causes the EEG. MEG provides a high spatial density of recording points, which is difficult to obtain with EEG. The magnetic fields, are less distorted than electrical fields, because of the blurring effect of the skull, which acts as a low-pass filter for electrical potentials, providing, in this way, better conditions for the recording of fast activity. Moreover, inaccuracies in estimating the conductivities of the skull and other tissues of the head affect much more the interpretation of electrical than magnetic sources (Sobel et al., 2000;\n\t\t\t\tWilson et al. 2007; Ramantani et al.,2006;\n\t\t\t\tRamachandranNai et al., 2007; Anninos et al., 2010; Kylliäinen et al.,2006; Elger et al., 1989).
The MEG offers functional mapping information and measurement of brain activity in real time, unlike CT, MRI and functional magnetic resonance imaging (fMRI) which provide anatomical, structural and metabolic information. With the MEG the brain is seen in‘action’ rather than viewed as a still image. Finally, the MEG has far more superior ability to resolve millisecond temporal activity associated with the processing of information which is the main task of the brain. Thus, both normal spontaneous rhythms and pathological activities are readily identified in MEG waveforms as we do with the EEG waveforms. Whereas, MEG signals reflect current flow in the apical dentrites of pyramidal cells oriented tangential to the skull surface, EEG signals reflect both tangential and radial activities (Williamson and Kaufman, 1987; Cohen D and Cuffin, 1991; Lopes da Silva and Van Rotterdam,1987;\n\t\t\t\tRose and Ducla-Soares, 1990; Hamalainen, 1993; Makela, 1996). For all of the above reasons we preferred the use of MEG for the evaluation of seizures.
In this study we investigated the possibility of any epileptic behavior caused by febrile seizures in 4 young sisters, by means of MEG. We utilized MEG to measure epileptic behavior because EEG abnormalities were not useful for the prediction of the development of subsequent epilepsy.
Four young sisters within the age range of 2 - 5 years were referred to our Lab by the Pediatric Department of our University General Hospital in order to be examined with MEG. There were no EEG, CT and MRI examinations in the patients’ records. Informed consent for the methodology and the aim of the study was obtained from their parents prior to the procedure.
The MEG recordings were carried out in a magnetically shielded room with a whole head 122-channel-biomagnetometer (Neuromag-122, Helsinki, Finland) (Anninos et al., 2010; Kotini et al., 2010; 2008; 2005;2004;\n\t\t\t\t2002; Tonoike et al., 1998; Antoniou et al., 2004) (Figure 1). All studies performed precisely 10 days after fever subsided for the purpose of comparison. The time duration of each MEG measurement was 3 min.
There was adequate head coverage for all children by the whole head helmet-shaped dewar. The MEG sensors were adjacent to the scalps. The sensors were consisted of rectangular pairs of planar-type gradiometers aligned in a helmet-shaped dewar vessel, into which the patient’s head was inserted during the measurement. The pick-up-coils of the device are shaped like figure-of-eights to make them ‘near-sighted’, i.e. sensitive to sources in the brain, but insensitive to ambient noise fields. The device employs planar gradiometers that record at each of the 61 measurement sites the magnetic field component normal to the helmet-shaped dewar bottom surface.
The 122-channel-biomagnetometer
All MEG data were inspected carefully off-line for movement artifacts which were cut off from the data trace. The data were bandpass filtered between 0.03 and 130 Hz and sampled at 400 Hz. During off-line data analysis, we used a low-pass filter at 40 Hz and high-pass at 2-8 Hz to extract the spike component from the slower background activity.
When a clear dipole pattern was seen in the magnetic field distribution around the spike peak, the single equivalent current dipole (ECD) model was fitted in the patient’s spherical head model to the recorded signals. We defined acceptable ECDs as those with a goodness-of-fit to the model of >80% and with ECD strength between 100 and 400 nAm (nano Ampere metre).
For the transformation of the ECD locations, the following coordinate system was used: x-axis perpendicular to the other two axes through the anterior commissure, y-axis passing through the anterior and posterior commissure, and z-axis perpendicular to the y-axis through the anterior commissure at the middle plane of the brain.
Normal subjects of similar age who served as controls didn’t show ECDs in their MEGs because normal controls did not have any spike activity on which to fit the data. The same sort of analyses was performed on the normal control data.
Table 1 exhibits the clinical characteristics of each child. After the MEG signals were recorded, an ECD model was estimated at each time point, within the encompassing signal segment, using a single dipole model.
