Iris Publishers-Open access Journal of Otolaryngology and Rhinology | Evolution of Hearing

 

Authored by Rohit Mehrotra*

Introduction

Evolution of hearing dates back to some 250 million years ago along with mammalian evolution. To understand the evolution of hearing, one needs to understand the basic mammalian evolution first. Beginning of mammal evolution first seen in Triassic period about 230 million years ago, during which all land vertebrates developed tympanic middle ear. Mammals with their various characteristic traits, arose during the Triassic period some 250 million years ago and quickly gave rise to number of separate lineages. From Triassic, evolved the jurrasic (200 million years ago) followed by the cretaceous (100 million years ago). Multituberculata (middle of lineages) formed the major group in creataceous. Cenozoic evolved from cretaceous (50 million years ago). Monotremes (egg laying mammals) forms the major group here. The THERIANS (modern mammals that does not lay eggs) split into marsupials and placentals during the cretaceous period and are the dominant creatures today.

Hearing evolution follows the ear structures evolution which started in the dryolestes (late jurrassic mammals) and continued to its present state. In other words, dryolestes were the combination for ancestral uncoiled cochlea and the neomorphic bony cochlear from which marsupials and placentals ear structures evolved. Earliest mammalian cochlea were only about 2mm long and contained a lagena macula. In multituberculate and monotreme mammalian lineages, the cochlea remained relatively short and did not coil. In modern therians (placental and marsupial mammals), cochlear coiling develops, first showing in late jurassic mammals featuring 270-degree coiling and length of 3mm. High frequency hearing with fully coiled cochlea seen first in Cretaceous.

Beginning of mammal evolution first seen in Triassic period about 230 million years ago, during which all land vertebrates developed tympanic middle ear. Due to simultaneous changes in the jaw joint, number of bones at the back of jaw joint were freed and established a middle ear containing three ossicles. Multituberculates (middle of lineages), a successful group of mammals had robust middle ear bones and uncoiled short cochlea(2-6.5mm) with lagenar macula. Monotremes (egg laying mammals) had uncoiled, relatively short (4.4 to 7.6mm length) cochlea. Soft tissues do not fully conform to shape of bony canal and coiled in opposite direction near the tip. Middle ear is very stiff and hearing restricted to lower and middle frequencies. Audiograms were V shaped, centered at 5 KHz or U shape with rapid loss of sensitivity below 3 KHz and above 16 KHz. Presence of lagenar macula at apical end of monotreme cochlear canal correlate with its likely presence in multituberculate cochlea at one end and with modern avian and reptilian cochleae at other end.

Coiling of cochlea is for efficient innervations and blood supply. Elongation of cochlea is related with increasing resolution of sound frequency. Curved gradient of coiled cochlea focuses acoustic energy towards apex (most sensitive for lower frequency). These new changes are related with earliest diversification of metatherians and eutherians in cretaceous leading to increase hearing in cenozoic and living marsupids and placentals. First report of coiled cochlea was seen in Dryolestes leiriensis (late Jurrasic mammal), 150-millionyear- old fossil in Cladotheria clade. Dryolestes are near relative to modern marsupials and mammals. Detailed evolution of inner and middle ear as well as auditory pathways are explained below.

Evolution of Inner Ear Structures

The earliest mammalian cochlea were smooth bony walled canals with no firm contact to soft tissue. In late jurrasic fossil mammalian cochlea, bony canal became integrated into soft tissue. Both primary and secondary laminae were present supporting the inner and outer edges of basilar membrane and cochlear ganglion was enclosed within the bony wall. Nerve fibres pass through the clear openings in the bone to enter organ of corti. The development of primary osseous spiral lamina probably resulted from coiling of cochlear canal.

Thus during the Jurassic, the ancestors in therian mammal lineage increase the length of their cochlea moderately, continued the partial coil, integrate soft and bone tissues and reduce the number of cells across the organs The eventual loss of lagena macula from cochlear apex at some time during the cretaceous enabled therian mammals to reduce calcium concentration in cochlear endolymph to micromolar levels leading to evolution of tectorial membrane (which was highly sensitive to ionic environment), mechanosensory channels of hair cells and perhaps the properties of Prestins. The evolution of acetylcholine receptor systems that controls the outer hair cells afferent feedback correlates with evolution of prestins in therians. Prestins gradually evolved into more effective components of motor system specialized for effects in a useful range of cell potentials.

The earliest land vertebrates had an auditory papilla that rested on solid tissue and had an otolith covering. In amphibians, the otolithic membrane was replaced by tectorial covering free of otoliths. In all the following lineages, freely suspended basilar membrane originated. In other lineages, the basilar membrane showed partial tuning, with only moderate frequency selectivity. Only in Therian lineage did a bony support system originate for basilar membrane which was later accompanied by sharp frequency selectivity of oscillations of basilar membrane /organ of corti complex .

First report of coiled cochlea was seen in Dryolestes leiriensis (late Jurrasic mammal), 150-million-year-old fossil in Cladotheria clade. Dryolestes are near relative to modern marsupials and mammals. Cochlea is 3.3mm long and 270 degree coiled. Bony interior structure was the newer development seen different from the primitives ones. CT scans showed the presence of curved track of fine cochlear foramina with each foramina being a separate entrance of individual fascicle of cochlear nerve (Foramina forms sieve like cribriform plate in internal acoustic meatus in marsupials).

In Dryolestes, primary bony lamina and its associate ganglion canal extend along basal half turn (180 degree) of cochlear canal but not reaching apical quarter cochlear turn whereas in marsupials and placentals, the primary bony canal reach to apex of entire coiled cochlea. The more primitive cochlea was a simple tube, straight or slightly curved, with a single large opening for cochlear nerve in internal acoustic meatus, without any interior bony structures for cochlear innervations. Difference with Monotremes was the presence of bony cochlear ganglion canal and primary bony lamina for nerve fibres in Dryolestes. Similarity being the presence of cochlear nerve foramina of sieve-like cribriform plate. Hence Dryolestes were the combination for ancestral and uncoiled cochlear canal and the neomorphic bony feature of cochlear innervations, from which the more derived and sophisticated ear structures of marsupials and placentals developed .

