Grading systems for salivary gland biopsies of Tarpley.
\\n\\n
Released this past November, the list is based on data collected from the Web of Science and highlights some of the world’s most influential scientific minds by naming the researchers whose publications over the previous decade have included a high number of Highly Cited Papers placing them among the top 1% most-cited.
\\n\\nWe wish to congratulate all of the researchers named and especially our authors on this amazing accomplishment! We are happy and proud to share in their success!
\\n"}]',published:!0,mainMedia:null},components:[{type:"htmlEditorComponent",content:'IntechOpen is proud to announce that 179 of our authors have made the Clarivate™ Highly Cited Researchers List for 2020, ranking them among the top 1% most-cited.
\n\nThroughout the years, the list has named a total of 252 IntechOpen authors as Highly Cited. Of those researchers, 69 have been featured on the list multiple times.
\n\n\n\nReleased this past November, the list is based on data collected from the Web of Science and highlights some of the world’s most influential scientific minds by naming the researchers whose publications over the previous decade have included a high number of Highly Cited Papers placing them among the top 1% most-cited.
\n\nWe wish to congratulate all of the researchers named and especially our authors on this amazing accomplishment! We are happy and proud to share in their success!
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Lembrikov is a senior lecturer at the Faculty of Electronics, Electrical and Communication Engineering of the Holon Institute of Technology (HIT), Holon, Israel. B. I. Lembrikov received his Ph.D. in Nonlinear Optics at the Technion – Israel Institute of Technology in 1996. Since then he was an invited researcher at the Haifa University, at the Max Planck Institute High Magnetic Field Laboratory at Grenoble, France, at the Technion, Haifa, Israel. Dr. B. I. Lembrikov is an author of the book \\Electrodynamics of Magnetoactive Media\\, a number of chapters in scientific books, a large number of papers in international peer reviewed journals and reports delivered at the international scientific conferences. He actively participated in a number of research projects concerning optics of nanoparticles, optical communications, UWB communications. The main research fields of interest of Dr. B. I. Lembrikov are nonlinear optics, optical and UWB communications, nanostructures, quantum dot lasers.",institutionString:"Holon Institute of Technology (HIT)",position:null,outsideEditionCount:0,totalCites:0,totalAuthoredChapters:"10",totalChapterViews:"0",totalEditedBooks:"3",institution:{name:"Holon Institute of Technology",institutionURL:null,country:{name:"Israel"}}}],coeditorOne:null,coeditorTwo:null,coeditorThree:null,coeditorFour:null,coeditorFive:null,topics:[{id:"1225",title:"Optical Physics",slug:"optics-and-lasers-optical-physics"}],chapters:[{id:"65062",title:"Introductory Chapter: Nonlinear Optical Phenomena",slug:"introductory-chapter-nonlinear-optical-phenomena",totalDownloads:683,totalCrossrefCites:0,authors:[{id:"2359",title:"Dr.",name:"Boris",surname:"Lembrikov",slug:"boris-lembrikov",fullName:"Boris Lembrikov"}]},{id:"64727",title:"Nonlinear Schrödinger Equation",slug:"nonlinear-schr-dinger-equation",totalDownloads:825,totalCrossrefCites:0,authors:[{id:"198550",title:"Ph.D.",name:"Jing",surname:"Huang",slug:"jing-huang",fullName:"Jing Huang"}]},{id:"63615",title:"Three Solutions to the Nonlinear Schrödinger Equation for a Constant Potential",slug:"three-solutions-to-the-nonlinear-schr-dinger-equation-for-a-constant-potential",totalDownloads:569,totalCrossrefCites:0,authors:[{id:"93519",title:"Dr.",name:"Gabino",surname:"Torres-Vega",slug:"gabino-torres-vega",fullName:"Gabino Torres-Vega"}]},{id:"63619",title:"Hydrodynamic Methods and Exact Solutions in Application to the Electromagnetic Field Theory in Medium",slug:"hydrodynamic-methods-and-exact-solutions-in-application-to-the-electromagnetic-field-theory-in-mediu",totalDownloads:338,totalCrossrefCites:1,authors:[null]},{id:"64097",title:"Polarization Properties of the Solitons Generated in the Process of Pulse Breakup in Twisted Fiber Pumped by ns Pulses",slug:"polarization-properties-of-the-solitons-generated-in-the-process-of-pulse-breakup-in-twisted-fiber-p",totalDownloads:462,totalCrossrefCites:0,authors:[null]},{id:"63461",title:"Towards Enhancing the Efficiency of Nonlinear Optical Generation",slug:"towards-enhancing-the-efficiency-of-nonlinear-optical-generation",totalDownloads:421,totalCrossrefCites:0,authors:[null]},{id:"63480",title:"Widely Tunable Quantum-Well Laser: OPO Diode Around 2 μm Based on a Coupled Waveguide Heterostructure",slug:"widely-tunable-quantum-well-laser-opo-diode-around-2-m-based-on-a-coupled-waveguide-heterostructure",totalDownloads:399,totalCrossrefCites:0,authors:[null]},{id:"63398",title:"Stimulated Raman Scattering in Micro- and Nanophotonics",slug:"stimulated-raman-scattering-in-micro-and-nanophotonics",totalDownloads:679,totalCrossrefCites:1,authors:[null]}],productType:{id:"1",title:"Edited Volume",chapterContentType:"chapter",authoredCaption:"Edited by"},personalPublishingAssistant:{id:"185543",firstName:"Maja",lastName:"Bozicevic",middleName:null,title:"Ms.",imageUrl:"https://mts.intechopen.com/storage/users/185543/images/4748_n.jpeg",email:"maja.b@intechopen.com",biography:"As an Author Service Manager my responsibilities include monitoring and facilitating all publishing activities for authors and editors. From chapter submission and review, to approval and revision, copyediting and design, until final publication, I work closely with authors and editors to ensure a simple and easy publishing process. I maintain constant and effective communication with authors, editors and reviewers, which allows for a level of personal support that enables contributors to fully commit and concentrate on the chapters they are writing, editing, or reviewing. I assist authors in the preparation of their full chapter submissions and track important deadlines and ensure they are met. I help to coordinate internal processes such as linguistic review, and monitor the technical aspects of the process. As an ASM I am also involved in the acquisition of editors. 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In one method, the data are collected by analog to digital conversion of the ECG signal and computer evaluation of the RR intervals from the ECG signal. In the second method, devices are used whose output is the RR interval alone. The advantage of the first method is the control of accuracy and flexibility of the evaluations. The second method has the advantage of storing smaller amount of data, and it can be easily used online.