Two out of the 4 children shown ECD dipoles located at the right - temporal areas (Figs.2,3, child No 1,3), as active regions responsible for febrile seizures. These children were scheduled for future clinical examination with EEG due to the high number of events of febrile seizures (Table 1).
The children had a family history of febrile seizures. Their uncle (fathers’ brother) had one event of febrile seizures and occurrence of epilepsy seizures during his life.
Figures 4, 5 exhibit the scalp MEG distribution for the children No.3,4 respectively. There are no ECD dipoles.
The clinical characteristics of each child. F: Female; N: Normal, ECD: Equivalent Current Dipole
The most prevalent pathology following febrile seizures is a recurrence, which occurs in about one-third of the cases. The most reliable risk factors for the reappearance reported are the onset of first febrile seizures at less than 18 months of age and the family history of febrile seizures. Two other specific risk factors for reappearance are the peak temperature and the duration of the fever period prior to the seizure. The higher the peak temperature, the lower is the risk of recurrence and, the shorter the fever period before seizure, the higher
The scalp MEG distribution and the ECD dipole indicated by the arrow in the child No.1 (Table 1). The coordinates are : x (left/right), y (anterior/posterior), and z (superior/inferior)
is the risk for recurrence. Furthermore fearing new seizures, the parents are faced with a concern of their child\'s chance of developing epilepsy or mental retardation (Østergaard, 2009; Berg et al., 1997).
There are only three reports in the literature investigating febrile seizures with MEG. Mayanagi et al. (1996) studied the clinical features of mesial temporal lobe epilepsy in 24 cases. A history of febrile convulsion, particularly in the form of status epilepticus, seemed to be a prognostic factor. For presurgical evaluation, EEG, MRI, MEG and single photon emission computed tomography (SPECT) were important tests.
Mohamed et al. (2007) referred to a previously healthy 10-year-old boy who developed generalized convulsive status epilepticus following a mild febrile illness. Ictal and interictal MEG demonstrated dipole sources projecting from the right mesial temporal region.
The scalp MEG distribution and the ECD dipole indicated by the arrow in the child No.3 (Table 1). The coordinates are : x (left/right), y (anterior/posterior), and z (superior/inferior)
Diffusion-weighted imaging showed restricted diffusion involving the right hippocampus. Right anterior temporal lobectomy resulted in cessation of status epilepticus.
Anninos et al. (2010) studied 15 children within the age range of 2 - 7 years who experienced febrile seizures. Eight children showed ECDs located at the left-temporal, right-temporal, occipital, and frontal lobe, as active regions responsible for febrile seizures. They assumed that the interictal epileptiform discharges are a consequence of febrile seizures.
The most simple and widely used model that can explain a certain MEG surface map is the ECD, which assumes that the magnetic fields recorded at the surface can be accounted by a dipolar source. This model arises from the physiological observation that the main neuronal sources of MEG activity consist of palisades of cortical pyramidal cells, with elongated apical dendrites oriented perpendicularly to the cortical surface. The estimation of a dipole model is reasonable only if the magnetic field on the surface has focal characteristics(Sobel et al., 2000; Ramachandran et al. 2007;\n\t\t\t\tRamantani et al., 2006; Wilson et al., 2007;\n\t\t\t
The scalp MEG distribution in the child No2 (Table 1). The coordinates are : x (left/right), y (anterior/posterior), and z (superior/inferior)
Scheler et al. 2007; Papanicolaou et al., 2006;\n\t\t\t\tWu et al., 2006;Chuang et al., 2006). This model allows characterization of the source of neuronal activity in the brain and is useful in focal epilepsies, in which small areas of brain tissue trigger the seizure and are important in obtaining a good spatiotemporal localization of the foci. However, MEG might be helpful in more complex epileptic patterns (generalized epilepsy).
We defined acceptable ECDs as those with a goodness of fit to the model of >80%. Standard ECD analysis defines the spatial extent of an epileptogenic zone when reliable ECD localizations are gathered to form a single cluster (Oishi et al., 2006;\n\t\t\t\tIida et al.,2005). One single cluster of MEG spike sources can indicate the primary epileptogenic zone for complete resection and seizure control. Multiple clusters indicate complex and extensive epileptogenic zones and necessitate intracranial EEG monitoring. MEG is a technique for measuring the magnetic fields associated mainly with intracellular currents, while the EEG measures mainly extracellular field potentials. Intracellular currents are well modeled by the ECD model.