STRIP 2 (Striatin interacting protein 2) plays a functional role in the first synapse between inner hair cells and nerve fibres. When at the cochlear sensory epithelium, they found a significant reduction in auditory nerve synapses. STRIP 2 underwent strong positive selection in mammalian lineage and played important role in inner ear physiology. Extensive evolutionary remodeling that this gene underwent in mammalian linage provided an adaptive value. Genes responsible for changes were Neurogenin-1 (Ngn 1) for the progenitor determination of ganglion neurons, Neuro D(neurod1) for forming and maintaining the ganglion neurons, brain derived neurotrophic factors (BDNF) and neurotrophin 3 (NT3) for supporting the ganglionic innervations to hair cells. According to phylogeny, formation of cochlear ganglion by co-option of such genes and genes for related epithelio mesenchyme interaction, had occurred first in evolution in Cladotherian clade in the middle Jurrassic.

Changes in Middle Ear

Early vertebrates had an otic structure, indicating the presence of stapes in the matrix of posterior underside of skull. Stapes forms the only link between palate and otic region of brain case. Palate was potentially mobile and was involved with buccal ventilation. When the palate bone was released from this role by development of alternative mechanisms, stapes could specialize as purely auditory ossicle. Further adaptations for eating, including versatile jaw movements and more precise dental occlusion, have been interpreted as directly setting the stage for mammalian adaptation of posterior of posterior jaw bones for hearing. Over millions of years, bones with integral part of jaw support system in early reptiles, lost their eating function as reptilian jaw foreshortened with new articulation leading to reduction in size and form the three bone ossicular chain common in modern mammalian middle ear.

Early mammal tympanic middle ear was restricted to poor sensitivity and to low frequency, derived by presence of very short papillae, the stapes size, bony component connecting quadrate to inner ear and connection of middle ear to lower jaw. Malleus remained attached to lower jaw. In early mammal Morganucodon, the middle ear had function in jaw support and was not sufficiently evolved to be termed as transitional middle ear. For the first half of evolutionary history, mammals did not hear high frequencies. In Monotremes and multituberculates, upper limit remained below 20KHz and gradual increase in upper limit of hearing to 20KHz. After full coiling of cochlea achieved, middle ear evolved to freely suspended form of therians and Prestins evolution was a significant leap forward, high frequency hearing evolved and today represented in therian cochlea with length between 7 mm(mouse) and >50 mm(blue whales).

Auditory Pathway Changes

Humans had the smallest auditory system per brain size, owing to large brain size compared to auditory system. This small ratio was secondary result of expansion of other, non-auditory parts of brain with expanded occipital and temporal lobes. Medial olivary nucleus, part of superior olivary complex is relatively large in humans than in cats and other mammals, due to potential, based on large head size, for localization of sound by inter aural analysis of low frequencies. In contrast, greatest development of lateral olivary nucleus occurs in echolating mammals, bats and porpoises but remains smaller in primates, monkeys and apes owing to be related to limited range of audible frequencies, particularly in higher ranges. In echolating animals, large size of nucleus serves as hearing range extending over 100 KHz. The reduction in humans correlates with high frequency limit at approximately 18KHz.

Small cell cap of the cochlear complex in comparison to all other nuclei, showed pronounced reduction in humans as an implication of less diversity and complexity in auditory processing at subcollicular levelin human brain. These reductions viewed as biological adaptation of auditory system. Earliest mammals exploited nocturnal niches, which were relatively free of large, diuran reptiles and therefore, hearing and smell were more useful at night than vision. This lead to development other adaptation of homoiothermy (constant internal body temperature) for better heat retention at night, with superficial insulation which required a high sustained activity level, accompanied by stable metabolism rate. This in turn required regular efficient ingestion of food leading to continous changes in dental and jaw morphology and articulation, further leading to changes in middle and inner ear.

Human Hearing Evolution

Five parameters of hearing-high frequency cutoff, low frequency sensitivity, lowest threshold, best frequency and total area of audible field were compared and studied.

High frequency hearing

Range of high frequency hearing extends from a low near 18 KHz for man to about 120 KHz for dolphin and bat. The striking difference in upper limits of frequency is due to presence of ossicular linkage in middle ear of mammals. Amphibians, reptiles and birds have only single functional bone in middle ear for sound conduction from tympanic membrane to cochlea (columella or stapes) and three bones in lower jaw (dentary, angular and articular) whereas mammals have three bones in middle ear and one in lower jaw(dentary). Ossicular linkage acts as simple lever providing mechanical transformation that matches impedance of air to cochlear fluid impedance. Since high frequency vibrations require this matching of impedance, hence evolution of middle ear ossicles was detrimental for radical difference in upper limit of hearing between mammals and non-mammals.

Selective pressure for accurate sound localizations have been the driving force behind the final stage in evolution of mammalian variety of middle ear. In man evolution, from the early Eocene onward, progressively wider set ears released man’s ancestors from selective pressure for high frequency hearing resulting in regression of upper limit. Mammals that have small binaural time disparities, either because of close set ears or marine environment, increase their accuracy in localizing sound source by maximizing the availability of binaural spectra disparities which in turn is through sensitivity to high frequency. High frequency hearing is a result of selective pressure for accurate and instantaneous localization of source of brief sounds.

Low frequency sensitivity

1. It is not a primitive mammalian character.

2. Animals in man’s line of descent showed marked improvement in low frequency hearing.

3. Increase in low frequency sensitivity, though almost linera across the phyletic sequence, was probably not steady in time.

4. Low frequency hearing improved slowly until the Paleocene, then quickly through the Eocene- then remained unchanged till present.

Lowest threshold

1. Large differences in general sensitivity among animals occur between levels at lowest stages (i.e. opossum-hedgehogtree shrew levels phyletically; cretaceous to Paleocene, historically). This difference might be related to rigidity of tympanic suspension. The ring of bone (ectotympanic) that supports eardrum is incomplete in opossum and more complete in tree shrew. This progressive encirclement of tympanum is accompanied by development of sturdy auditory bulla. Lack of this rigid support for tympanic membrane in primitive mammals results in loss of energy during first link in transmission of air movements to cochlear fluids and resultant insensitivity.

2. Frequency of lowest threshold has declined in man’s lineage- the greatest drop probably occurring during the Eocene.

Best frequency

1. High frequency hearing is related to direct effect of selective pressure for accurate sound localization. Animals with a high best frequency always have a high upper limit of hearing, and animals with high upper limit usually have a high best frequency.

2. The uniquely mammalian capacity for high frequency hearing is probably the result of selective pressure for sound localization.

Area of audible field

1. Average audible field of mammals is larger than birds and reptiles owing to mammalian capacity for high frequency hearing.