\nIn the first method, usually the number of collected data (sampled ECG signal) is of two to three orders of magnitude larger than the RR interval data. Thus if only RR interval is analyzed, a large amount of data is unused. In this paper we are trying to take advantage of the ECG sampled signal and to derive new information in addition to the conventional RR interval analysis [1, 2, 3, 4, 5].
\nThe ECG signal spectrum is bounded below the frequency fB by using an electronic filter and sampled at rate larger than 2fB, thus excluding aliasing from spectral analysis [6]. A similar procedure cannot be applied to the RR interval spectral analysis, and in this case an aliasing is possible. One of our main efforts in this paper is devoted to the problem of how to detect aliasing in the RR interval spectral analysis.
\nIn order to get an insight, we performed an experiment, in which the ECG signal of one of the authors (AG) was detected, while the breathing rate was larger than half the heart rate. A constant breathing rate for a time exceeding 5 minutes was monitored with good accuracy using a special breathing procedure with a metronome. The results show distinctively a very sharp peak in the spectral analysis of the ECG signal and corresponding (diffused) aliasing peaks in the RR interval spectral analysis.
\nThe spectral analysis of the ECG signal was performed with the standard FFT procedures. The spectral analysis of the RR intervals was performed with several techniques in order to take into consideration that the data were unevenly sampled. This is presented in Section 2. In Section 3, we discuss the possibility of aliasing in the spectral analysis of the RR intervals. In Section 4, we compare power estimations of ECG’s and RR intervals of three experiments. In Section 5, we analyze the results. In Section 6, summary and conclusions are presented.
\nThe methods of spectral analysis are well developed for evenly sampled data [6, 7]. The RR interval data are unevenly sampled in time. In most cases an analysis is performed with respect to beat numbers which are evenly spaced. We will below justify this method using least square principles. But as was recently indicated by Laguna et al. [8], the resampling of data is causing the appearance of additional harmonics. They recommend to use a method developed by Lomb [9]. The errors of resampling the beats can, to large extent, be overcome by using a cubic spline interpolation. In this work we are suggesting a new method of treating unevenly sampled data, which, unexpectedly, gave good results beyond the Nyquist frequency.
\nLet us assume that the RR intervals are given at unevenly sampled times \n
and let us generate in the interval \n
We will use the discrete Fourier transform (DFT) for a basis formed from the evenly sampled times \n
The coefficient \n
with the result
\nEqs. (3 and 5) can be handled easily with standard FFT programs. This is the usual procedure which is adopted in most of the papers dealing with RR interval analysis [4, 5].
\nFFT can be applied more efficiently if the unevenly sampled data are interpolated at evenly spaced intervals of Eq. (2). The cubic spline interpolation is one of the good ways to do it.
\nThe Lomb method [9] was extensively analyzed in Ref. [8]. We give here only the formulae in the form of the Lomb normalized periodogram:
\nwhere \n
We present here a new method of treating unevenly spaced events which we call the “nonuniform discrete Fourier transform” (NUDFT).
\nLet us assume that \n
Our aim is to find a good approximation to this expression in terms of the unevenly sampled signal \n
We start with the Euler summation formula:
\nand make the following decomposition of the integral on the right hand side of Eq. (9)
\nand approximate each of the integrals on the right hand side with the trapezoidal rule
\nFrom Eqs. (9) and (11), we obtain:
\n\n
When \n
and the final result, the approximation to Eq. (8), after rearranging the terms, becomes
\nwhere
\nwith the inverse formula
\nwhich is an interpolation formula for \n
Aliasing is a result of undersampling and is a well-known phenomenon. In Ref. [10], aliasing was looked upon from the point of view of symmetry. It is an example of wrong symmetry and as such should be given more attention. It is the outcome of an incomplete basis. It was found in Ref. [10] that for evenly sampled data with a sampling rate \n
where \n
In order to avoid the aliasing symmetry of Eq. (17), the frequencies should be bounded by the Nyquist frequency (denoted here by \n
The ECG signal was sampled with sampling rate 250 Hz, and an electronic filter was applied, which have eliminated practically all frequencies above 32 Hz, thus aliasing cannot occur at frequencies below 125 Hz or even below 32 Hz. The RR intervals were calculated directly from the ECG signal. The sampling rate for RR intervals can be defined only for evenly sampled data and for the methods that interpolate the unevenly sampled data, or one can consider the average sampling rate from Eq. (1) in both cases:
\nwhere \n
Another possibility of detecting aliasing is by comparing the heart rate spectrum with the ECG signal spectrum. Marked differences below the Nyquist frequency for the power distribution of the RR intervals compared to the ECG signal power distribution in the same range may indicate aliasing. But we do not have yet a sound basis to treat this problem.
\nWe have devised an experiment which definitely demonstrates the aliasing in the RR interval spectrum. To the best of our knowledge, this is the first experiment in which one can exactly know the correct frequency above the Nyquist frequency and can follow the development of the aliasing, which appears to be diffused to great extent because the symmetry of Eq. (17) is represented not by one sampling rate but by a distribution of sampling rates, as the RR interval is unevenly sampled.
\nBelow we describe three experiments. One of them was devised to demonstrate aliasing and the other two for learning about the relations between the RR interval spectrum and the spectrum of the ECG signal.
