*Article* **Sheep's Head as an Anatomic Model for Basic Training in Endoscopic Sinus Surgery**

**Constantin Stan 1,2, Laszlo Peter Ujvary 1,\*, Cristina Maria Blebea 1, Doini¸ta Vesa 2,\*, Mihai Ionu¸t Tănase 1, Mara Tănase 1, Septimiu Sever Pop 1, Doinel Gheorghe Rădeanu 1, Alma Aurelia Maniu <sup>1</sup> and Marcel Cosgarea <sup>1</sup>**


**Abstract:** *Background and Objectives*: This study aims to establish the sheep head as a viable anatomical model for training in functional endoscopic sinus surgery through comprehensive anatomical examination and training-based assessment of participants' satisfaction. *Materials and Methods*: Participants were divided into three groups according to their prior experience in endoscopic sinus surgery; in total, 24 participants were included. Each participant in the study was assigned to perform the designated procedures on a single sheep's head. Following the completion of the procedures, each participant was provided with a 14-item comprehensive satisfaction questionnaire with a scale attributed from 1 to 5. The normality of distribution was checked by applying the Shapiro-Wilk Test. The Kruskal–Wallis test was applied to compare study group sentiment of agreement towards individual procedures. *Results*: No significant differences were noted between the answers of the different groups. For the resident group, the average satisfaction score was 4.09 ± 0.54; junior specialist group 4.00 ± 0.55; for the senior specialist group overall satisfaction average score was 4.2 ± 0.77. *Conclusions*: The sheep's head can be successfully used for learning and practicing manual skills and the use of instruments specific to functional endoscopic sinus surgery. Moreover, the sheep head model can be used for training in other diagnostic or surgical procedures in the field of otorhinolaryngology, such as endoscopy of the salivary glands, open laryngotracheal surgery, or in otologic surgery, but also in other different surgical fields such as neurosurgery, ophthalmology or plastic surgery. Despite the differences between the ovine model and human anatomy, it provides a resourceful and cost-effective model for beginners in endoscopic nasal surgery.

**Keywords:** surgical training; simulation; sinus surgery; animal model; FESS

#### **1. Introduction**

The process of surgical training in Functional Endoscopic Sinus Surgery (FESS) heavily relies on the availability and accessibility of well-equipped laboratories that facilitate endoscopic dissection on cadaveric heads. However, the limited availability of cadavers due to medical, ethical, and moral considerations has led to the exploration of alternative methods, specifically the utilization of anatomical models that closely resemble the human head [1]. In order to achieve this objective, efforts have been made to develop techniques that can ease the learning process. One proposed approach involves using sheep heads as anatomical ex vivo models, although the literature on this subject is currently scarce and lacks comprehensive studies [2].

For endoscopic sinus surgery training, both the in-vivo ovine model and cadaveric simulations offer high handling fidelity. In certain countries, in-vivo animal simulation

**Citation:** Stan, C.; Ujvary, L.P.; Blebea, C.M.; Vesa, D.; T ˘anase, M.I.; T ˘anase, M.; Pop, S.S.; R ˘adeanu, D.G.; Maniu, A.A.; Cosgarea, M. Sheep's Head as an Anatomic Model for Basic Training in Endoscopic Sinus Surgery. *Medicina* **2023**, *59*, 1792. https:// doi.org/10.3390/medicina59101792

Academic Editors: Adriana Neagos, Daniela Vrinceanu, Codrut Sarafoleanu and Mahmut Tayyar Kalcioglu

Received: 10 September 2023 Revised: 28 September 2023 Accepted: 7 October 2023 Published: 9 October 2023

**Copyright:** © 2023 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https:// creativecommons.org/licenses/by/ 4.0/).

is prohibited, making animal cadaveric simulation a more accessible substitute [3,4]. The ovine sinus model allows the acquisition of endoscopic surgical skills using video endoscopic techniques. It is cost-effective, portable, and adaptable for use in various settings [5]. Moreover, the ex-vivo ovine model for training does not require institutional review committee approval and raises fewer ethical concerns compared to live animal models [5,6].

This study aims to establish the sheep head as a viable anatomical model for training in functional endoscopic sinus surgery through comprehensive anatomical examination and training-based assessment of participants' satisfaction.

#### **2. Materials and Methods**

#### *2.1. Image Acquisition for Anatomical Description and Anatomical Sectioning*

After ethical approval was granted (AV258/28.02.2022), an anatomical feasibility study was undertaken regarding the sheep head as an alternative for FESS training. For the anatomical study, 26 fresh-frozen adult sheep heads (Native Romanian Turcana sheep) were procured from the local slaughterhouse (veterinary clearance was obtained), at a price of 10 Romanian lei (RON) a piece, roughly the equivalent of two euros a piece. One head was defrosted and used as a sample for imaging acquisition and endoscopy and the other head was used to provide sectional anatomical details. The second head (frozen at −20 ◦C) was serially sectioned in sagittal and transverse planes. The sagittal plane was paramedian to the septum, dividing the skull into two equal parts. The transverse sections were 2.5 cm in thickness. Sectional photographs were taken, and important anatomical elements were digitally labeled. The obtained information was presented to the participants through oral presentations and written handouts.

#### *2.2. Model Preparation for Surgery and Instrumentation*

Prior to the initiation of the maneuvers, a preparatory phase was undertaken, during which the fresh frozen sheep heads were allowed to undergo a gradual thawing process at room temperature for a duration of approximately 14 h. As a subsequent step in the preparatory process, the nasal cavities of the sheep heads were irrigated with a saline solution. Ultimately, before beginning the evaluation process, the tip of the nose was sectioned to facilitate endoscopic maneuvering, a useful aspect also presented by other authors [7]. Table 1 lists the equipment and instruments used for training.