2. Man’s ancestors gradually attained more extensive audible fields by increasing their sensitivity to low frequency until the focene. Since that time the audible field has slightly regressed due to loss of high frequency hearing.

3. The total area of audible field increased until the Eocene and has decreased since then. The increase at early stages was due to increase in low frequency sensitivity while the high frequency remains unchanged. The decrease at later stages was due to loss of high frequency sensitivity while low frequency sensitivity remained unchanged.

The Lineage of Modern Amniotes and their Characteristic Hearing Organ Morphologies

Four basic types of amniote ear refer to mammalian, avian, lizards and turtle. Except for turtles all groups developed sensitivity to high frequencies.

Turtles have the least specialized hearing organ, resembling early stem reptiles. Hair cells are unspecialized, innervated by both afferent and efferent nerve fibres and respond to low frequencies. The stereovillar bundles of all hair cells are uniformly oriented with weak morphological gradients. The ion channel compliment of hair cell membranes create electrical resonances at preferred frequencies. The basilar papilla was the first hair cell organ to form over a moveable membrane (basilar membrane, BM). BM shows no special frequency selectivity in turtles and lizards. Lizard auditory epithelia varies from <100 micrometers to >2mm and in number of hair cells from <60 to >2000. Hair cells may be covered by a continuous tectorial membrane (TM), by a TM that is divided into chain of sallets, or have no TM at all. Lizard papillae show two hair cell types. One papillar area contain hair cells with greater basal diameter, large numbers and larger afferent nerve fibres and an efferent innervations. All have same (abneural) orientation. Functionally, these cells respond to low frequencies (below about 1 KHz). The second type is smaller in size, smaller and fewer afferents, and complete lack of an efferent innervations. All have groups of neurally and abneurally oriented hair cell bundles (bidirectional orientation). Cells respond to frequency above 1 KHz, with an upper limit of 4KHz and micromechanically tuned. Evolution of tympanic middle ear initiated the development of high frequency hair cell areas of stem lizards.

Birds and mammals: Both have specialized hair cell populations located across the width of papilla, essentially at all frequency locations and within a continuous tonotopic organization. Both groups have independently-developed responses to high frequency, in some birds upto 10KHz, in some mammals even beyond 100 KHz. Papillar elongation was generally more extensive than the maximum of 2mm in lizards. Owl papillae reach 11mm and whale papillae 105mm. the coiled cochlea, which evolved after divergence of marsupial placental line in late Mesozoic, was a mechanism of accommodating a long papilla. In mammals, basilar membrane frequency selectivity is identical to that of inner hair cells and afferent fibres. Response is feature of entire organ, and no component is separable without reducing sensitivity and selectivity. This linking is not well developed in birds because the hair cells that connect to most of the afferent fibers are not over free BM, but over the limbus.

To summarise, it can be said that most important changes in cochlear mechanisms during phylogeny were initiated by changes in middle ear. This led to predominance on micromechanical tuning, a profound elongation of papilla, and the specialization of hair cells to generate a division of labor in birds and mammals.

Conclusion

Evolution of hearing started 250 million years ago along with mammalian evolution and continued during the human evolution. Inner ear structures as well as middle ear structures continued to evolve to its present state in humans and other vertebrates. Simultaneously hearing also evolved correlating with the changes in ear structures. Thus, three parallel series of development over 150 million years ago led to high frequency hearing only in most modern therian cochleae:

1. The initially stiff middle ear gradually became lighter and more freely suspended.

2. The initially very short cochlea was gradually elongated and the soft tissues incorporated bony support elements of basilar membrane and thus better matched the middle ear impedance. The cochlea coiled and eliminated the lagena macula.

3. Prestins gradually evolved into more effective motor system components specialized for effects in a useful range of cell potentials with further specialization in late evolving echolating species.

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Iris Publishers-Open access Journal of Otolaryngology and Rhinology | Hearing Loss Gene Panel Testing: Considerations for Clinical Practice

 

Authored by Alpana M Kulkarni*

Abstract

Hearing loss gene panel testing has now been introduced into mainstream NHS (National Health Service) as genetic test which can be offered to families with child with hearing loss. Clinicians requesting this test need to have an understanding of its sensitivity, specificity of this test and its limitations and challenges. They also need to be aware of the ethical issues which may arise by undertaken this test and counsel families accordingly before requesting this test.

Keywords: Sensorineural hearing loss; Gene panel testing

Introduction

1 in 1000 children is born with sensorineural hearing loss. 2.7 in 1000 children develop hearing loss in late childhood and the incidence increases to 3.5 in 1000 in adolescence [1]. Genetic diagnosis of hearing loss is important from prognostic point of view, offering advice for suitable intervention such as cochlear implant in Connexin 26 deafness, or oral speech with cochlear implant in Usher’s syndrome due to retinitis pigmentosa. Around 50% of hearing loss is genetic in origin and of these at least 20% is syndromic and 80% is non-syndromic [2]. Syndromic loss can be identified with single gene testing using Sanger sequencing approach, for example EYA1 mutation in Branchio-Oto-Renal syndrome. This condition clinically manifests through phenotypical changes such as preauricular pits or tags along with sensorineural or mixed hearing loss. Similarly, testing for Connexin 26, which is the commonest cause of non-syndromic hearing loss (NHSL) and responsible for ≤50% of non-syndromic autosomal recessive loss, is currently requested by single gene testing in the UK [3]. However, if single gene testing is negative then no conclusion is reached about the aetiology of the deafness. In some cases, sequential single gene tests may be carried out for different genes but this is expensive.

Genomics England was initially set up to deliver the ‘100,000 Genomic Project’ and further funding has been given to expand the UK’s NHS biobank to sequence one million whole genomes in the next five years. Thus, the genetic laboratory services in the UK have rapidly expanded to meet this demand. With next generation sequencing, also called ‘massive parallel sequencing’, it would be possible to test for millions of DNA fragments in one reaction. Thus, technology which target and enrich specific areas of the genome coupled with massive parallel sequencing is now the new norm for genetic testing for hearing loss. The genetic labs are now offering non-syndromic and syndromic hearing panel testing using this technology. With the hearing panel testing, currently more than 100 genes (both non syndromic and syndromic) can be tested for any pathologic variants and with turnover time of 12 to 14 weeks, a genetic diagnosis can benefit a child and the family with hearing loss.

What is in the literature?