\nWe present below results of three experiments. In the first experiment, the ECG signal was collected in a normal resting state. The aim of this experiment was to compare the ECG spectrum with the RR interval spectrum. In the second experiment, very slow breathing was monitored at a rate of 0.04 Hz. Again the ECG and RR interval spectra were compared. In the third experiment, very fast breathing was accurately monitored at the rate of 74/min and 84/min. These respiratory rates were above half of the heart rates, thus allowing to observe in detail the development of aliasing.
\nIn this experiment (linked with the names of Zahi and Ori, where the second is one of the authors: O.G), which was done in normal, resting conditions, we compare the power estimation of the RR interval and the ECG signal, from which the RR interval was obtained. The ECG signal was sampled at a rate of 250 Hz. Stable intervals of 7-minute duration were chosen for analysis.
\nIn Figure 1a the power distribution of the ECG signal of Zahi is depicted. The attenuation of the power with increasing frequency above 12 Hz is due to the action of an electronic filter. Above 32 Hz the contribution is practically zero. The average heart rate was 0.97 Hz. The above results were zoomed to the interval [0–12] Hz in Figure 1b. One can see distinctively the peak around the average heart rate and the higher harmonics of this peak. The second harmonic is missing, but the third, fourth, fifth, and sixth are distinctively visible; higher harmonics became more and more smeared and indistinguishable above the sixth harmonic. One should also note the large difference in power in the heart rate range, below the Nyquist frequency of 0.49 Hz, which is much smaller than the peak around the average heart rate 0.97 Hz.
\nThe relative power of the ECG signal of Zahi, (a) in the spectral range of 0–36 Hz and (b) in the spectral range of 0–12 Hz.
The power distribution of the RR intervals in the range {0–0.5} Hz was computed according to the methods discussed in Section 2 and is presented in Figure 2a (DFT, beat number analysis), Figure 2b (Spline interpolation), and Figure 2c (NUDFT). For comparison also the power distribution of the ECG signal in the above range is presented in Figure 2d.
\nThe relative power computed (from the ECG signal of Zahi) by four different methods, in the spectral range of 0–0.5 Hz, (a) by DFT, (b) by spline interpolation of the RR data, (c) by NUDFT, and (d) from the ECG signal.
The results of Figure 2a–c are quite similar, but the spline interpolation (Figure 2b) and the NUDFT (Figure 2c) are practically identical. The three graphs show the structure commonly found in the power estimation analysis of RR intervals, namely, the existence of the “high-frequency” (HF), “low-frequency” (LF), and the “very low-frequency” (VLF) peaks. The ECG spectrum shows qualitatively the same structure (but not a quantitative agreement), except that the ECG spectrum is highly suppressed below 0.04 Hz, in the VLF region, indicating a possibility of aliasing in this region in the RR analysis.
\nIn Figures 3 and 4a–d, the results of Ori are presented. The conclusions are similar to those of Zahi, except that in the ECG spectrum, both VLF and LF peaks are missing, indicating the possibility of aliasing in these regions for the RR analysis. Also in the ECG spectrum of Ofek, VLF and LF, present in Figure 5a, are missing. VLF is missing in J.C.’s ECG spectrum (see Figure 6a–6b).
\nThe relative power of the ECG signal of Ori.
The relative power computed (from the ECG signal of Ori) by four different methods, in the spectral range of 0–0.52 Hz. (a) by DFT, (b) by spline interpolation of the RR data, (c) by NUDFT, (d) from the ECG signal.
The relative power computed (from the ECG signal of Ofek) by two different methods, in the spectral range of 0–0.6 Hz, (a) by spline interpolation of the RR data, (b) from the ECG signal.
The relative power computed (from the ECG signal of J.C.) by two different methods, in the spectral range of 0–0.46 Hz, (a) by spline interpolation of the RR data, (b) from the ECG signal.
In this experiment (linked again with the name Ori), we have checked the ECG spectrum near the VLF region, as the VLF was absent in the ECG spectrum for the resting state in the first experiment. The question was whether such a result persists in all ECG spectra. Therefore we have probed the VLF region by monitoring very prolonged breathing with a rate of 0.04 Hz. For the spectrum of RR intervals, we found that the DFT, spline interpolation, and NUDFT give similar results, and again NUDFT was practically identical to the spline interpolation. Therefore we present only the results of NUDFT, which are presented in Figure 7a. For comparison the spectrum of the ECG signal is given in Figure 7b. In Figure 7a one can see a very clean pattern of a peak at 0.04 Hz and its higher harmonics. In Figure 7b one can see a similar but somewhat diffused pattern. Thus this experiment indicates that similar respiratory patterns exist in both the RR and in the ECG signals.
\nThe relative power computed (from the ECG signal of Ori with breathing rate of 0.04 Hz) by two different methods, in the spectral range of 0–0.62 Hz, (a) by NUDFT, (b) from the ECG signal.
In this experiment (linked to the name Alex, who is one of the authors: AG), very fast breathing was accurately monitored at the rate of 74/min and 84/min, respectively. These rates were well above half of the average heart rate, thus allowing to observe in detail the development of aliasing. In Figure 8 the ECG spectrum is dominated by the very high and narrow peak at the frequency \n
The relative power of the ECG signal of Alex with a breathing rate of 1.234 Hz.
The relative power computed (from the ECG signal of Alex with a breathing rate of 1.234 Hz) by two different methods, in the spectral range of 0–1.5 Hz, (a) by NUDFT, (b) from the ECG signal.
A 100 bin histogram of the heart rates of Alex which are subtracted by the breathing rate of 1.234 Hz.
In principle the NUDFT and the Lomb methods should not be used above the Nyquist frequency. Surprisingly enough we have found that both methods have a sharp peak at \n
Similar results for the breathing frequency 84/min are presented in Figures 11–12.
\nThe relative power of the ECG signal of Alex with a breathing rate of 1.404 Hz.