**Table 1.** Equipment and instruments used for endoscopic maneuvers.

The support was innovated by Mladina and Karl Storz Gmbh to fix in position and secure the lamb's head (Figure 1) [7,8]. In our study, we used it for the sheep's head, which, although it is more voluminous, could be fixed without problems.

**Figure 1.** View of the sheep's head secured in the Karl Storz® special head holder.

A series of basic endoscopic maneuvers using the sheep's head as a model was performed by 24 participants. Each participant was allocated one sheep head (Table 2).



#### *2.3. Participant Selection*

Participants were divided into three groups according to their prior experience in endoscopic sinus surgery. The first group was formed by 10 first-year otolaryngology resident doctors with minimal or no experience in endoscopic sinus surgery. The second group consisted of 10 junior otolaryngology specialists with 3–5 years of exposure to rhinology procedures. The third group was formed by four senior otolaryngologists with over 20 years of experience.

#### *2.4. Participant Assessment—Satisfaction Questionnaire*

Each participant in the study was assigned to perform the designated procedures on a single sheep's head, targeting both nasal fossae. Following the completion of the procedures, each participant was provided with a 14-item comprehensive satisfaction questionnaire (File S1). For each answer, a scale from 1–5 was attributed, 1 denoting "totally disagree", and 5 signifying "completely agree". This allowed participants to provide nuanced feedback, enabling a comprehensive assessment of their overall satisfaction and perception of the performed procedures.

#### *2.5. Statistical Analysis*

For statistical analysis, Statistical Package for the Social Sciences (SPSS) 26.0 (Armonk, NY, USA: IBM Corp) was used. Data from the questionnaire was collected as numerical variables (1–5). For each group, mean and standard deviation were calculated for an individual answer within the questionnaire. The normality of distribution was checked by applying the Shapiro–Wilk Test. The Kruskal–Wallis test was applied to compare study group sentiment of agreement towards individual procedures.

#### **3. Results**

#### *3.1. Basic Endoscopic Anatomy*

Relevant anatomical structures regarding the endoscopic dissection can be seen in Figures 2–4. Opposed to humans, the inferior turbinate is comprised of two parts.

**Figure 2.** (**a**) Endoscopic view of the sheep's left nasal fossa. 1—inferior part of inferior turbinate; 2—superior part of inferior turbinate; 3—nasal septum; (**b**) endoscopic view of the posterior septal defect specific to the ovine model described by Mladina [7]—dotted white line. Right nasal fossa, 1—the lower limit of the septal defect; 2—the superior limit of the septal defect; 3—inferior turbinate; 4—lateral nasal wall; 5—nasal floor.

**Figure 3.** (**a**) Endoscopic view—left nasal fossa—1—middle turbinate; 2—lateral nasal wall; 3 septum. (**b**) Endoscopic view—left nasal fossa; 1—medialized middle turbinate; 2—natural ostium of the maxillary sinus; 3—uncinate process.

**Figure 4.** Endoscopic images of sub-perichondral dissection of the septum and turbinate fracture. (**a**) Sub-perichondral dissection of the septum, (**b**) Instrumental lateral fracture of the inferior turbinate. 1—lateral nasal wall; 2—inferior turbinate; 3—Cottle dorsal scissors; 4—insertion of the inferior turbinate to the lateral nasal wall.

The excision of the inferior turbinate permits the visualization of the middle turbinate. By gently and medially displacing it using an elevator, the natural ostium of the maxillary sinus becomes visible. To further enhance access and facilitate surgical intervention, the backbiter antrum punch can be employed to enlarge the natural ostium, resulting in the creation of a broad middle antrostomy.

#### *3.2. Procedures and Evaluation*

Following the extraction of a foreign body, attention was directed to raising the mucosal flap, bone resection and repositioning of the mucosal flap to mimic the maneuver performed during an actual turbinoplasty. Endoscopic septoplasty was undertaken as shown in Figure 4a. Following the initial procedures, the inferior turbinate was resected as a whole to facilitate the visualization of the middle turbinate—Figure 4b.

By medializing the middle turbinate, the natural ostium of the maxillary sinus is also pointed out, which was widened with the help of the backbiter antrum punch to create an anthrostomy. The last procedure undertaken was the ethmoidectomy—Figure 5a,b.

**Figure 5.** (**a**,**b**) Endoscopic images of instrumental removal of ethmoidal cells.

The assessment of the overall satisfaction and perception of the performed procedures was as follows in Table 3.

**Table 3.** Satisfaction questionnaire assessment.


<sup>1</sup> = Kruskal-Wallis test; ENT = otolaryngology; SD = standard deviation; Values for each question and for each group are presented as mean and standard deviation. For most of the answers, no significant difference were noted between the answers of the different groups.

For the resident group, the average satisfaction score was 4.09 ± 0.54; junior specialist group 4.00 ± 0.55; for the senior specialist group overall satisfaction average score was 4.2 ± 0.77 (Figure 6). Considering the average score for all responses noted for each individual group, no statistical differences can be noted, with a *p*-value of 0.598.

#### **4. Discussion**

Overall satisfaction in all groups was equal to or above 4 out of 5, meaning that a strong agreement has been reached in all groups, regardless of previous experience, in favor of considering the sheep's head as a useful model for endoscopic endonasal surgical training.