Shearer, et al. [2010] [4] tested 9 patients with hearing loss to evaluate the feasibility of massive parallel sequencing by testing the exons of all genes involved in NSHL. 605 single nucleotide polymorphisms (SNP) were genotyped by Sanger sequence to test the sensitivity and specificity of the parallel sequencing technologies. Causative mutations were identified in all positive but not negative controls indicating that this technology can be used successfully to identify mutations in hearing loss [4]. Subsequently many studies have demonstrated the usefulness of this methodology.

Shearer, et al. [2016] carried out a literature review to evaluate the use of new genetic techniques for genetic diagnosis of hearing loss. They studied 20 studies which included 426 control samples and 603 patients with unknown hearing loss. Control analysis showed >99% sensitivity and specificity for clinical use of massive parallel sequencing tests. They identified that the overall diagnostic rate was 41% (range of 10% to 83%) and it varied due to factors, such as inheritance and pre-screening prior to testing [5]. A further study by Cabanillas, et al. 2018 [6] developed a panel with 199 genes including syndromic and non-syndromic sensorineural hearing loss and demonstrated a diagnostic yield of 42% in patients with sensorineural hearing loss [6].

It is important however to develop the right panel of genes and precise targeted genomic areas to improve the sensitivity, the challenges are to interpret the variants with appropriate clinical data. So, it is vital that there is a close collaboration between the Clinician who is requesting the test with the genetic lab scientist. A comprehensive medical and family history should be provided with the request. Study by Christina M Sloan Heggen, et al. [2016] [7] performed comprehensive clinical genetic testing with massive parallel sequencing on 1119 sequential patients. Yield of the genetic cause of hearing loss was found in 39% (440) patients. The diagnostic yield was highest considerably based on phenotype and was highest for patients with positive family history [7].

Personal practice

In my clinical practice I have instigated this panel testing as second line in families where more than one child has been identified with non-syndromic autosomal recessive hearing loss. So far three families each with two affected siblings have been tested and they all have been identified with pathogenic mutations. It will be useful to have an algorithm depending on the characteristics of the Clinicians case load based on ethnic groups, family history and phenotypical presentations. For example, if an MRI of the inner ears shows widened vestibular aqueduct then single gene testing with Pendrin gene is more appropriate, whereas if two children are affected in the same family with normal parents and normal MRI, then hearing panel testing should be instigated (see attached Algorithm as an example).

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Iris Publishers-Open access Journal of Otolaryngology and Rhinology | Antimicrobial Photodynamic Therapy for Treatment of Refractory Chronic Rhinosinusitis: A Pilot Study

 

Authored by Amin Javer*

Abstract

Background: Inflammation in refractory chronic rhinosinusitis (RCRS) is complicated by persistent microbial colonization resistant to medical treatment. Antimicrobial photodynamic therapy (aPDT) has been shown to be effective in eradicating in-vitro biofilms of chronic rhinosinusitis microbes and reducing mucosal inflammation. It is an emerging tool for treatment of RCRS.

Objective: To evaluate the safety and efficacy of aPDT in a cohort of our patients diagnosed with RCRS.

Study design: Retrospective case series.

Materials and methods: Patients with persistent inflammation and suspected chronic biofilm within the sinuses despite appropriate medical and surgical treatment were treated with aPDT using a diode laser and methylene blue (as photosensitizer) on an outpatient basis. Patient outcomes were reviewed at 3 and 6 months post-aPDT. Endoscopic sinus scores and adverse events were recorded at each visit.

Results: Sixteen patients were recruited and treated with aPDT. Of these, 14 patients completed their follow-up visits. Forty-three sinuses (5-frontal, 21-ethmoid, 16-maxillary, 1-sphenoid) in the fourteen patients (13-females, 1-male) were treated (Mean: 2.7 sinuses/patient per treatment). The average age of patients was 53.7 years. Nine of the fourteen patients treated showed improved endoscopic scores in the sinuses after 6 months. (Mean MLK Score difference±SD: 1.81±2.76). Three patients expressed minor and transient adverse events (slight bleeding, stinging sensation) immediately after the procedure and none at 3 and 6 months. The clinicians’ experience with the procedure was satisfactory.

Conclusion: Patients with CRS can be safely treated with aPDT on an outpatient basis. These early results, while promising, will require validation in prospective clinical trials.

Keywords: Refractory Chronic Rhinosinusitis; Photodynamic therapy; Biofilm; Methylene blue

Abbreviations: aPDT: Antimicrobial photodynamic therapy; AFRS: Allergic fungal rihinosinusitis; CRS: Chronic rhinosinusitis; CRSwNP: Chronic rhinosinusitis with nasal polyps; CRSsNP: Chronic rhinosinusitis without nasal polyps; EDTA: Ethylenediaminetetraacetic acid; FESS: Functional endoscopic sinus surgery; MAD: Mucosal atomization device; MLK: Modified Lund-Kennedy; MRSA: Methicillin-resistant Staphylococcus aureus; QoL: Quality of life; RCRS: Refractory chronic rhinosinusitis

Introduction

Rhinosinusitis is among the most common conditions in North America, affecting more than 31 million people annually [1,2]. Chronic rhinosinusitis (CRS) prevalence, however, is difficult to extrapolate because of the heterogeneity of its presentation and imprecise diagnosis [3]. Refractory chronic rhinosinusitis (RCRS) is defined as persistence of signs and symptoms of CRS despite technically adequate functional endoscopic sinus surgery (FESS) and adequate postoperative medical management [4]. RCRS has significant detrimental health effects such as reduced quality of life (QoL), fatigue, sleep disturbance, sexual dysfunction, olfactory dysfunction and depression [5]. The summation of these effects has a profound impact on productivity. It is estimated that the annual productivity cost associated with RCRS is $10,077.07 per patient [6].

Several pathophysiologic mechanisms for persistent CRS disease have been described. One of these is persistent bacterial biofilm formation secondary to a microbial dysbiosis within the affected sinonasal cavity [7]. Biofilms are a complex organized community of germs that adhere to the mucosal surface and surrounded by an extensive extracellular polymeric substance (glycocalyx) that is composed primarily of polysaccharides [8]. They begin their life cycle as independent bacteria, which become sessile and initiate the biofilm formation process by adhering to a surface and forming microcolonies [9]. Biofilms allow bacteria to evade host defenses and decrease susceptibility to antibiotic therapy. They also cause a deliberate release of planktonic bacteria, resulting in implantation and population of new anatomic locations [10]. Several organisms have been implicated in the formation of biofilms including: Staphylococcus aureus, Pseudomonas aeruginosa, Streptococcus pneumoniae and other gram-negative rods [11]. Due to the unique properties of biofilms, new directions in therapy are constantly being sought for the treatment of patients with RCRS secondary to microbial dysbiosis and biofilm formation [12].