The relative power computed (from the ECG signal of Alex with a breathing rate of 1.404 Hz) by two different methods, in the spectral range of 0–1.6 Hz, (upper figure) by NUDFT, (lower figure) from the ECG signal.
Since our experiment, which demonstrated how aliasing is developing in human beings, nobody had performed experiments on human beings. The reason is that till now, nobody dared (except one of us, AG) to do extremely fast breathing of 74 breaths/min and 84/min, for more than 5 minutes. After reading our preprint, Campbell [17] and his colleagues found an aliasing in fish [17]. Other researchers were more concerned with preventing aliasing, observing the phenomenon in speeded heart rate, and in constructing aliasing filters [18, 19, 20, 21].
\nThe ECG signal spectrum is bounded below the Nyquist frequency fB by using an electronic filter and sampled at rate larger than 2fB, thus excluding aliasing from spectral analysis. A similar procedure cannot be applied to the RR interval spectral analysis, and in this case an aliasing is possible. One of our main efforts in this paper was devoted to the problem of how to detect aliasing in the RR interval spectral analysis.
\nIn order to get insight into this problem, three experiments have been analyzed. In the first experiment, the ECG signal was collected in a normal resting state. The aim of this experiment was to compare the ECG spectrum with the RR interval spectrum. In the second experiment very slow breathing was monitored at a rate of 0.04 Hz. Again the ECG and RR interval spectra were compared. In the third experiment, very fast breathing was accurately monitored at the rate of 74/min and 84/min, respectively. These respiratory rates were above half of the heart rates, thus allowing to observe in detail the development of aliasing.
\nThe experiments which were described above led us to the following conclusions:
The spectral analysis of the ECG signal is more sensitive and accurate than the RR interval spectral analysis and is free from aliasing. Still in the present stage, it contains too much information to be of practical use. Efforts should be made to understand what will be the best way to extract information (not related to the heart condition alone as in the standard analysis of ECG) about the external influences on the heart signal.
We have conducted an experiment which gave a clear insight about the mechanism of aliasing in the RR interval spectrum. The very sharp peak in the spectrum of the ECG signal, which came as the result of enforced quick breathing, reappeared as a diffused signal in the RR spectrum. The extension of the diffuseness agrees with the extension of the sampling rates of unevenly sampled data.
The VLF peak observed in the RR interval spectrum is usually missing in the ECG spectrum. This leads us to suspect that the VLF observed in the RR spectrum has its origin in aliasing.
In some cases the LF peak does not show up in the ECG spectrum. This led us to suspect that part of the LF peak is of aliasing origin.
Unlike in electronic devices, it is very difficult to devise procedures to detect aliasing in humans. In electronic devices aliasing can be easily detected by changing the sampling rate. In humans the fluctuations of the heart rate are of the same order as the required changes in the sampling rates. It will be an important task to develop a proper procedure for detecting aliasing in humans.
We have developed a new technique for spectral analysis for unevenly sampled data called nonuniform discrete Fourier transform (NUDFT). When employed to the RR data, below the Nyquist frequency, it gave similar results as those obtained by interpolating the data with a cubic spline. Above the Nyquist frequency, the correct peak in the spectrum was detected with great accuracy. A similar result was obtained with the recently rediscovered Lomb method. We interpret this unexpected result by a partial destruction of aliasing symmetry in both methods. More efforts should be made in order to understand the anti-aliasing properties of the above methods.
We consider aliasing to be a wrong symmetry, resulting from the use of an incomplete basis, which has intrinsic symmetries inconsistent with the properties of the signal. Aliasing can be partially removed by reducing the symmetry of the basis.
Microscopic findings involving lymphocytic infiltration surrounding the excretory ducts in combination with the destruction of acinar tissue are representative for both minor and major salivary glands and are pathognomonic changes for SS. Parotid, lip, or sublingual salivary gland biopsy is performed in the diagnosis and monitoring of SS, but currently only labial salivary gland biopsy (LSGB) is included into classification criteria of SS. LSGB is used for the diagnosis of Sjögren’s syndrome (SS). The current classification criteria of SS, approved by the American College of Rheumatology (ACR) and the European League against Rheumatism (EULAR) in 2016, include LSGB as a part of weighted sum of five items [1]. The presence of focal lymphocytic sialadenitis (FLS) with a focus score of 1 foci/4 mm2 glandular tissue is a positive score of LSGB. Lip salivary glands are widely distributed in the labial mucosa of the oral cavity. They are largely used for assisting the diagnosis of SS, because they are easily accessible and lie above the muscle layer. They are separated from the oral mucous membrane by a thin layer of fibrous connective tissue. Orientation and identification of glandular tissue is the easiest. The risk of excessive postoperative bleeding is decreased because the arterial supply to the lip lies deep. These anatomical implications and pathognomic changes predispose of labial salivary glands to the biopsy [1, 2, 3, 4, 5, 6, 7].
\nLabial salivary gland biopsy is considered a minor surgical procedure and can be performed on the ambulatory basis. There is no standardized technique that yields adequate tissue for analysis and minimizes adverse effects. The lack of uniformity in methodology and potential adverse effects of LSGB hinders its application. LSGB is treated as a safe and simple surgical procedure without severe postoperative complications. One of the most severe complications of LSGB is sensitive nerve injury. This localized sensory alternation can be described as an anesthesia, a reduced or partial loss of sensation, a transitory numbness, or a hypoesthesia. These sensations can last for a few months or can be permanent. Persistent lip numbness occurs in up to 6% of biopsies performed in the lower lip [8]. The branches of the mental nerve in the lower lip are closely associated with the salivary glands, and this anatomical relationship increases the risk of postoperative sensory sensations. Additionally, the branch of the mental nerve usually divides into two sub-branches: a horizontal and a vertical, which have an ascending course toward the vermillion border and are in close relation to the labial salivary glands. Incisional biopsies shorter than 2 cm performed with a scalpel have reported complications ranging from 0 to 9.3%, whereas those using larger incisions (2–3 cm) have described complications in the range of 3.7–31%. Transient disorders of lip sensitivity are found to occur in up to 11.7% of procedures. Persistent lower lip hypoesthesia is reported in about 3.4–4% of cases. Larger incisional biopsies and punch biopsies are associated with a higher risk of both transient and persistent lower lip numbness. Other possible complications of LSGB are less severe, usually transient or temporary, and are associated with localized postoperative inflammation or improper healing. The symptoms of postoperative inflammations are local pain and swelling. Blood vessel injuries result in hematoma. The possible delayed complications are the formation of granulomas, internal scarring, and cheloid formation. Labial salivary gland injuries can result in mucous extravasation cysts. Some patients can report burning or tingling sensations, and functional deficits during the immediate postbiopsy period such as eating, sleeping, or speech difficulties [9, 10, 11, 12].