The extraction of a foreign body from the nasal fossae necessitates hand–eye coordination, particularly due to the utilization of a 2D endoscopy image, which requires accurate depth perception and spatial orientation. Participants in all groups agreed that simulating foreign body extraction is a good procedure to learn utilizing this model.

Although other authors [7,8] recommend the complete removal of the anterior septal portion for better endoscopic visualization, we chose to keep a part of the anterior septum, considering the advantage it offers us for practicing septoplasty. Even so, this specific modification was advantageous in facilitating the accessibility and maneuverability required during endoscopic procedures. All study group participants were in strong agreement with the benefits offered by the sheep model in endoscopic septal resection training, with no statistical differences noted between groups.

The training scenario simulating a turbinoplasty provided a learning experience to enhance participants' endonasal tissue handling skills. This exercise proved to be particularly advantageous for beginners, as it offered a controlled environment in which to refine their skills.

The deliberate and controlled execution of partial resection and mucosal flap manipulation within the nasal cavity proved to be an invaluable training tool. By carefully excising a segment of the inferior turbinate, it becomes possible to accentuate the prominence of the middle turbinate, which serves to identify the natural ostium of the maxillary sinus.

Although the overall satisfaction was high in all groups there are a few drawbacks when considering the anatomical similarities. Similarity of anatomical landmarks compared to humans received an average score of 3.1. Also, procedures like ethmoidectomy and maxillary anthrostomy did not receive an overall high satisfaction score, averaging 2.6 for ethmoidectomy and 3.6 for anthrostomy.

There are few studies that have highlighted the utility of the ovine model as a viable substitute for surgical training in the field of functional endoscopic sinus surgery.

Gardiner [9] was the first author to propose the sheep's head for training in endoscopic sinus surgery, proposing both simple and more complex maneuvers. Awad et al. [5,6] also proposed the sheep's head for surgical training in endoscopic rhino-sinusal surgery, showing clear advantages of its use, demonstrating the face, content and construct validation of this anatomic model. Mladina et al. [7,8,10] in their studies chose the lamb's head, due to its smaller size, which allows the use of standard endoscopic rhino-sinusal surgery instruments. He implemented a training program in endoscopic rhino-sinusal surgery using the lamb's head, which proved to be useful for the trainees and allowed the transition to the next level in endoscopic sinus surgery training, i.e., human cadaver training.

Although 3D printing technology has been frequently used for preoperative assessment in endoscopic sinus surgery [11], it is also used to create anatomical models for surgical training in FESS, with the possibility of creating high-fidelity models, being able to simulate certain sinus pathologies, benefiting from validation in this sense, but without benefiting from the real feeling of the tissues, an important disadvantage compared to the sheep's head training.

Even with the mentioned drawbacks, we consider that the ovine FESS model can be an integrative part of surgical training alongside artificial models. Combining the precise anatomy of the artificial models with the feel and overall experience of the ovine model, a more complex teaching experience could be achieved, considering the importance of functional endoscopic sinus surgery [12].

Otologic surgery is another field where the ovine model has been successfully implemented in the training and preparation of young doctors. Anschuetz et al. [13] carried out a study that developed and validated the ovine model for surgical training in endoscopic ear surgery. The anatomy of the sheep's ear was compared with that of humans and was used to perform a series of otological surgical procedures such as canaloplasty, myringoplasty, and ossiculoplasty. Procedures were subjectively evaluated using a postoperative questionnaire, using a scale from 1 to 10. Mean procedure times were as follows: canaloplasty (29.7 ± 13.2 min), middle ear dissection (7.7 ± 2.6 min), myringoplasty (7.7 ± 4.3 min), and ossiculoplasty (10.4 ± 2.7 min). Canaloplasty and flap elevation time decreased from 46.4 to 16.2 min over the study (absolute difference: 30.2 min, 95% CI 22.28–38.12). Subjective ratings were high: tissue quality (8.9/10), overall satisfaction (8.3), and learning experience (8.8). Beckmann et al. [14] carried out a study in which, using the ovine model, they evaluated the learning curve of laser stapedotomy for trainees, with considerable improvement of operative times once the maneuver is repeated. The experienced surgeon maintained a steady average time of 15:01 min throughout the training without any intraoperative issues. The fellow reduced surgical time gradually from 27:21 (first five cases) to 24:10 min (last five cases), and the resident also reduced this time from 42:38 to 21:08 min. Training methods in otosclerosis surgery are very limited, which is why the ovine model proved to be more than useful for this purpose.

Fernandez et al. [15] using eight lamb heads simulated rare situations that may occur intraoperatively in stapes surgery. Thus, floating footplate, footplate fracture, luxation of the incus or necrosis of the long process, overhanging facial nerve, and obliterative otosclerosis could be simulated. A subjective questionnaire with a scale from 1 to 10 was used to determine the satisfaction of the study participants. Taking into account that the options for surgical training in stapes surgery are very limited, the ovine model used in this regard proved to be an excellent learning method for young otologists.

The sheep model was also used for the training of plastic surgery fellows. Isaacson et al. [16] evaluated the possibility of surgical training using the sheep's head for a series of plastic surgery techniques performed for pathologies of the eyelids and the orbit. They harvested 10 sheep heads after the completion of an in vivo study. They evaluated a series of procedures such as upper eyelid blepharoplasty, ptosis repair, upper eyelid repair procedure in facial paralysis, lateral canthotomy, lower acantholysis, narrowing of the lower eyelid, and transconjunctival approach to the floor of the orbit. The overall utility was excellent but remarks were made for limitations due to anatomical variations, one of which is the anatomy of the lacrimal system.