Antimicrobial photodynamic therapy (aPDT) is a novel treatment modality showing promise in the treatment of bacterial biofilms. It has been applied successfully in dentistry [13], wound infections [14], oncology [15,16], dermatology [17] and gynecology [18]. A range of photosensitizing molecules have been used with phenothiazinium dyes (methylene blue, toluidine blue, and PP904) being the most common [19]. Investigations of aPDT in vitro have shown it to be lethal against all classes of microorganisms: gram-positive and gram-negative bacteria, fungi, viruses, parasites and even spores [20]. In addition to its antimicrobial effects, PDT also demonstrates a marked anti-inflammatory effect, and has also been shown to effectively treat the polymicrobial biofilms involved in CRS [21-23]. We describe a pilot study on the safety and efficacy of aPDT in the management of CRS patients who are refractory to appropriate medical and surgical therapy.

Materials and Methods

Patients

Ethics approval for this study was obtained from the Providence Health Care Research Ethics Board of the University of British Columbia (Ethics number: H15-01411). Electronic medical charts were reviewed of all patients treated with aPDT between November 2013 and March 2015 at our tertiary rhinology centre.

Patients were included in this review if they had undergone at least one aPDT treatment at our centre. Patients are only offered aPDT if they had already received complete FESS at least 6 months prior and also demonstrated recalcitrance to appropriate adjunctive medical therapy. Appropriate adjunctive medical therapy at our centre includes at least 18 weeks of topical budesonide (Pulmicort ®, Astra Zeneca,) 0.5mg/2ml delivered via impregnated nasal saline irrigation or the mucosal atomization device (MAD), 3 weeks of culture-directed oral antibiotics or antifungals (Itraconazole) as necessary for more than 2 discrete infections per year, at least 6 weeks of low-dose macrolide therapy, and oral steroids (Prednisone 0.5mg/kg 2 week taper).

Patients with sinonasal tumors, autoimmune and systemic inflammatory diseases affecting the upper airway were excluded. Patients receiving aPDT were followed up regularly post-aPDT with detailed endoscopic examinations and graded using the modified Lund-Kennedy (MLK) endoscopic scoring system. The scores were recorded at baseline and at each follow-up visit after aPDT treatment. Digital images of the sinuses were recorded at each visit. Adverse events reported in the immediate post-procedure period were also recorded.

The device used for the aPDT was the SinuwaveTM Ceralas E® (Ondine Biomedical). Following endoscopy, nasal debridement was performed if needed and bacterial sinus culture was collected via a culture swab (Starswab II®, Starplex Scientific Inc., Ontario, Canada) or specimen trap (Argyle™ Covidien, MA, USA). Three milliliters of the photosensitizing agent (methylene blue) was then sprayed into the affected sinuses using a curved suction under direct endoscopic visualization with a 3mm 30º rigid endoscope. The Sinuwave Light Delivery Catheter (Figure 1) is made of a malleable yet firm material that is bent to facilitate the introduction into the sinus to be treated. The distal end of the catheter houses a balloon that surrounds the laser projecting tip. Inflation of the balloon facilitates equivocal assortment of the photosensitizing agent on the sinus wall mucosa, mechanical evacuation of purulent or mucinous discharge that is located in the sinus as well as equal distribution of the laser light to the surrounding mucosa. The catheter is introduced under endoscopic guidance, occasionally under topical anesthesia (Lidocaine 10% spray, 20mg per nostril), into the sinus that is about to undergo the treatment. The balloon is inflated with saline. The amount of saline used is determined by the volume of the sinus cavity. As the balloon inflates, it starts to swell in a retrograde fashion out of the ostium and the resistance to balloon inflation increases. The inflation is carried out via a port located at the proximal end of the catheter. The catheter is connected to the Sinuwave Laser Console. Once in place and well inflated, the sinus is illuminated using a low-level laser at 670 nm wavelength (Figure 1). The laser power (0.5W to 4.90W) is calibrated according to the amount of saline (<1ml-15ml) used to inflate the balloon, as established by the manufacturers protocol. Once activated, the catheter is left in place for a duration of 4 minutes. At the conclusion of treatment, the balloon is deflated and removed. The sinus cavity is then re-examined and evaluated for any immediate adverse reactions to the treatment.

Statistical analysis

Demographic and baseline characteristics were extracted from patient charts and recorded for each subject. Demographic data included age (years), sex, history of smoking and ethnicity. Baseline characteristics included diagnosis, history of sinus surgery, endoscopic sinus score (MLK), endoscopic imaging, and culture results collected prior to receiving aPDT treatment. The number of sinuses treated per session was also recorded. Categorical, explanatory variables were summarized by frequency and absolute proportions. Continuous, explanatory variables were summarized by mean and standard deviation. The primary outcome variable was endoscopic mucosal scores evaluated before and after treatment. The outcome variable was recorded as a continuous, numerical outcome and summarized by mean and standard deviation. Data were collected, de-identified, and stored in a securely encrypted electronic database.

Results

Sixteen patients were recruited and treated with aPDT at our centre during the review period (November 2013 to March 2015). All of the demographic data is summarized in (Table 1). Of these, 14 patients were followed up for at least 6 months after the procedure. Two patients did not complete 3 months of follow up, however they were followed up at 6 months and no adverse effects were noted. Clinical and baseline characteristics are summarized in (Table 1). Two patients received 2 successive aPDT treatments while the others (n=12) received only one treatment. Forty-three sinuses (5-frontal, 21-ethmoid, 16-maxillary, 1-sphenoid) in the fourteen patients were treated (Mean: 2.7 sinuses/patient per treatment with a total of 16 treatments). Eleven (79%) of the patients were being managed for chronic rhinosinusitis with nasal polyps (CRSwNP) and 3 (21%) were managed for chronic sinusitis without nasal polyps (CRSsNP). Nine (64%) of the patients had also been diagnosed with allergic fungal rhinosinusitis (AFRS) using the Bent and Kuhn diagnostic criteria [24]. The average number of FESS procedures undergone by the patients prior to their initial aPDT session was 1.14±0.4 (mean±SD).