\nLabial glands biopsy may be an excisional or incisional technique. The most recommended site is normal-appearing mucosa of the lower lip. Usually, it is a scalpel biopsy. A wide range of surgical approaches have been described for harvesting a few accessory glands from the lower lip using different instruments such as a scalpel, a punch, or cup forceps. The use of a forceps with a fenestrated active end to stabilize the lip has also been suggested. The excisional biopsy is carried out by excising an ellipse of oral mucous membrane down to the muscle layer. Ideally, 6–8 minor glands must be harvested and sent for histopathologic examination. The wound should be closed with 4-0 silk sutures, which are removed after 4–5 days. The modification of this method is the technique with a mucosal excision of 3.0 × 0.75 cm. Another recommended technique is a 1.0–1.5-cm-wedge-shaped excision of the mucosa between the midline and commissure. The incisional biopsy is described as a 1.5–2.0-cm linear incision of mucosa, parallel to the vermillion border and lateral to the midline. Gorson and Ropper reported a 1-cm vertical incision just behind the wet line through the mucosa and submucosa [31]. It is usually that case that the lateral lip compartments are advocated for biopsy, because of the glandular-free zone in the center of the lower lip. Berquin et al. described an oblique incision, starting 1.5 cm from the midline and proceeding latero-inferiorly to avoid the central glandular-free zone. The vertical incision technique is associated with less pain, less swelling, less scar formation, and less difficulty in eating when compared with the horizontal incision technique. There is insufficient evidence to support the superiority of one technique over the others, and the shape and the size of the incision can be considered a matter of preference. The incision shape includes elliptical, circular, linear, horizontal, vertical, and wedge shapes, and the incision length varies from a few millimeters to 2 cm.
\nAnother recommended modification is using loupe operation glasses to precisely excise the salivary glands without disturbing the direct underlying sensible nerves. The alternative technique to scalpel biopsy is the minor salivary gland punch biopsy. This biopsy can be performed by a single operator, and it is less expensive than classical scalpel biopsy. This technique consists of obtaining the biopsy from the buccal side of the lower lip, which is stabilized by the patient him/herself using a 4–5 mm punch, which permits the retrieval of a cylinder of tissue up to 8 mm in length. The punch biopsy is suggested because of the absence of risk to the patient and because of its simplicity. However, the punch biopsies do not provide enough material for the diagnosis of Sjögren’s syndrome. Moreover, the findings of this study strongly discouraged the punch technique for minor salivary gland lip biopsy and provided information on the superiority of the linear incisional biopsy in terms of neural damage [12, 13, 14, 15, 16].
\nBased on our own clinical experience, a 1.0–1.5-cm linear, horizontal incision of mucosa parallel to the vermillion border and lateral to the midline with the tip of a 15 scalpel is worth to recommend. The lower lip should be retracted and everted under tension to expose the inner surface and allow visualization of the minor salivary glands just to the depth of the mucosa. Local anesthesia injected submucosally with 0.5–1.0 ml of 1% lidocaine with 1:200,000 epinephrine is sufficient. The anesthesia hydrodissects and lifts the mucosa away from the salivary glands, provides delivery of local anesthetic directly to sensory nerve fibers, and temporarily displaces small vessels deep in the glands to promote hemostasis and visualization during the dissection. In this technique, both margins of incision should be gently crafted to access the submucosal layer. This stage of procedure can be performed using blunt-tipped iris scissors or a scalpel by spreading in a plane perpendicular to the mucosal incision and parallel to the direction of the sensory nerve fibers. This technique is fast, simple, and leaves a small scar. The linear incision secures a good adherence of wound margins and proper and fast healing. Unfortunately, this method is not effective in small amounts of salivary glands. Sometimes, it is difficult to find the sufficient amount of labial glands. Moreover, it may be difficult to harvest a sufficient number of labial salivary glands in atrophic mucosa of patients with long-standing SS. In these cases, the recommended method is a 1-cm lenticular incision of mucosa, lateral to the midline, and removal of the mucosa to uncover the submucosal layer and obtain a few adjacent salivary glands. This technique ensures good visibility into the operating field to avoid blood vessels and nerve injures. This incision provides adequate glandular tissue for diagnosis. The wound should be closed by a few nonresorbable, single, interrupted stitches. One very important issue is to harvest only labial salivary glands without muscular or other tissues. It is the most valuable specimen for histopathological examination, because it only includes glandular tissue. Additionally, this technique decreases the risk of nerve damage and postoperative pain and assures successful healing. Sensory nerve fibers are almost always visible just below the plane of dissection, and care should be taken to identify and preserve them. The next very important issue is not to puncture the labial glands to reduce the risk of mucous extravasation cyst formation. It is even better to remove all visible labial salivary glands from the operating field before suturing in order not to damage the glands or their ducts. Patients should also avoid taking steroids before the biopsy. The factors potentially contributing to a false-negative rate include the use of oral steroids that may result in immunosuppression and confound histopathologic results. The tissue specimens should be immediately placed in a wide-mouthed container, coded, and fixed in a generous amount of 10% formalin buffered saline for 24 h (Figures 1 and 2).