The scalp MEG distribution in the child No.4 (Table 1). The coordinates are : x (left/right), y (anterior/posterior), and z (superior/inferior)
In our study, 2 out of 4 children were positive to ECDs, whereas the rest were negative. This fact depends on the activity of the patients’ brain during the MEG measurements. If exhibits epileptic behavior, then we will observe ECDs, otherwise we would not. Neuroimaging studies are not necessary in children with simple febrile seizures. EEG\'s have been found to have limited value( Jones and Jacobsen, 2007). Abnormalities on EEG do not predict the occurrence of future seizures or the subsequent development of epilepsy. (Kuturec et al., 1997; Joshi et al., 2005). It is well known that EEG is an unhelpful diagnostic procedure and we use it only when we want to distinguish “febrile convulsions” from convulsions with fever (Panayiotopoulos, 2002; Püst, 2004;\n\t\t\t\tChung et al., 2006).
Time domain analysis of neuromagnetic data give information about the underlying neuronal generators and especially is appropriate for transient behavior. The utility of the ECD algorithm depends on the goodness of fit between the structure of the sources in the model and the neuronal sources. Frequency domain localization of ECD sources is useful if the underlying neuronal generators are differentiated harmonic content and spatial distribution. The existence of such sources has been demonstrated by the determination of ECD components of activity with both a sharp spectral peak and localized source volume. Both frequency and time domain analysis may be applied to the same epoch of time. The coincident occurrence of spike activity localization in the time domain and slow activity localization in the frequency domain may be an interesting tool for localization of epileptic activity. The separation of a complex set of sources underlying spontaneous activity into distinct components is an initial step in determining the functional significance of spontaneous activity
Children with febrile seizures have a six-fold excess (3%) of subsequent afebrile seizures and epilepsy than controls. The risk is 2% after a simple and 5-10% after a complex febrile seizure. We tried to find a method that can supply us some prognostic indicators for possible epileptic behavior in children who experienced febrile seizures and have a family history of them. We assume that one of these prognostic indicators might be the existence of epileptiform discharges modeled by ECDs. Of course, further investigation is needed in order to assess the exact role of the ECDs and the occurrence of epilepsy in young children with a family history of febrile seizures.
(ILAE) International League Against Epilepsy
(EEG) Electroencephalography
(CT) Computed tomography
(MRI) Magnetic resonance imaging
(SQUID) Superconductive Quantum Interference Device
(MEG) Magnetoencephalography
(fMRI) Functional magnetic resonance imaging
(SPECT) Single photon emission computed tomography
(ECD) Equivalent current dipole
The primary function of the lungs is the exchange of gas occurring at the level of alveoli, which are arranged as acini in the lung parenchyma. There is strong need to understand the mechanisms of alveolar maintenance and repair because damage to this region underlies many chronic adult lung diseases, such as chronic obstructive pulmonary disease, idiopathic pulmonary fibrosis, acute respiratory failure in pneumonia, and acute respiratory distress syndrome. Additionally, insufficient development of alveoli results in various neonatal and childhood diseases including bronchopulmonary dysplasia [1]. Despite the pivotal role of the alveoli in the development of lung diseases, the pathogenesis of these various conditions is still largely unknown, and treatment options for patients remain limited.
There is clear evidence that environmental exposures and genetic predisposition contribute to the pathogenesis of idiopathic pulmonary fibrosis (IPF). IPF is defined as a specific form of progressive chronic fibrotic interstitial pneumonia, that is occurring mainly in older adults, and is limited to the lungs [2]. IPF remains relatively rare, with an estimated incidence of roughly 10 cases per 100,000 person-years. Nonetheless, IPF is a lethal lung disorder with a predicted survival of 3–6 years from the onset of symptoms. Most of the deaths among patients with IPF are due to respiratory failure or complicating comorbidities [3]. The pathogenesis of IPF is characterized by continuous insults or micro-lesions to the alveolar epithelium, which result in abnormal activation of both epithelial cells and fibroblasts. Finally, there is an alteration in the deposition of collagen, which contributes to the irreversible fibrosis typical of the disease [4]. Various risk factors have been identified in the development of IPF, that can be divided between intrinsic and extrinsic [5]. Intrinsic risk factors include genetics, aging, sex, lung microbiome [6, 7, 8, 9], while extrinsic risk factors comprise cigarette smoking, environmental exposures, and air pollution [10, 11]. Moreover, studies of familial clustering of pulmonary fibrosis provided evidence that IPF is associated with genetic susceptibility. Multiple genes can affect alveolar stability, for example, genes encoding surfactant proteins A and C, genes associated with enhanced cell senescence by disruption of telomerase function, with the integrity of the epithelial barrier, and with mutant desmosome proteins [12, 13, 14, 15].