Nasal cultures done prior to the aPDT showed various classes of microbes; fungi (Aspergillus sp. and Rhizopus), gram-positive cocci (S. aureus, S. epidermidis and S. pneumoniae) and gram-negative bacilli (H.influenzae, Klebsiella and E.coli). The mean difference (±standard deviation) in the pre and post endoscopic scores was 2.38±2.96 (range: -2-34 points) using the MLK scoring system. Endoscopic sinus scores taken at 3 and 6 months showed a reduction in inflammation from baseline in 9 of the 14 patients (Table 2). Regarding safety of the procedure, no major complications were observed. Out of 43 sinuses intervened, 3 reports of transient effects were identified. The adverse events included slight bleeding, stinging sensation in the sinuses and a slight headache during the procedure. None of these events required medical intervention or persisted for any length of time beyond the clinic visit.

Illustration: case E

An 89-year-old male being managed for RCRS with nasal symptoms for over 2 years. Current treatment included topical intranasal steroids, saline irrigation, multiple episodes of long-term low dose macrolide antibiotics and oral steroids. He presented with a history of recurrent sinus infections, nasal polyposis, hyposmia and long-standing nasal obstruction. He underwent FESS 9 months prior to his first aPDT procedure. Intra-operative findings revealed multiple grade 3 polyposis and purulent discharge in all sinuses. His immediate postoperative management was uneventful. Post-operatively, he began to suffer from recurrent episodes of sinus infections. He continuously cultured S. aureus from his sinuses at every visit despite antibiogram guided oral and topical antibiotic and anti-inflammatory treatment for his CRS.

He received bilateral aPDT to all sinuses, and showed an immediate improvement in endoscopic sinus scores. His MLK mucosal grading score improved from a total of 4/6 on the right side to 0/6 at three months follow-up. However, his left side was at 0/6 and showed mild inflammation of 2/6 at three months follow-up. He then received a second treatment of aPDT 6 months later due to the suboptimal response. At that time his right side remained stable with mild edema (1/6) and the left side scores were 4/6 immediately prior to the second aPDT treatment. This dropped to 2/6 three months post-treatment. Post aPDT sinus culture showed normal respiratory flora. His medical management remained the same 6 months prior to aPDT and 6 months post aPDT.

Discussion

Treatment and management of refractory CRS continues to be a difficult scenario for rhinologists. Despite adequate surgery and medical treatment, gaps in current knowledge about etiology and disease characterization, clinical control in this group of patients is challenging. Different agents have been described as possible causatives including chronic osteitis [25], chronic bacterial infection, fungi [26] and staphylococcal superantigens.

Photodynamic therapy is a non-invasive non-pharmacological treatment, with widespread use in other fields of medicine [13- 15,17]. In chronic periodontal disease aPDT has demonstrated efficacy in cases where conventional antibiotic therapies can be challenging (ie. biofilms, gram-negative bacteria, and antimicrobial resistant organisms). The mechanism of action is based on the concept of disrupting the bacterial cell wall structure with oxygen free radicals. These free radicles are generated as a result of the interaction between certain wavelengths of laser light and photoactive material such as methylene blue dye in our study. Several studies have shown promising results in reduction of methicillin-resistant Staphylococcus aureus (MRSA) biofilm. More recently, a study looking at the antibiotic resistant polymicrobial biofilms of Pseudomonas aeruginosa and MRSA in a maxillary sinus model were treated with a methylene blue/ethylenediamine tetraacetic acid (EDTA) photosensitizer and 670-nm non-thermal activating light. The results demonstrated that aPDT reduced the CRS polymicrobial biofilm by >99.99% after a single treatment. Multiple benefits could potentially derive from the utilization of non-pharmacological treatment of infections, particularly avoidance of microbial resistance [27].

Our study represents the first clinical experience of aPDT in a cohort of patients with refractory CRS. The most common diagnosis in this group of patients was CRSsNP [% 31.25], with CRSwNP including AFRS [% 68.75] being the most prevalent subgroup in this category. Analyzing safety outcomes, we only encountered 3 mild and self-limiting adverse events during the study out of a total of 43 intervened sinuses: a stinging sensation in 2 patients and mild bleeding in one. Some of these may be explained by the fact that the balloons were hard to insert into some of the paranasal sinuses as the current version of the balloon catheter tip is fairly soft and requires some manipulation to insert into the maxillary and frontal sinuses. There is a slight learning curve for placement of the balloon catheter within the sinuses. Physician experience with the placement of the balloon likely plays an important role in comfort for the patient. Local anesthetic may be applied to avoid such discomfort and pain.

In terms of efficacy, the clinical response we obtained showed a significant reduction in endoscopic mucosal scores at 3 months. We observed some fluctuation of the mucosal scores including a worsening in 7 patients at the 6-month post-procedure visit, but these scores did not diminish to original baseline values. This might be explained by the fact that biofilm-mediated diseases often show a relapsing and remitting course and have variable growth rates with variations in clinical presentation [28]. Although pre and post-treatment mucosal membrane electron microscopy was not utilized, the enhancement in sinus score and reduction in purulent discharge is an indirect marker of efficacy of the treatment as well as improved post-treatment mucociliary clearance.

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Iris Publishers-Open access Journal of Otolaryngology and Rhinology | ‘POLIDON’ Approach-A Novel Approach of Mastoidectomy in the COVID-19 Pandemic

 

authored by Mostafa Kamal Arefin*

Abstract

Background: WHO declared COVID-19 outbreak as pandemic in March, 2020, which was started from Wuhan of china. Mastoidectomy is an aerosol generating procedure. If a patient of COVID-19, either confirmed, suspected or asymptomatic career, requires mastoidectomy urgently, it’s a critical issue for the health care professionals for the highly contagious nature of this novel corona virus. Here, some simple, but novel and very effective measures will be discussed for protection of all health care providers (HCPs). Polythene sheet and Povidone Iodine are the change makers in this novel approach of mastoidectomy, mentioned in this article. So, we named the technique as ‘POLIDON approach’ of mastoidectomy.

Material and method: Placement of a transparent, sterile polythene sheet which acts as an interface between patient and surgeons and all other OR staffs is an important issue. Meanwhile, extended use of Povidone Iodine (PVP-I) is recommended in different way. Mouthwash for gargling and nasal application either by spray or nasal irrigation or drop will reduce viral load from nose and mouth of patient. HCPs should use PVP-I prophylactically also. Thus, the chance of transmissibility of novel coronavirus is reduced. Meanwhile, Povidone Iodine should be mixed with irrigating fluid to help in reduction of contamination by bone dust mixed with fluid, produced during surgery.