In the field of laryngology the ovine model was used for training in open laryngotracheal surgery. The head and neck were used to simulate a series of surgical procedures, such as tracheotomy, laryngoplasty, tracheal resection with tracheal sutures, and laryngectomy with pharyngeal sutures. This time, the ovine model could be successfully implemented for the training of open surgical techniques, having the advantage of the learning of surgical skills and tissue handling on a model close to humans [17].

The ovine model was also described in the field of dentistry to aid in the learning curve of sinus augmentation. Valboneti et al. analyzed the sheep and human maxillary sinuses anatomy using cone beam computed tomography and histology. Obvious maxillary sinus differences were identified between the human head and ovine model, which were taken into account in order to carry out the experimental procedures [18].

The ovine model was also successfully used for training in sialendoscopy, Borner et al. [19] implemented such a training program in salivary gland endoscopy using the sheep's head, a novelty in the field considering that, for training in these procedures, pig's head was used for several years. The Stenson and Wharton ducts could be successfully visualized endoscopically and therapeutic maneuvers were also simulated by removing a stone from the Stenson duct.

The ovine head was also frequently used for training in different neurosurgical procedures. Kamp et al. [20] simulated a brain tumor model using agar-agar solution injected into fresh sheep brains. The tumor model would vary depending on the concentration of the injected solution, so a high concentration could cause the appearance of well-defined tissue masses, simulating possible brain metastases, while a solution with a lower concentration could cause the appearance of a diffuse infiltrative tissue, thus simulating a primary tumor formation at the level of the brain tissue. This model made it possible to simulate different intraoperative scenarios for young neurosurgeons, with the advantage of learning manual skills and obtaining a haptic sense, in a much more relaxed environment and without the pressure of real intraoperative scenarios.

Korotkov et al. [21] looked for an accessible anatomical model for the training of anterior clinoidectomy, the procedure performed in the case of vascular and tumoral conditions located at the frontotemporal level, which requires a high level of surgical training. Five formalized sheep heads were evaluated, at the level of which, through silicone injection, the presence of dural and extradural lesions was simulated. All the procedures were carried out successfully, thus demonstrating the fact that the sheep head model can be a good alternative to the human cadaver.

Another use of the sheep head model belongs to Altunrende et al. [22], who used the sheep skull for the training of neurosurgeons and ophthalmology residents in performing orbitotomy and frontal craniotomy using dissection under the microscope with good results and with satisfaction in the training of microsurgical techniques for the approach of the optic nerve and optic canal.

Limitations of this study include a small number of participants who belonged to a single training institution. Moreover, our study did not evaluate the transfer of skills acquired using this anatomical model in real endoscopic sinus surgery. Although effective in preparation, the ovine model has a major disadvantage compared to medical practice due to the lack of vascularization and the lack of inflammatory reaction of the rhino-sinusal mucosa often encountered in surgical practice.

In this sense, to extend our research and to eliminate this limitation, in vivo training sessions for endoscopic sinus surgery could be performed using sheep under general anesthesia with orotracheal intubation. In this way, participants can also face intraoperative bleeding, an essential aspect of the surgical training of young doctors. After performing the surgical procedures, in order to avoid their possible suffering, the sheep would be euthanized in accordance with ethical aspects.

At the moment, the training of young doctors in endoscopic sinus surgery is done through the residency program, which involves practicing directly on the live patient, in the operating room under the direct supervision of an experienced guiding surgeon. However, this determines the limitation of the surgical gestures that can be performed by the young doctor, to avoid possible intra- and post-operative complications. Regarding surgical training in FESS using alternative anatomical models, there is still no organized framework in many countries, leaving room to extend the solutions to this particular ovine model too. To the best of our knowledge, there are various courses organized in university centers in our country, on synthetic anatomical models or even on the ovine model, as is otherwise organized in our center. In this sense, we want to improve the simulation conditions by using in the future the in vivo ovine model, which comes with a series of clear advantages.

#### **5. Conclusions**

The sheep's head can be successfully used for learning and practicing manual skills in the use of instruments specific to functional endoscopic sinus surgery, but also for learning some basic endoscopic sinus procedures. Moreover, the sheep head model can be used for training in other diagnostic or surgical procedures in the field of otorhinolaryngology, such as endoscopy of the salivary glands, open laryngotracheal surgery, or in otologic surgery, but also in other different surgical fields, such as neurosurgery, ophthalmology or plastic surgery. Despite the differences between the ovine model and human rhino-inusal anatomy, it provides resources and minimal cost for beginners who want to develop skills applicable to their practice accuracy.

Similar data from the literature are quite limited, which is why this study should have an important role in the implementation of an anatomical model of a sheep's head for the training in functional endoscopic sinus surgery in our training center and others, considering the accessibility, reliability, and viability of the sheep's head and very good results obtained from its use.

**Supplementary Materials:** The following supporting information can be downloaded at: https:// www.mdpi.com/article/10.3390/medicina59101792/s1, File S1. Satisfaction Questionnaire.