Chronic obstructive pulmonary disease (COPD) is another chronic lung pathology, representing a serious and growing global health problem, as it is currently a leading cause of death worldwide [16]. COPD is a disease characterized by irreversible airflow reduction, associated with a decline in lung function and increased inflammatory response [17]. It represents a massive health problem, and it is estimated to affect around 200 million people worldwide, with a projected estimate towards further increase in the near future [18]. COPD is the result of the interaction between genetic susceptibility and environmental factors [19]. A well acknowledged genetic cause is α1-antitrypsin deficiency [20], while among environmental factors cigarette smoking represents the main cause; nonetheless, environmental pollution, occupational exposure to dust and fumes, and exposure to passive smoke can induce an increased risk in non-smokers, as well [21, 22]. Exposure to cigarette smoke, which contains a large number of pro-oxidant molecules [23], causes direct damage to the epithelial cells of the airways, leading to increased inflammation and activation of neutrophils, macrophages and lymphocytes in the airways [24]. There is currently no cure for COPD, but fortunately most symptoms can be treated and controlled mostly pharmacologically, at least delaying its progression and worsening. It represents indeed the most common indication for lung transplantation, that is the only conclusive therapeutic option for severe COPD, particularly in younger patients.
Cigarette smoking likely represents the single most significant risk factor for several lung conditions, and it is strongly associated with COPD and IPF, both familial and sporadic. Although observations about environmental risk factors have many biases and limitations [25], increasing knowledge on the underlying causes of lung diseases is evidencing how oxidative stress (OXS) and reactive oxygen species (ROS) play a crucial pathogenetic role (Figure 1).
Oxidative stress in lung pathogenesis. Intrinsic and extrinsic risk factors contribute to the progression of lung damage in the development of idiopathic pulmonary fibrosis (IPF) and obstructive pulmonary disease (COPD). In particular, cigarette smoking, environmental exposures, and air pollution induce an increase of reactive oxygen species (ROS) and oxidative stress condition, which play a crucial pathogenetic role in lung diseases. ROS, such as H2O2 and O2−, generated from NOX2 and NOX4, have a central role in the pathogenesis of pulmonary diseases. Indeed, ROS produced by these enzymes are involved in alveolar epithelial cell apoptosis, activation of inflammation, and induction of tissue fibrosis, that are all mechanisms underlying the progression of IPF and COPD. Figure was prepared using images from Servier Medical Art by Servier (https://smart.servier.com), which are licensed under a Creative Commons Attribution 3.0 Unported License.
The lungs are indeed highly susceptible to ROS-induced injuries. ROS are commonly thought to be a harmful by-product generated in cellular systems. However, recent studies have suggested that ROS physiological levels regulate important biological functions in cellular processes [2, 26]. Normally, ROS are tightly controlled by enzymes and antioxidant molecules. Nonetheless, excessive ROS accumulation may occur under certain conditions, thus making detoxification by the antioxidant system difficult. The result is indeed a condition called OXS that can affect cell proliferation, differentiation, aging, and death [27]. Cigarette smoke is responsible for significant oxidant burden and decreased antioxidant capacity even in plasma [28, 29]. ROS produced from cigarette smoke, combustion of organic matter and gases, like ozone and nitrogen dioxide, are featured on the lung epithelium [30], and could decrease antioxidant defenses, increasing OXS in the lungs [31].
A disrupted function of the redox system can consequentially impact on key cell signaling pathways involved in disease progression. Conversely, several signals can alter the oxidative state of lung cells. For example, the lung is constantly exposed to biomechanical forces, such as fluid shear stress, cyclic stretch, and pressure, due to the blood flowing through the pulmonary vessels, and the distension of the lungs during the breathing cycle. It is indeed known that cells within the lung respond to these changes by activating signal transduction pathways that can also alter their redox state with pathophysiological consequences [32]. Particularly in the vasculature, the two types of biomechanical stimuli, such as frictional force known as shear stress (SS), or wall shear stress (WSS) that acts tangentially to the vessel, could determinate dysregulation of the cellular redox status, that in turn could have effects on intracellular signaling pathways involved in disease progression [33]. For example, exposure of endothelial cells to laminar SS can induce a suppression of ROS levels [34, 35]. Conversely, exposure of endothelial cells to WSS using an irregular flow induces an increase of ROS levels and a reduced bioavailability of the vasodilator molecule NO [36], which is involved in preventing the activation and adhesion of platelets and leukocytes to the wall of the injured vessel [37].