Conclusion: As mastoidectomy is an aerosol generating procedure, and novel coronavirus is highly contagious, so higher level of protection is required. A simple and cheap polythene sheet as barrier drape as well as rational and novel use of Povidone Iodine, i.e. the proposed ‘POLIDON’ approach can significantly reduce the chance of corona virus transmission among the health care professionals working in the operation theatre.

Keywords: POLIDON; Mastoidectomy; COVID-19; Povidone Iodine; Polythene

Abbreviations: PVP-I: Povidone Iodine; HCP: Health care provider

Background

WHO declared COVID-19 outbreak as pandemic in March 2020, which was started from Wuhan of China. During this pandemic, (every person or patient has chance of being infected with corona virus,) nobody is immune of being infected with coronavirus or being asymptomatic career of this [1]. Mastoidectomy is an important surgical procedure in which all the accessible mastoid air cells are accenterated with an aim to make the ear safe [2-4]. CSOM with extracranial and intracranial complications are indications of emergency or urgent mastoidectomy. The indications of urgent or emergency mastoidectomy are a bit changed recently [5,6]. In the last few decades brain abscess due to CSOM was advocated and practised to be treated in two stage, at first incision and drainage of brain abscess, then 2-4 weeks later mastoid exploration. But recently single stage urgent otological procedure is advocated (and it is without any delay) for minimizing mortality and morbidity. In a developing country- like Bangladesh, lot of patients present to the hospitals at advanced stage usually with complications, like mastoiditis (not responsive to conservative treatment), facial palsy, labyrinthitis, extradural abscess, brain abscess, meningitis, lateral sinus thrombosis, otitic hydrocephalus which warrants urgent surgery [5-7]. In our context, emergency mastoidectomy is not uncommon, especially in our centre, i.e. Dhaka Medical College Hospital, a tertiary level hospital [8].

Mastoidectomy is an aerosol generating procedure. If a patient of COVID-19, either confirmed, suspected or asymptomatic career, requires mastoidectomy for any of those indications, it’s a critical and alarming issue for the health care professionals, including doctor, nurse, other OR (operating room) staff for the highly contagious nature of this virus [9]. In current situation prior to any (routine) surgery report of RT-PCR test for coronavirus is mandatory. Negative results do not preclude SARS-CoV-2 infection and should not be used as the sole basis for patient management decisions. Negative results must be combined with clinical observations, patient history, and epidemiological information [10]. In a developing country- like Bangladesh, patient presents to the hospitals at advanced stage usually with complications, like mastoiditis, facial palsy, labyrinthitis, extradural abscess, brain abscess, meningitis, lateral sinus thrombosis, otitic hydrocephalus [8,11].

RT-PCR test for detection of coronavirus is not available throughout the country, due to lack of laboratory facility, kit, technologist and other support. Due to partial or complete lockdown state mobility for the patient is also not easy rather very difficult. So, confirmation of COVID-19 by RT-PCR test can’t be done instantly everywhere. Prior to surgery it’s recommended to do a CT scan of chest to find clue regarding COVID-19 [12]. But sometimes situation is unfavourable for doing it also. Few days or even hours are demarcating line between life and death or overall morbidity. For this reason health care professionals should take maximum protections for their own safety within lots of limitation, seeming every patient as a COVID-19 patient. Though the government, local authorities, personally all HCPs are trying to provide or collect adequate personal protective equipment (PPE) or other measures, throughout the world there is deficiency of it. In a resource constraint country, like us, we need to have cheap, affordable, easily available measures for protection. Here, some simple, but novel and very effective measures will be discussed for protection of all health care providers (HCPs) in this aerosol generating procedure. Polythene and Povidone Iodine are the change makers in this novel technique of mastoidectomy, mentioned in this article. So, we named the technique as ‘POLIDON technique’ of mastoidectomy.

Material and Method

In our setting, placement of a transparent, sterile polythene sheet which acts as an interface between patient and surgeons and all other OR staffs is the most important issue. Meanwhile, extended use of Povidone Iodine (PVP-I) is recommended in different way. Mouthwash for gargling and nasal application either by spray or nasal irrigation or drop will reduce viral load from nose and mouth of patient. HCPs should use PVP-I prophylactically also. Thus the chance of transmissibility of novel coronavirus is reduced [13-15]. Meanwhile, Povidone Iodine should be mixed with irrigating fluid to help in reduction of contamination by bone dust mixed with fluid, produced during surgery. This technique was innovated by the corresponding author and applied in Dhaka Medical College Hospital and Taqwa General Hospital (, a private hospital) in three emergency/ urgent mastoid surgeries.

Povidone Iodine

In 1955 Povidone-iodine (iodine with water-soluble polymer polyvinylpyrrolidone, PVP-I) was invented. The active moiety, non PVP‐bound (free) iodine is released into solution from the PVP‐I complex. PVP delivers the free iodine to target cell membranes. Free iodine, that mediates the basic mechanism of action (oxidation of amino acids and nucleic acids in biological structures), which is difficult to counteract. This basic mechanism of action leads to strong microbicidal activity expressed by multiple modes of action that include the disruption of microbial metabolic pathways, as well as destabilisation of the structural components of cell membranes, causing irreversible damage to the pathogen. Consumed free iodine is then replaced by PVP‐bound iodine. The concentration of free iodine is the determining factor of the microbicidal action of PVP‐I. In a study investigating the virucidal activity of different disinfectants, Electron micrographic study revealed that, exposure of iodine led to destruction of nucleoproteins of viral particle-which is the main mechanism of action [16, 17]. However, disruption of surface proteins essential for the spread of enveloped viruses has also been noted [16, 18]. Furthermore, Iodine is a scavanger of free radical oxygen species, contributing to anti-inflammatory properties [16, 19]. This interaction ultimately results in microbial death [16-26].