**Author Contributions:** Conceptualization, C.S., A.A.M. and M.C.; methodology, C.S. and M.C.; software, C.S., L.P.U. and C.M.B.; validation, M.C., A.A.M. and C.S.; formal analysis, C.S., S.S.P., D.G.R. and D.V.; investigation, C.S., M.T., M.I.T. and D.V.; resources, C.S., D.G.R. and L.P.U.; data curation, L.P.U. and C.M.B.; writing—original draft preparation, C.S., M.I.T. and M.T.; writing review and editing, C.S., S.S.P. and L.P.U.; visualization, M.T., D.V. and C.M.B.; supervision, M.C. All authors have read and agreed to the published version of the manuscript.

**Funding:** This research received no external funding.

**Institutional Review Board Statement:** The study was conducted in accordance with the Declaration of Helsinki, and approved by the Institutional Review Board of the "Iuliu Hatieganu" University of Medicine and Pharmacy. Registration number AV258/28.02.2022.

**Informed Consent Statement:** Informed consent was obtained from all subjects involved in the study.

**Data Availability Statement:** The data presented in this study are available on request from the corresponding author. The data are not publicly available due to privacy and ethical reasons.

**Conflicts of Interest:** The authors declare no conflict of interest.

#### **References**


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### *Article* **Management of Capillary Hemangioma of the Sphenoid Sinus**

**Irina-Gabriela Ionita 1,2, Viorel Zainea 1,2, Catalina Voiosu 1,2, Cristian Dragos Stefanescu 1,2,\*, Cristina Aura Panea 1,3, Adrian Vasile Dumitru 1,4, Ruxandra Oana Alius <sup>2</sup> and Razvan Hainarosie 1,2**


**Abstract:** *Background and objectives:* Capillary hemangiomas are rare, benign vascular tumors that mainly affect the skin and soft tissue, with scarce appearance within the nasal cavities and paranasal sinuses. *Materials and methods:* We present a case report of capillary hemangioma of the sphenoid sinus and a review of the literature in the last ten years. *Results:* Clinical and endoscopic examination of the nose, radiologic assessment and particular histologic features contribute to the correct diagnosis of capillary hemangioma of the nose and paranasal sinuses. *Conclusions:* Transnasal endoscopic resection of capillary hemangioma located in the nose and paranasal sinuses is a valuable treatment method with good outcomes.

**Keywords:** capillary hemangioma sinus; endoscopic surgery; sphenoid tumor

#### **1. Introduction**

Capillary hemangiomas are rare, benign vascular tumors that mainly affect the skin and soft tissue. These tumors are frequently encountered in infants and children, more common in the female population, and are rarely diagnosed in adults [1].

Hemangiomas are vascular tumors that appear due to endothelial cell growth. Proliferation of regular (with normal architecture) endothelial cells is characteristic for hemangiomas. They should not be mistaken for vascular malformation, which occurs due to defects of vascular morphogenesis [2]. Vascular malformations are lesion defined by vascular anomalies determined by the alteration of embryogenesis and vasculogenesis [2].

Most hemangiomas appear on the skin in the head and neck region, but only 12% occur in the nose and paranasal sinuses with a predominance of the nasal cavity location [3,4]. Hemangiomas in the paranasal sinuses are rare findings, and most cases are reported in the maxillary sinus. Kim S.J. and Kwon S.H. reported maxillary sinus involvement in only 8% of hemangiomas affecting the sinonasal epithelium; no sphenoid sinus involvement was described in this study [4]. The same authors state that the nasal septum and inferior turbinate were the most common sites affected by hemangiomas with 40.5% and 29.7% of all cases, respectively [4,5], but other sites such as the nasal vestibule, middle turbinate, and uncinate process have been reported [6]. The presence of a capillary hemangioma within the sphenoid sinus is rare, and there are limited scientific papers regarding this specific site of appearance [1].

Intracranial hemangiomas are also rare cases, with a female predilection in adult patients, but with a possible rapid evolution, especially in pregnant women or women in the peripartum period [1,7,8]. Some authors state that pregnancy (due to all its hormonal changes) triggers the tumor's progression and can cause recurrence of the hemangioma [8].

**Citation:** Ionita, I.-G.; Zainea, V.; Voiosu, C.; Stefanescu, C.D.; Panea, C.A.; Dumitru, A.V.; Alius, R.O.; Hainarosie, R. Management of Capillary Hemangioma of the Sphenoid Sinus. *Medicina* **2023**, *59*, 858. https://doi.org/10.3390/ medicina59050858

Academic Editors: Adriana Neagos, Daniela Vrinceanu, Codrut Sarafoleanu and Mahmut Tayyar Kalciogu

Received: 28 February 2023 Revised: 21 April 2023 Accepted: 23 April 2023 Published: 28 April 2023

**Copyright:** © 2023 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https:// creativecommons.org/licenses/by/ 4.0/).

The location and size of the tumor will determine the clinical manifestation, but headache and visual impairment are the most frequent symptoms.

#### **2. Materials and Methods**

The aim of this manuscript is to present a case report of capillary hemangiomas of the left sphenoid sinus and a review of the literature in the last ten years.

We reviewed English articles published in 2013–2023 on PubMed and the Wiley Online Library. An interrogation was made on specific terms "capillary hemangioma sinus", "capillary hemangioma nose", and "capillary hemangioma sphenoid". On PubMed, the search using the specific terms mentioned above revealed 35 articles, but only 14 were related to the nose and paranasal sinuses. In the Wiley Online Library, the investigation revealed 23 manuscripts with capillary hemangioma, but only 6 articles referred to the nose and paranasal sinuses. During the interrogation, we found no series of sphenoid sinus capillary hemangiomas. The articles presenting this specific localization were case reports. The included case series regarding capillary hemangioma consisted of a limited number of patients and were usually retrospective studies.