A significant role in the pathogenesis of COPD is precisely the imbalance of ROS production and antioxidant capacity [38]. Changes in the redox balance in the lungs and circulatory system, genetic polymorphisms, and activation of transcription factors, such as the nuclear factor kappa B (NF-κB), lead to the molecular pathogenesis of COPD [39, 40]. Oxidized proteins and lipid products, such as isoprostanes and carbonylated proteins, can be identified in exhaled air, bronchoalveolar lavage fluid, and lung tissue from patients with fibrotic lung diseases and COPD [41, 42]. Furthermore, clinical worsening of COPD is often associated with down-regulation of the antioxidant system, thus a possible therapeutic method for COPD could be the administration of redox-protective antioxidants [38]. Finally, it is possible that maintaining a balance between oxidant and antioxidant species in COPD affected smokers may slow down disease progression [43].
As discussed, smoking, occupational exposures like asbestos or silica, and radiation are the principal sources of OXS with overproduction of ROS, that could lead and contribute to pulmonary fibrosis [44]. Indeed, OXS is an important molecular mechanism underlying fibrosis in a variety of organs, including lungs. Bleomycin-induced pulmonary fibrosis, the most commonly used experimental animal model, has been shown to be associated with marked increase in the level of ROS, oxidized proteins, DNA and lipids [45]. Following lung injury three main mechanisms (i.e. inflammation, coagulation disturbances, and OXS) are involved and alter the lung interstitial cell compartment and extracellular matrix (ECM) homeostasis, resulting overall in pulmonary fibrosis. ROS can be produced by several cellular types involved in fibrosis including alveolar macrophages [46, 47, 48] and lung epithelial cells [49]. In particular, ROS generated from the mitochondria of stressed or damaged epithelial cells are very important; their mitochondrial dysfunction results in the generation and release of ROS, such as H2O2 and O2−, further enhancing OXS and cell damage [50]. As previously discussed, NAD(P)H oxidase is the main source of ROS, and isoforms NOX1, NOX2, and NOX4 have a central role in the pathogenesis of pulmonary fibrosis [51] (Figure 1). For example, NOX4 is strongly expressed in the hyperplastic alveolar epithelium of IPF patients [52], and ROS produced by NOX4 are involved in alveolar epithelial cell apoptosis. Continuous epithelial apoptosis further supports activation of inflammatory processes and cytokine release, including myofibroblast activating molecules, such as TGF-β1, PDGF, IL-1, and TNFα (Figure 1). There is also evidence of direct pathogenetic involvement of these enzymes in IPF, for example for NOX2: in fact, supporting data have shown that mice genetically deficient in NOX2 do not develop IPF after bleomycin or carbon nanotubes exposure [51, 53]. Finally, the interplay between oxidative stress and TGF-β1 signaling is of great importance in promoting fibrosis. In fact, TGF-β1 is the most profibrogenic protein and can directly stimulate NOX-mediated ROS production, while OXS in turn can activate latent TGF-β1, setting up a vicious profibrogenic positive feedback loop [54].
As mentioned previously, fibrosis and oxidative stress are linked to a dysregulation of cellular homeostasis and impaired alveolar structure in chronic lung diseases [55]. Despite the paramount importance of animal models in biomedical and clinical research, they often do not fully recapitulate the pathogenesis of human IPF [56]. Moreover, there is increasing social and political pressure on reducing animal experimentation, according to the 3R’s principle of replacement, reduction, and refinement. Furthermore, the associated costs of animal purchasing, housing, and handling cannot be ignored, as well [57]. Under this perspective, 3D cultures (such as organoids) and innovative microfluidic devices (such as “organs-on-chip”) represent useful platforms to perform significant investigations in vitro on multiple topics, including the pathogenesis of COPD, IPF, or other lung diseases. They grant simultaneous multicellular culture and cell–cell interactions that overcome the limitations of standard monolayer cell cultures, allowing a step forward towards reproducing the complexity of tissues. Moreover, specific protocols and setups make it possible to simulate many more elaborated pathogenetic features, such as ontogenetic-like mechanisms, tunable biomechanical cues, altered gas/liquid interfaces, as well as immune cells recruitment and activation (Figure 2). Physiologically relevant in vitro systems are also suitable to discover and test new drugs and therapeutics, supporting the clinical translation of novel protocols in a “personalized medicine” perspective [1].