Virucidal activity of PVP-I

Povidone‐iodine has been reported as having the highest virucidal activity profile among several antiseptics such as Chlorhexidine (CHG), Benzalkonium chloride (BAC), BEC and Alkyldiaminoethyl‐glycine hydrochloride (AEG) [16, 20]. PVP-I has been shown to be active in vitro against the coronaviruses that have caused epidemics in the last two decades, namely SARS-CoV causing the severe acute respiratory syndrome (SARS) epidemic of 2002-3 and MERS-CoV the agent responsible for causing the Middle East respiratory syndrome (MERS) epidemic of 2012-13. SARS-CoV-2 is highly homologous with SARS-CoV, and as such it is considered a close relative of SARS-CoV1015. In his study Egger et al suggests that, upto 0.23% concentration of PVP-I is virucidal [17, 18]. Kariwa showed that treatment in vitro of SARS-CoV with various preparations of PVP-I for 2 minutes was enough to reduce viral activity to undetectable levels [14]. The lowest concentration used was 0·23%, found in an over the counter throat spray [18]. Recent studies conclude that SARS-CoV-2 should behave similarly 21[16-26].

Plastic/Polythene

Modern healthcare would not be possible without the use of plastic materials. Polythene is one type of it, which is popular for its greater flexibility, comfort and mobility. Polythene, with its exceptional barrier properties, light weight, low cost, durability, biocompatibility and transparency, is ideal for medical applications.

Today’s most innovative medical procedures are dependent on plastics

We designed a technique to use it like ototent (please see Figure) [27].

Proposed Steps of Mastoidectomy in COVID-19 pandemic:

1. Consent- written informed consent is mandatory.

2. Preparation of patient

a) Prior to surgery, patient is to gargle with 10-15 ml PVP-I 1% (undiluted) or 30 ml 0.5% (diluted with same amount of water) mouthwash solution

b) Nasal irrigation with PVP-I (0.5%) is to be given, in case of difficulty or inconvenience of patient PVP-I nasal spray or drop should be applied.

3. Preparation of members of surgical team

a) Sterile surgical gown should be put over impermeable gown or protective apron.

b) FFP3 or FFP2 or N95 mask or PAPR on face

c) Eye protective goggles

d) Hood cap is preferable than simple cap forehead protection.

e) Double gloves is preferable.

f) All health care professionals are proposed to use PVP-I for gargling and applying in nose in same manner as proposed for patient for protection as adjunct to PPE before and/ or after mastoidectomy.

g) During induction of anaesthesia and intubation full surgical team, except anaesthetist and one or two staff, necessary for this step, is to stay outside the OT. 5minutes later full team is to enter into the OT.

4. Positioning of the patient.

5. Skin should be prepared with PVP-I 10% solution.

6. PVP-I is to be mixed with irrigating fluid in atleast 1:10, i.e. 100 ml in 1litre of normal saline.

7. Draping is to be done properly.

8. Infiltration of local anaesthesia with Lignocaine with adrenaline.

9. A postauricular incision (usually) is to be made.

10. Skin, subcutaneous tissues are to be dissected.

11. Temporalis fascia is to be harvested.

12. Posteriorly or superiorly based flaps are to be made.

13. Another incision in external auditory canal 1 to 4 o’clock (traditionally 6 to 12 O’clock) position is to be made.

14. Mastoid retractors are to be fixed in position so that whole tympanic membrane (TM) could be visualized.

15. Margin of perforation is to be freshened.

16. Tympanomeatal flap is to be elevated.

17. Prior to start of drilling one or two additional, transparent, sterile polyethene sheet is to place and fix over the operative field, like an extra drapping sheet and a tent, where the apex is formed at microscope objective eye piece. This step can be performed prior to incision also.

Hands of surgeons and all necessary instruments kept inside the polythene sheet, the tent. Surgeons hands are to be fixed with the polythene sheet with adhesive tape.

Some ports in polythene sheet like microscope drape, for entry of surgeon and assistant’s hand can be made.

18. Mastoid drilling is to be started targeting the triangle of attack.

19. Drilling is to be continued for complete disease removal and completion of surgery

20. Cartilage or TORP or PORP is to be used for ossiculoplasty or other type of reconstruction.

21. Temporalis fascia is to be placed properly.

22. Wound is to be closed in layers after proper haemostasis.

23. Ototent made by polythene is to be removed.

24. Mastoid bandage is to be applied.

25. Anesthesiologist is to start the reversal process.

During extubation full surgical team, like before, is to stay outside OT again. Five minutes after extubation they should enter inside OT.

26. Proper doffing is to be done after the operative session [2- 4].

Preparation of Application of Povidone Iodine or PVP-I Prior to Surgery

For gargling and mouthwash

For fully conscious patient

a) PVP-I 1% solution (undiluted) 10 ml for 30 sec to 1 minute or 0.5% solution (diluted by mixing same amount of water, i.e. 10 ml PVP-I with 10ml water) 20ml for 1-2 minutes.

b) For patient with altered consciousness - A sponge swab or similar is soaked in 2-5 ml of 1% PV P-I and this is carefully wiped around all oral mucosal surface.

For nasal application

Nasal spray: 2-3 puff in each nostril with a standard atomizing devise with 0.5% solution of PVP-I or

Nasal irrigation: Irrigate or wash through both nostril with 200-300 ml (100-150 ml in each nostril) of 0.5% PVP-I solution or

Nasal drop: If nasal spray or irrigation facility is not available apply nasal drop 3-4 drops in each nostril [13, 14, 28].

Preparation of PVP-I mixed irrigating fluid

ml of PVP-I 10% solution is to be mixed with 900ml of Normal saline to make a PVP-I 1% solution. 50 ml of PVP-I 10% solution can be mixed with 950 ml of Normal saline also.

Polythene: Simple, transparent polythene.

The plastic/polythene sheet allows good mobility of the hands of the surgeons. In spite of being transparent or translucent, there may have some degree of glare. Several modifications can be done. Our focus is on the simplest method. Any positive modification is appreciable. We designed a technique to use it like ototent (please see Figure) [27]. Microscope drape is an alternative, relatively expensive, but not available everywhere, especially in developing or any resource constraint country [9, 22].

Special considerations

1) Number of health care professionals in the OT should be minimum. In an ear surgical procedure, only one or two surgeons is/are needed to be in the OR and all observers should be excluded. This is important to reduce potential exposures, but also to limit use of PPE (mainly N95 masks).

2) Experienced and skilled surgical team is must.

3) If facility and time allows mastoidectomy should be done under general anaesthesia in a negative pressure room.

4) Electrocauterization by monopolar diathermy should be avoided, otherwise minimized.

5) For educators, making a video recording of the surgery is to be suggested to share with trainees, if possible, rather trained them under direct guidance [24] (Figures 1-5).

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