\nLinear incision and scalpel biopsy of labial salivary gland biopsy. A few labial salivary glands exposed and visible in the operating field.
Labial salivary gland specimen.
Labial salivary gland biopsy is an objective test of SS and plays a significant role in the diagnostic process. In fact, the presence of either anti-SSA/SSB seropositivity or a positive lip biopsy is a requirement for an individual to be classified as having SS. The microscopic confirmation of SS is based on the presence of focal lymphocytic sialadenitis (FLS) with a focus score ≥ 1 per 4 mm2 of glandular tissue. According to the revised American-European Consensus Group’s (AECG) classification criteria and the ACR classification criteria for SS, an LSGB is considered positive if minor salivary glands demonstrate FLS, with a focus score of 1 or more, as evaluated by an expert histopathologist. A lymphocytic focus is defined as a dense aggregate of 50 or more lymphocytes adjacent to normal-appearing mucous acini in salivary gland lobules that lacked ductal dilatation. Focal lymphocytic sialadenitis is applied to specimens that show the presence of 1 or more foci of lymphocytes located in periductal and perivascular locations. The foci can contain plasma cells, but these must be a minority constituent of the inflammatory infiltrate. The focus score can be calculated for those specimens showing the histopathologic appearance of FLS. The number of lymphocytic foci is then determined for all the gland lobules in a single tissue section. The focus score is then calculated as the number of foci per square millimeter of glandular tissue multiplied by four, which then yields foci/4mm2. A focus score of 1 equates to 1 focus/4 mm2. To determine the focus, a calibrated eyepiece grid or image analysis software with a closed polygon tool is used. FLS has to be distinguished from nonspecific chronic sialadenitis. The symptoms of nonspecific sialadenitis are mild to moderate acinar atrophy, interstitial fibrosis, and ductal dilatation, with lymphocytes and macrophages often scattered in the parenchyma, but not forming dense aggregates of 50 or more lymphocytes immediately adjacent to normal-appearing acini. In addition to the focus score (FS), two scoring systems for salivary glands are in use for the diagnosis and classification of SS. These systems are based on the presence of foci [7]. Grading according to Tarpley’s system involves destruction of acinar tissue and fibrosis (Table 1). Grading according to the Chisholm and Mason system is based on the presence of infiltrates from slight to one or more foci (Table 2) [16, 17].
\nGrade | \nDescription | \n
---|---|
0 | \nNormal | \n
1 | \n1 or 2 Aggregates | \n
2 | \n>3 Aggregates | \n
3 | \nDiffuse infiltrate with partial destruction of acinar tissue with or without fibrosis | \n
4 | \nDiffuse infiltrate with or without fibrosis destroying the lobular architecture completely | \n
Grading systems for salivary gland biopsies of Tarpley.
Grade | \nDescription | \n
---|---|
0 | \nAbsent | \n
1 | \nSlight infiltrate | \n
2 | \nModerate infiltrate or less than one focus | \n
3 | \nOne focus | \n
4 | \nMore than one focus | \n
Grading systems for salivary gland biopsies of Chisholm and Mason.
Focus: a cluster of 50 or more lymphocytes and histiocytes.
\nAggregate: approximately 50 cells (lymphocytes, plasma cells, or histiocytes).
\nFocus lymphocytic sialadenitis should be differentiated with other microscopic findings:
Nonspecific chronic sialadenitis NSCS
Sclerosing chronic sialadenitis SCS
Granulomatous inflammation
Infiltrates within normal limits
Marginal zone (MALT) lymphoma
Germinal center
Nonspecific chronic sialadenitis (NSCN) is characterized by scattered or focal infiltrates of lymphocytes, macrophages, and plasma cells that are not adjacent to normal-appearing acini and located in gland lobules that exhibit some combination of acinar atrophy, interstitial fibrosis, duct dilation, and luminal inspissated mucus.
\nSclerosing chronic sialadenitis (SCS) is an advanced stage of NSCS in which interstitial fibrosis, various patterns of chronic inflammation, and acinar atrophy predominate.
\nGranulomatous inflammation is present when there are clusters of CD68 positive macrophages, with or without occasional multinucleated giant cells and absent necrosis.
\nInfiltrates within normal limits can be diagnosed in minor salivary glands with normal appearing architecture and scattered plasma cells, but without acinar atrophy and few if any lymphocytes.
\nMarginal zone (MALT) lymphoma is diagnosed in minor salivary glands exhibiting diffuse lymphocytic infiltration with loss of glandular architecture and composed of sheets of CD20 positive cells without follicular distribution, few scattered CD3 positive cells, and few if any follicular dendritic (CD21 or CD23 positive) cells.
\nGerminal center presence is estimated in hematoxylin and eosin (H&E) stained sections by the presence of a cluster of relatively clear staining cells within a lymphocytic focus. More specific identification of germinal centers requires immunohistochemical staining for follicular dendritic cells with anti-CD21 or CD23 [4, 9].
\nThere is no standardization of labial salivary gland biopsies in SS, but there are several points of importance in LSGB. The first issue refers to a sufficient amount of glandular tissue. A reasonable compromise is four glands, although a minimum sized evaluable surface area (8 mm2) may be achieved with 2–3 glands. The largest possible area to be sampled would give the best results, but a larger operative field increases the surgical risk. On the other hand, some glands may be atrophic or damaged, and the volume of the material obtained through the biopsy should be sufficient to overcome this artifact and achieve a valid result. It is more recommended to evaluate multiple different lobules than to concentrate on a single abnormal lobule, which may not be typical of the entire gland. In routine management, H&E staining is used in order to determine these structures. For clinical trials, additional staining with CD21 as well as CD20 and CD3 is required. CD21 is a marker of follicular dendritic cells. Germinal centers should be reported and pathologists are advised to use caution in order to avoid overestimating germinal centers by relying solely on CD21. Furthermore, the distribution of the inflammatory cells in the gland may be uneven. Considering this uneven distribution, a single tissue section may result in underdiagnosis. While increasing the number of sections has the potential to reduce this problem, the optimal number of sections has yet to be determined. Some research suggests taking labial salivary glands at different depths from the same incision. Focus score can change significantly at different tissue depths within the minor salivary glands. Multiple sections for LSGB increase the diagnostic value and are more representative than a single section [7, 10] (Figure 3).