In vitro models of lung pathology. Both organoids and lungs-on-chip allow the creation of 3D systems where complex cell–cell interactions and multi-cellular cultures are possible. Moreover, drug discovery and testing in these settings can provide important preliminary results in vitro. Several features, though, are better reproduced in specific 3D systems, for example the inclusion of an extracellular matrix, or the modelling of ontogenetic-like mechanisms better fit in organoid cultures. Conversely, biomechanical cues, gas and liquid interfaces, and immune cells response are more finely tunable with organs-on-chip technology. Figure was prepared using images from Servier Medical Art by Servier (https://smart.servier.com), which are licensed under a Creative Commons Attribution 3.0 Unported License.
Three-dimensional culture systems offer multiple advantages for in vitro phenotype control in order to obtain physiologically relevant settings [58]. The simplest 3D culture system is represented by spheroids, which can be obtained from embryonic-like stem cells or several resident lung cell types, particularly those with a facultative stemness potential (e.g. pneumocytes, Clara cells [59]). Lung cell spheroids, despite their simplicity, can provide useful preliminary models even for the study of complex pathological issues. Alveoli-like structures obtained from distal airway stem cells [60] or Oct-4+ progenitor cells [61] have been used for the study of viral infections (e.g. H1N1 influenza virus, or SARS-CoV), the pathogenesis of tissue damage, and subsequent mechanisms of tissue repair. As another example, lung spheroids from stromal primitive cells [62] have significantly contributed to the elucidation of novel pathogenetic mechanisms during organ reconditioning procedures, in particular during ex vivo lung perfusion (EVLP) protocols before lung transplantation. In fact, OXS strongly contributes to tissue damage during EVLP. It has been shown that inhibition of NOX2 activity during thermic stress and starvation (mimicking EVLP conditions) can reduce ROS production, thus being protective for lung epithelial cells [63, 64]. Finally, specific interference of cigarette smoke with Wnt/β-catenin signaling has been described in human fibroblasts, impairing their capacity to support spheroid growth of lung epithelial cells, which can be considered in this case as a stemness assay linked to the activation of a repair mechanism [65].
The more complex example of organotypic 3D cultures is represented by organoids. Lung organoids are self-assembling structures of lung cell types that replicate cell–cell interaction, cell-ECM interaction, and organ structure and function at the microscale, as similar as possible to in vivo histological architecture. They can be used as models of both physiological and pathological settings. Strikoudis et al. have modelled pulmonary fibrosis in lung organoids to study Hermansky-Pudlak syndrome (HSP) [66]. IPF and HSP both are characterized by lung fibrosis, and are now considered as similar clinical entities, albeit with distinct etiology. Lung organoids were generated from embryonic stem cells (ESCs) with specific mutations that strongly predispose to HSP. The resulting organoids displayed a fibrotic phenotype, with an enhanced number of mesenchymal cells, and increased deposition of fibronectin and collagen. Interestingly, HSP organoids share a strong signature with lung samples from IPF patients, including the overexpression of interlukin-11 (IL-11), a key driver of the fibrotic process that is stimulated also from OXS [67]. This finding validates HSP lung organoids as a tool to study IPF and other lung diseases characterized by fibrosis [66]. Similarly, Wilkinson et al. have developed an organoid from induced pluripotent stem cell (iPSC)-derived fibroblasts functionalized with hydrogel beads, that acts as a 3D alveolar template within a rotating bioreactor [68]. Interestingly, they discovered that organoid formation was not possible in their conditions without the inclusion of fetal lung fibroblasts. Treatment of cultures with exogenous TGF-β1 consistently increased contraction, expression of Collagen 1 and α-SMA, and the emergence of fibroblastic foci within the treated organoid. This system showed features of tissue scarring similar to IPF, thus confirming the feasibility of organoid culture systems to model lung fibrosis. Moreover, these lung organoids can recapitulate even a more complex and representative lung microenvironment when cultured with endothelial and epithelial cells [68]. As an example, using lung organoids from patients with IPF, Surolia et al. described a 3D model to predict the invasive response of IPF fibroblasts to antifibrotic drugs therapy. They observed that inhibition of vimentin intermediate filaments assembly can reduce the invasiveness of lung fibroblasts derived from the majority of the IPF patients tested, uncovering a possible novel therapeutic target for pulmonary fibrosis [69].