The aim of this paper is to present the case of a 31-year-old female patient referred to our clinic by a regional ENT specialist for an excruciating headache (eight out of ten on the Numeric Pain Rating Scale) experienced during a flight, which partially resolved after oral analgesic intake. She was first treated by her otolaryngologist with oral antibiotics, oral steroids, and nasal drops with improvement of the severe headache, but a computed tomography of the paranasal sinuses was recommended. There is no personal history of allergies or other medical associated conditions, no ENT- specific symptoms such as nose bleeding or rhinorrhea, and no neurologic or ophthalmologic manifestations. The patient also denied any history of head trauma or previous nasal and sinus surgery or pregnancy.

Complete physical examination and flexible optic examination of the nasal cavities, pharynx, and larynx (with white light and narrow-band imaging) revealed a nasal septum deviated to the left side, inferior turbinate hypertrophy grade III, and a pulsatile area at the level of the left sphenoethmoidal recess with an atypical vascular pattern on narrow-band imaging examination, without abnormal nasal or sinus discharge. The nasopharynx was mass-free, without signs of inflammation or secretions. On flexible endoscopy, no mass was visible within the nasal cavity or the left sphenoethmoidal recess. The rest of the specific ENT examination was normal.

The computed tomographic (CT) examination described a 32 × 28 mm pseudo-cystic lesion in the left sphenoid sinus that occupied approximately 80% of the sinus cavity, in close relation with its posterior wall. The lesion was located within the sinus cavity without extension into the sphenoethmoidal recess or the nasopharynx. No bone erosions were visible on the imaging. All other paranasal sinuses appeared well aerated and tumor-free (Figure 1a–c). The CT assessment also highlighted the nasal obstruction with left posterior nasal septum deviation that determines blockage of the left sphenoethmoidal recess and bilateral inferior turbinate hypertrophy.

Upon admission to the hospital, the standard blood tests were carried out in order to establish any systemic impairment caused by the intrasinusal lesion. All blood work came back negative for any signs of inflammation or infection. Internal medicine assessment was also performed as part of the preoperative anesthesiology protocol. Written informed consent was obtained. During preoperative discussions, the goals of the surgery and the potential risks and complications, both intraoperative and postoperative, were explained to the patient. After preanesthetic assessments were checked, the patient underwent endoscopic sinus surgery to address the left sphenoid sinus under general anesthesia with orotracheal intubation. Septoplasty and inferior turbinate resection were performed to allow adequate access to the left sphenoethmoidal recess. The left sphenoid sinus was opened under endoscopic control with a zero-degree endoscope, and a reddish mass occupying approximately one-third of the sinus was identified. To adequately approach the lesion, a large opening of the sphenoid sinus was performed, and the mass was carefully detached from the posterior wall of the sphenoid sinus, ablated (Figure 2), and sent for histopathology examination. The dissection of the lesion from the wall of the left sphenoid sinus was carried out cautiously in order to avoid iatrogenic incidents. In the course of the dissection, the bleeding was limited. After removal of the tumor, the posterior wall of the left sphenoid sinus was assessed, and no bone discontinuities were observed. During surgery, we were able to appreciate the size of the intra-sphenoidal lesion as being smaller than the size measured on the computed tomography assessment. At the end of surgery, bilateral nasal packing with Merocell No. 8 was performed. The nasal packing was maintained for 48 h. Then, the nasal packing was removed with no bleeding, and nasal saline instillation was recommended at discharge. The patient did not suffer any intraoperative and postoperative complications, and the recovery was uneventful. After the surgery, all symptoms subsided, and the patient was discharged with no complaints and scheduled for follow up in one week.

(**a**)

**Figure 1.** *Cont*.

(**b**)

**Figure 1.** CT of the paranasal sinuses - (**a**) axial, (**b**) coronal, and (**c**) sagittal planes—lesion in the left sphenoid sinus.

**Figure 2.** Intraoperative aspect—dissection of the mass within the left sphenoid sinus after tactical resection of the deviated nasal septum.

Histopathological examination and immunohistochemistry established the diagnosis of capillary hemangioma with desmoplastic stroma. The pathologist described, on hematoxylin–eosin (HE) staining, tumor proliferation composed of endothelial cells without atypia, forming delicate vascular structures without lumens. The aspect was of a benign vascular proliferation formed by endothelial cells that form fragile submucosal vascular structures; some vessels appeared slightly dilated and with intraluminal red blood cells (Figures 3 and 4). The pathologic assessment did not identify any ulcerations. Immunohistochemical analysis of the tumor showed that it was CD31- and CD34-positive, with Ki67 < 1%. Both immunohistochemical markers CD31 and CD34 are positive in endothelial cells, but CD31 is considered the most dependable endothelial marker [9].

**Figure 3.** Solid area from a capillary hemangioma represented by a tumor proliferation composed of endothelial cells without atypia forming vascular structures without lumens. HE stain, ×400.

After surgery, clinical and endoscopic assessments were performed every month in the first three months, afterward the visits were scheduled for every three to six months. Flexible nasal endoscopy revealed patent nasal cavities and a patent left sphenoid sinus ostium (Figure 5). No signs of bleeding or abnormal nasal discharge were visible during any of the check-ups. Moreover, the patients' quality of life improved due to tactical removal of the deviated nasal septum and turbinoplasty. Postoperatively, the patient declared the absence of headaches and improved nasal breathing. Four months after resection, the patient received an enhanced brain (head) magnetic resonance imaging (MRI). The left sphenoid sinus was mass-free, without residual hemangioma (Figure 6).