\nConfirmation of SS in LSGB. Focus score 4 (staining H&E, magnitude 10×).
\n
Differentiation of FLS with nonspecific chronic sialadenitis and sclerosing chronic sialadenitis
Severe acinar atrophy, interstitial fibrosis, and increase in fat cells in biopsy specimens
Age-related features in biopsy specimens (increased fibrosis, acinar atrophy, and adipose tissue
Lack of the measurement of the infiltrate [7]
There are also other histopathological features in the labial glands that are associated with SS and therefore might be indicative of this disease. Lymphoepithelial lesions (LELs) are striated ducts, which are infiltrated by lymphocytes with concurrent hyperplasia of the epithelial cells. They are found both in parotid and labial glands, and are more representative of parotid glands than labial glands.
\nSeverity of the LELs can be classified into three stages: stage 1: a partial LEL (affecting <50% of the epithelium), stage 2: developed LELS (affecting 50–100% of the epithelium), and stage 3: occluded LELs (fully circumferentially affected epithelium without lumen).
\nBesides LELs, the salivary gland of SS patients also presents a relative decrease in IgA + plasma cells. Several studies showed that a relative decrease of <70% IgA + plasma cells was more sensitive and more disease specific than the FS. Both features can help assess the salivary gland biopsies for the diagnosis of SS, especially when the FS in the biopsy is <1 [7, 19, 20, 21, 22, 23].
\nThe main alternative types of salivary gland biopsies in SS are parotid gland biopsy and sublingual gland biopsy. Parotid gland biopsy allows the clinician to monitor the disease progression and to assess the effect of an intervention treatment in SS. Parotid tissue can be harvested easily, repeated biopsies from the same parotid gland are possible, and the histopathologic results can be compared with other diagnostic results derived from the same gland, such as secretory function, sialographic appearance, and ultrasonography. Furthermore, parotid biopsy is better in the identification of lymphomas. The main possible complications are facial nerve damage, Frey’s syndrome, and development of sialoceles and salivary fistulae. A temporary change in sensation in the skin area of the incision is also a well-documented complication after parotid biopsy. Some patients might also develop preauricular hypothesis, although this is usually temporary. Furthermore, in SS, the salivary gland tissue is replaced by fatty tissue, and the risk of harvesting fatty tissue is thereby increased if done by inexperienced physicians. Parotid biopsy is particularly recommended in pediatric patients in whom SS is suspected and who have a negative minor salivary gland biopsy result. Incisional biopsy of the parotid gland overcomes most of the disadvantages of labial biopsy. When evaluating the parotid and labial biopsy, sensitivity and specificity are comparable, estimated to be 78 and 86%, respectively. Comparative studies suggest that both procedures—sublingual and parotid biopsy—retain a diagnostic potential comparable to that of lip biopsy and may be associated with lower postoperative morbidity. A comparison of sublingual gland biopsy with labial gland biopsy is better than that of labial gland biopsy, whereas the specificity of the latter is greater than that of the former. Sublingual gland biopsy is a relatively safe procedure, although the postoperative complications of sublingual salivary gland biopsy include ligaturing the Wharton duct, resulting from the placement of sutures, bleeding, and swelling in the floor of the mouth. Damage to the lingual nerve related to this biopsy technique has never been reported in the literature. No specialized histopathologic criteria have been established for the diagnosis of SS after a sublingual gland biopsy, and researchers merely used the criteria for labial gland biopsies [24, 25, 26, 27, 28].
\nThe rate of dry mouth in SS ranged from 41% at initial diagnosis to 84% 10 years after diagnosis. Hyposalivation or xerostomia measured by sialometry is one of the objective clinical criteria in the diagnosis of SS. According to the current classification criteria of SS, an unstimulated salivary flow rate of 0.1 ml/minute in sialometry gives a score of 1 to the weighted sum of 5 items. Dryness is also a subjective symptom of SS and is associated with many clinical implications. There are two possible sources of hyposalivation. The first possible origin is the presence of mononuclear cell aggregates around the ducts and acini of salivary glands resulting in functional and structural alterations of these glands and impairing their secretory function. In addition to the direct relationship between mononuclear cell infiltrations and secretory function, there are alternative pathways, such as induction of apoptosis of epithelial glands, alterations in aquaporin distribution, or inhibition of neurotransmission by antimuscarinic antibodies, lead to impaired glandular homeostasis. The second proposed hypothesis is the destruction of the duct and acinar cells of the salivary glands, and neural degeneration and/or the inhibition of nerve transmission. Hyposialia or decreased salivation can lead to xerostomia with clinical oral symptoms [29]. Dry mouth is associated with both objective and subjective signs and symptoms. The most common complaints related to dry mouth are presented in Table 3.
\nA dryness of the mouth in the morning and at night A frequent need to sip water A lip dryness, exfoliation, fissuring A predisposition to aphthae, ulcers, and mouth sores A burning sensation in the mouth A dysphagia A dysgeusia | \n
The most common complaints related to dry mouth.