Overall, these 3D self-assembled systems recapitulate numerous pathogenetic features of diseases, but nonetheless still show several limitations in their application as models, such as lack of vascular network, immune cells, and other supporting cells (Figure 2). These features need to be implemented to reach higher levels of physiological relevance for lung disease modelling [69].
In the last decade, the integration of advanced bioengineering approaches (e.g. 3D multicellular cultures) with microfluidic and microfabricated substrates has led to the development of devices called “organs-on-chip” [70]. These bioengineered tools allow fine control and tuning of the microenvironment architecture, media composition, and cell–cell interactions. The combination of lung cells and micro/nanoengineering devices gave rise to new in vitro models for the study of therapeutic approaches in pulmonary diseases. In fact, lungs-on-chip can recapitulate typical features of the parenchymal structure, and primary physiological or pathological conditions of the human lung microenvironment, such as liquid and gas interfaces [71] (Figure 2). In 2010, Hu et al. for the first time created a lung-on-chip using a soft lithography technique. Soft lithography offers the advantage to control the molecular structure of surfaces, the pattern of complex molecules relevant to biology, and to fabricate channel structures appropriate for microfluidics [72]. They produced a biomimetic microdevice that recapitulates the crucial alveolar-capillary interface of the human lung. This device is a 2.5D system since it contains monolayers of epithelial and endothelial cells that mimic the alveolar-capillary barrier, and permits investigation under dynamic conditions, with biomechanical cues in the form of SS due to perfusion, and strain similar to breathing [71]. However, ECM components are lacking in this model, and this significantly limits the relevance of this device, in particular concerning the study of pulmonary fibrosis. To address these limitations, other groups have designed arrays of 3D microtissue that are suspended over multiple flexible poly-dimethylsiloxane (PMDS) micropillars [73, 74, 75]. In particular, Sellgren et al. produced an advanced model by co-culturing interstitial fibroblasts with epithelial and endothelial cells [75]. They demonstrated the feasibility of including a stromal layer within lung-on-chip devices. Similarly, Asmani et al. have developed a human lung device to model key biomechanical events occurring during lung fibrogenesis, which include progressive stiffening and contraction of alveolar tissue. They used this system for predicting the efficacy of anti-fibrotic drugs for IPF patients, demonstrating that preventative treatments with these drugs can reduce tissue contractility, and counteract tissue stiffening and decline in tissue compliance [73]. Overall, these new approaches will give a better understanding of the complex pathogenesis of IPF.
As discussed above, COPD is a syndrome defined by progressive and chronic airflow limitation, due to the fact that lungs become inflamed, damaged, and narrowed. The main cause is smoking, but others exist such as long-term exposure to harmful fumes or dust, and rare genetic conditions [43]. As for IPF, the animal models of COPD present some limitations. For example, modelling cigarette smoke exposure fails to recapitulate some major airway phenotypes of COPD, such as hyperplasia of basal and mucin-producing cells, and mucus plugging of the airways [76]. Before the advent of lung-on-chip technology, the best-established in vitro model to study COPD disease and to address cigarette smoke-induced damage on human airway epithelial cells was the air-liquid-interface (ALI) culture system [77]. The defining feature of ALI cultures is that the basal surface of the cell is in contact with a liquid culture medium, whereas the apical surface is exposed to air [78]. These systems mimic the conditions found in the human airway, and drive differentiation towards different phenotypes [79]. One major limitation of conventional ALI models is that these static culture systems make dynamic processes, such as nutrient exchange and immune cell migration [80], difficult to study.