**Figure 4.** Classic appearance of a capillary hemangioma consisting of delicate vascular structures, some slightly dilated and with intraluminal red blood cells. HE stain, ×400.

**Figure 5.** Postoperative aspect—enlarged left sphenoid sinus ostium with no signs of inflammation, no nasal or sinus discharge, and no bleeding.

**Figure 6.** Enhanced brain MRI (axial and coronal plane)—no lesion detected within the left sphenoid sinus four months postoperatively.

#### **3. Discussion**

Hemangiomas are vascular tumors consisting of blood vessels and connective tissue that rarely affect the nose and paranasal sinuses and appear frequently on the skin in the head and neck region [9]. There are different types of classifications for hemangiomas depending on the moment of presentation and the pathologic and immunohistologic features. Hemangiomas can be congenital or infantile depending on the age of onset or presentation. From a histologic point of view, hemangiomas can be cavernous or capillary depending on the size of the blood vessels within the tumor [10]. Capillary hemangiomas have smalldiameter vessels, while cavernous hemangiomas present large-diameter vessels [2,10]. Capillary hemangiomas have a characteristic pattern of vascular proliferation with a "trunkand-branch" aspect, surrounded by pericytes, with a relative number of mitoses, fibromyoid

stroma, and well-represented inflammatory infiltrate [11]. Cavernous hemangiomas have large vascular spaces lined with endothelium [12]. Ulceration of the epithelium or atrophy can appear on microscopic examination of a capillary hemangioma [13]. In the nose and paranasal sinuses, capillary hemangiomas are more frequently encountered than cavernous hemangiomas [10]. A subtype of capillary hemangioma is lobular capillary hemangioma, also known as pyogenic granuloma. It appears on the skin and in oral and nasal mucosa (especially the anterior nasal septum, turbinates, nasal vestibule, or nasopharynx) [3,4]. The etiology of lobular capillary hemangioma is not completely understood, but some theories take into account hormonal implication (particularly pregnancy and contraceptive use), injury, trauma, and viral infections [3,13,14]. Lobular capillary hemangioma can be encountered during pregnancy and is defined by the term "granuloma gravidarum". It is located within the nasal cavities, and the main symptom is recurrent unilateral epistaxis. Managing nasal hemorrhage during pregnancy can be challenging for the ENT surgeon. The treatment should be efficient but as conservative as possible and care should be taken when prescribing certain drugs. Mohd Yusof J. et al. consider chemical cauterization with silver nitrate and anterior nasal packing to be first-line treatment for mild epistaxis during pregnancy [15]. In case of severe nose hemorrhage, surgical intervention with general anesthesia is necessary to control the epistaxis; all measures should be taken to minimize the risks of general anesthesia to the fetus [15]. Another classification of hemangiomas takes into account the presence or absence of a protein named endothelial cell glucose transporter 1 (GLUT1) [16]. In infantile hemangiomas, GLUT1 protein is expressed, whereas in congenital hemangiomas it is not [16]. A noteworthy aspect regarding hemangiomas of the nose and paranasal sinuses is their late presentation in adults (around 40 years), different from hemangiomas with other locations that appear at birth or soon afterward [10].

The symptoms can vary and depend on the location and size of the tumor, but unilateral nasal obstruction, recurrent unilateral epistaxis, and headache are among the commonest [14,17,18]. Hemangiomas are benign tumors with a slow growing rate. Usually, the patient is asymptomatic for a long period. When symptoms appear, the tumor has a considerable volume and exerts a mass effect on adjacent structures. Unilateral nasal obstruction develops progressively and advances slowly. In some cases, the nasal obstruction can be accompanied by rhinorrhea or mucopurulent nasal discharge if the drainage pathway of the affected sinus is blocked by the tumor. If the tumor is located in the anterior part of the nasal septum, unilateral recurrent anterior epistaxis is the dominant symptom. The severity of nasal hemorrhage is variable from mild to moderate and severe. In cases of mild and moderate epistaxis, local hemostatic maneuvers (nasal packing, chemical cauterization of site of bleeding) will control the bleeding. In cases of severe epistaxis, hospital admission is necessary, and emergency surgical maneuvers to control the nasal hemorrhage are imposed. A peculiarity of capillary hemangioma developing exclusively in the sinus cavity is the lack of nose bleeds in the clinical presentation of the patient. If the tumor is limited to a sinus cavity, then headache or facial pain represents the prevailing symptom. The unilaterality of the symptoms (and of the lesion) should raise suspicion of malignancy [10]. Another particular aspect of a lesion limited to the sinus cavity is the possibility of developing bony erosion through mass effect and locoregional extension without invasion into the surrounding structures. In advanced cases with orbital implication, ocular symptoms (proptosis, reduced eye mobility, impaired vision, ocular globe displacement) will accompany the nasal ones [19]. When intracranial involvement is also present, the neurologic symptoms are associated with the nasal manifestations [1]. A great range of neurologic symptoms can appear from diplopia to neurologic deficits and signs of increased intracranial pressure [8]. In the presented case, the patient had a history of chronic bilateral nasal obstruction and recurrent headaches. The intensity and particular features of the headache during the flight motivated the patient to seek medical attention. Although the symptoms were alleviated after the treatment prescribed by the general ENT specialist, the patient continued the medical investigations.