In SS, the gingiva and mucosa of the oral cavity are not protected by salivary mucins, leading to less lubrication of the tissues. This can cause signs such as oral mucosal inflammation, mucosal sloughing, erythematous mucosa, and traumatic ulcers. Patients may demonstrate depapillation of the tongue in advanced cases. With time, the concentration of lactoferrin, potassium and cystatin C in saliva grows, while the amylase and carbonic anhydrase concentration drops. Decreased secretion of saliva, the loss of its buffer properties, and a lower concentration of saliva proteins such as histatins, mucins, IgA, and proteins rich in proline and statherins increase the risk of opportunistic infections, mainly fungal infections by Candida albicans. The prevalence of Candida albicans is >68% in patients with SS. Oral candidiasis may be asymptomatic or may show as fissured tongue, rhomboid mid-tongue, nonspecific ulcerations, prosthetic stomatopathies, or generalized candidiasis. It most often takes the form of chronic candidiasis, and less often of pseudodiphtheritic candidiasis. Candida infections often present as atrophic or erythematous candidiasis and are associated with a burning mouth, which is described by approximately one-third of patients with SS. In SS patients, C. albicans, C. tropicalis, C. glabrata, and C. parapsilosis are mainly isolated. Apart from oral candidiasis, a number of other changes and symptoms regarding the oral mucosa may occur (Table 4).
\nCandidiasis Angular cheilitis Simple cheilitis Exfoliative cheilitis Aphthae Aphthoid lesions Nonspecific ulcerations Paleness of the oral mucosa Staphylococcal infection | \n
Symptoms of oral mucosa in the Sjögren’s syndrome.
Angular cheilitis may be accompanied with fungal infection. In simple cheilitis, dominant manifestations are lip exfoliation and cracking, their proneness to bleeding, periodic swelling, and burning. The lesions are mostly limited to lip vermillion, less often labial mucosa or the facial skin around the vermillion is affected. In exfoliative cheilitis, thick brown keratin plaques are also formed. Skin redness over the lip vermillion and swelling are more often observed [29].
\nSS patients are predisposed to rampant caries and traumatic oral lesions. Lack of antibacterial salivary proteins results in severe tooth caries, especially on the unexposed tooth spaces. Rampant cervical caries is the most typical manifestation to SS.
\nThe lymphocytic infiltrations are representative for all salivary glands and have other possible consequences. Although the sicca syndrome prevails, in a clinical presentation, a bilateral parotid swelling induced by progressive lymphocyte infiltration leads both to ductal inflammation and acinar destruction in about 50% of patients. Recurrent swelling and inflammations of the parotid or submandibular glands in SS are well documented. Slow salivary flow, acinar destruction, and lymphocytic infiltrations predispose to inflammation and salivary gland enlargement. This enlargement should be distinguished from lymphomas. The most significant complication of SS is the development of lymphoproliferative malignancy, which occurs in about 5% of SS patients. Malignant lymphoma, particularly mucosa-associated lymphoid tissue (MALT) lymphoma, is relatively a frequent complication of SS with an incidence ranging between 5 and 10% and a median time from SS to lymphoma diagnosis of 7.5 years. Lymphomas accompanying SS can be confirmed by histopathological examination of salivary gland biopsy. The detection of germinal centers (GC) in salivary gland biopsy can be a very sensitive and predictive feature for lymphogenesis. Antigen-driven B cell selection normally takes place in GC within secondary lymphoid organs, but there is conclusive evidence that also ectopic GC in the salivary glands of SS patients allow affinity maturation of GC B cells with somatic Ig gene hypermaturation. Parotid gland biopsy is more recommended for diagnosis of lymphomas than labial salivary glands [7, 18, 19, 20, 21, 22, 23].
\nDryness of the mucosa of the upper respiratory tract is a predominant symptom and results in nasal, oropharynx, nasopharynx, laryngopharynx, vocal cord dryness, and dryness of the skin of the external auditory meatus. The main laryngological symptoms accompanying SS include the following:
Dry nose with congestion, crusting, and epistaxis
Dryness, crusting, or atrophy of the nasal mucosa
Soreness and/or dryness of the throat
Viscid secretions on the posterior pharyngeal wall and tenacious mucus over the vocal cords
Dry wax and a “milky” appearance of the tympanic membrane
Dysphagia
Hoarseness
Otalgia
Tinnitus
A chronic dry cough
Dyspnea
Gastrotracheal reflux
Otitis externa
Myringitis
Sensorineural hearing loss
Facial hypaesthesia and trigeminal nerve neuropathy, and multiple cranial neuropathy [30, 31, 32, 33]
Other possible laryngological manifestations of SS are early and progressive hearing loss and symptoms related to neuropathy of the eighth cranial nerve. Approximately, a quarter of patients suffer from high-frequency hearing loss of cochlear origin, as detected by impedance audiometry or auditory brainstem procedures. The immunologic theory of sensorineural hearing loss (SNHL) in SS is based on antibody activity and cytotoxic T-cell-mediated apoptosis in the inner ear. It has been suggested that these autoantibodies induce thrombosis in the labyrinthine vessels, thereby causing damage to the inner ear, resulting in SNHL. The majority of primary SS patients exhibit hearing impairments of cochlear origin, principally at high frequencies. Sensorineural damage may be attributable to vasculitis or neuritis, or may represent an ototoxic effect of the drugs used to treat primary SS. Although there is no evidence of damage to the central auditory pathways in SS, these patients tend to have a higher prevalence of sensorineural hearing impairment compared with the general population. Idiopathic hearing loss may represent the initial manifestation of systemic vasculitis, including SS. The pathomechanisms underlying cranial neuropathy in SS have not yet been explained, except for trigeminal neuropathy due to ganglionopathy. The two possible mechanisms, vascular origin with damage to the vasa nervorum, and an immunologic cause inducing lymphocytic infiltration of the nerve have been suggested in nerve palsies related to SS. Vasculitis in peripheral neuropathy and ganglionopathy in trigeminal or ataxic neuropathies have been reported as the main pathogenic etiology. The rapid and almost complete recovery from nerve palsy after therapy with corticosteroids and azathioprine suggests that lymphocytic infiltrate, rather than a vasculitic process, was the cause of cranial neuropathy in SS [33, 34, 35, 36, 37, 38, 39, 40].
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\\n"}]'},components:[{type:"htmlEditorComponent",content:'Copyright is the term used to describe the rights related to the publication and distribution of original Works. Most importantly from a publisher's perspective, copyright governs how Authors, publishers and the general public can use, publish, and distribute publications.
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