In this regard, innovative approaches, such as microfluidic lungs-on-chip, have been developed in the last years and helped filling this gap. In 2016, Benam et al. developed the human lung “small airway-on-a-chip”, a microfluidic device that supports and drives full differentiation of a columnar, pseudostratified, mucociliary bronchiolar epithelium, composed of cells isolated from healthy individuals or people with COPD, underlined by a functional microvascular endothelium [81]. They demonstrated that COPD small airway chips recapitulate important features of the disease, such as selective cytokine hypersecretion and neutrophil recruitment from the vascular flow in response to epithelial activation by pathogen-like stimuli. Moreover, exposure of the healthy epithelium to interleukin-13 (IL-13) reconstituted the asthmatic phenotype that involves goblet cells hyperplasia, cytokine hypersecretion, and decreased ciliary function [82]. The same group improved this system by developing a “Breathing-Smoking Human Lung-on-Chip”, a novel device that consists of four components: a small airway on-chip, a smoke generating robot, a micro-respirator, and a control software that mimics human smoking and breathing. This smoking airway-on-a-chip system effectively recapitulated several key smoke-triggered molecular changes that are known to occur in lung epithelial cells, including increased OXS [83]. When human airway chips fabricated using cells from healthy donors were exposed to whole cigarette smoke, the authors observed a significant increase in the expression of the anti-oxidant gene heme oxygenase 1 (HMOX1), and increased phosphorylation of the transcription factor nuclear factor-like 2 (Nrf2). The latter induces expression of cytoprotective genes, including HMOX1, protecting cells from OXS and chemical toxicity. Furthermore, they identified new smoke-induced dysfunction, such as reduced ciliary beating, a novel biomarker of COPD disease, and studied the epithelial responses to smoke generated by electronic cigarettes [84]. However, the main limitation of this system is the absence of cellular stromal components.
As mentioned before, COPD represents a group of lung diseases that also include refractory severe asthma. In this regard, Nesmith et al. have designed a human airway musculature-on-a-chip with bronchiolar smooth muscle cells on an elastomeric thin film. To recapitulate asthmatic inflammation in vitro, they exposed this biomimetic tissue to IL-13, which resulted in hypercontractility and altered relaxation. Interestingly, the authors were able to show reverse asthmatic hypercontraction of smooth muscle cells using a muscarinic antagonist and a β-agonist, which are used clinically to relax constricted airway [85]. Similarly, Villenave et al. developed a model of severe asthma-on-chip containing a fully differentiated mucociliary bronchiolar epithelium underlined by a microvascular endothelium with fluid flow [86]. They infected the engineered tissue with human Rhinovirus (HRV), a leading cause of asthma exacerbation in children and adults; this led to a pro-inflammatory response characterized by ciliated cells death, goblet cells hyperplasia, release of cytokines, recruitment from the fluid flow and extravasation of human neutrophils across the endothelium. Infection of IL-13-treated Airway Chips with HRV to mimic the molecular response observed in severe asthma patients, induced upregulation of adhesion molecules (E- and P-Selectin, ICAM-1) in endothelial cells, and increase of neutrophil recruitment when compared with IL-13 or HRV stimulation alone [87]. The same group implemented this device to study the integrity of epithelial monolayers-on-chip, measuring trans-epithelial electrical resistance (TERT). They designed a new microfluidic device within a human lung airway chip that contains embedded electrodes, and demonstrated its utility for the assessment of airway barrier function, formation, and disruption in response to relevant external stimuli [88]. These studies suggest that Airway Chips may provide unique opportunities to explore lung pathogenesis, including responses to drug treatments for the evaluation of safety and efficacy of new drugs. Moreover, the possibility of studying the involvement and activation of immune cells certainly brings added value to these systems, allowing the study of physiologically relevant issues within an integrated model.
Basic and translational research on lung biology and pathology can greatly benefit from the development of 3D in vitro models that can maintain cell phenotypes and functions in a physiologically relevant way. Lung organoids and lungs-on-chip allow the creation of different kinds of in vitro microenvironments (Figure 2), that can be useful for the study of specific diseases, and for the elucidation of novel pathogenetic pathways. They represent in fact important translational models for the study of clinically relevant issues, for the identification of novel therapeutic targets, and for preliminary testing of new drugs. The main challenge in future developments is represented by the standardization of integrated protocols for the simultaneous inclusion of extracellular matrix, stromal components, immune cells, and biomechanical cues within 3D in vitro models. This step forward would provide a clinically relevant system for lung research, which would include all the actors involved in endogenous responses occurring in vivo. Nonetheless, despite several limitations still existing, the complexity of these models has been rapidly increasing in the past decade, and they must be considered as complementary in all respects to in vivo studies carried on in animal models.
This work was supported by grant # 2015BN82FK from the Italian Ministry of Education, University and Research (MIUR) to Isotta Chimenti.
The authors declare no conflict of interest.
IntechOpen publishes different types of publications
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