The imagistic assessment of choice is enhanced computed tomography, which allows identification of the site of the lesion, its characteristics, and its interaction with the surrounding structures. The relationship between the tumor and the base of the skull and orbit should be thoroughly checked. Binesh et al. reported two cases of ethmoid capillary hemangioma associated with bone erosion of the lamina papyracea in both adults and children; one case presented extensive bone erosion into the nasal septum and cribriform plate with extension into the anterior cranial fossa [19]. Pas M. et al. presented a case of left ethmoid and sphenoid sinus capillary hemangioma with involvement of the left cavernous sinus, extensive bone erosion, and intrasellar and parasellar extension [1].

The specific aspect of a capillary hemangioma on CT is a soft-tissue enhancing lesion associated (or not) with bone erosion located in the nose and/or paranasal sinuses [18]. According to some authors, the bone erosion is a result of the compression on the bony structures and is not an invasion of the surrounding bones [20]. Kim J.H. et al. described capillary hemangiomas from their series as well-defined, round–oval lesions, with significant enhancement at an early phase and diminished enhancement at the delayed phase on CT [12]. The same authors describe the appearance of a capillary hemangioma on MRI as low-signal masses on T1-weighted images with marked enhancement on contrast T1-weighted images and central masses surrounded by a hypo-intense peripheric rim on T2-weighted images [12].

Sometimes the histological diagnosis of capillary hemangioma can be difficult due to the endothelial proliferation pattern that resembles malignant lesions and ulceration that corresponds to granulation tissue [14]. Differential diagnosis can be made with nasal angiofibroma (when the patient is an adolescent male juvenile, angiofibroma can be taken into account), angiomatous polyp of the nose and sinuses, polypoid granulation tissue, inverted papilloma, lymphangioma, hemangiolymphangioma, glomangiopericytoma, or angiosarcoma [9,18,19,21]. Angiofibromas contain large-diameter blood vessels and stellate fibroblasts, which differ from the small-diameter vessels encountered in capillary hemangiomas [19]. Hemangiolymphangiomas are rare, lymph-containing vascular tumors characterized by multiple lymph vessels surrounded by loose fibrovascular stroma [2,21]. Glomangiopericytomas present more cells and less endothelial lining than capillary hemangiomas [19]. Angiosarcomas present malignant endothelial cells with extravascular extension and an infiltrative pattern, whilst capillary hemangiomas possess normal endothelial cells with no extravascular extension [11]. Histologic examination and immunohistochemistry establish the type of tumor. The aspect of the lesion on endoscopy and imagistic assessment can guide the surgeon, preoperatively, toward the correct diagnosis.

Surgical excision of the tumor is the preferred treatment method, and endoscopic trans-nasal surgery is most frequently used. Biopsies should be performed with care because of the high risk of bleeding due to the vascular nature of the tumor; any surgical maneuvers should be executed only after imagistic assessment [10]. Significant bleeding after biopsy should be expected when manipulating vascular tumors, and proper methods of hemostasis are imperative. Endoscopic trans-nasal removal of the tumor is considered safe and effective [22]. Furthermore, endoscopic sinus surgery is considered a minimally invasive approach for sinus hemangiomas with limited complications, reduced morbidity, and decreased hospitalization [10]. The excision can be made with electrocautery, laser, or even cryotherapy. Endoscopic surgery of intrasinusal lesions allows adequate visualization of the tumor and identification of the risk elements. Depending on the site and extension of the tumor, zero-degree or angled endoscopes can be used. Using both types (straight and angled) of endoscopes, the ENT surgeon can properly assess the sinus cavity and identify any residual tumor. Power instruments such as microdebriders should be carefully manipulated within sinus cavities, especially in the vicinity of surgical risk structures (orbit, skull base, internal carotid artery, optic nerve). Dissection with endoscopic forceps is recommended when bone erosion is identified on preoperative imagistic assessment. Preoperative CT is essential to understand the particularities of sphenoid sinus anatomy and its relation with the internal carotid artery and optic nerve—the two main risk structures in

the area. Sphenoid sinus pneumatization is another factor that influences the effect on the internal carotid artery and the optic nerve. According to Fadda G.L.et al., the iatrogenic risk of injury of the aforementioned anatomic elements is higher when extensive pneumatization of the sphenoid sinus exists [23]. The presented case had significant asymmetry of the sphenoid sinus, with a small right sphenoid sinus and a wide left sphenoid sinus; this is a postsellar-type variation of pneumatization of the left sphenoid sinus. Due to the significant inequality of the sphenoid sinuses, both internal carotid arteries are in close proximity to the left sphenoid sinus. This makes them more susceptible to injury during sphenoid sinus approach. One study describes the postsellar variation as being less frequent in the studied population, but more commonly associated with protrusion of the internal carotid arteries and optic nerve within the sinus cavity [23]. Angiography with embolization may be performed before surgery, but there is no consensus among authors [6,14,20]. Preoperative embolization decreases the risk of significant bleeding during surgery and causes a regression of the tumor, allowing the ENT surgeon to manipulate the lesion and to properly dissect and ablate it. Due to the small number of reported cases and the lack of comprehensive studies, there are no available guidelines regarding the management of nasal and sinus capillary hemangiomas. Hasegawa et al. presented three cases of maxillary sinus hemangiomas that were embolized before surgery and limited perioperative bleeding was achieved (between 30 and 100 mL) [24]. Tzu-Hang C. et al. performed surgical excision of the tumor without prior embolization in all studied cases and reported no recurrence [20]. We performed endoscopic sinus surgery with no preoperative embolization in the presented case. Resection of the nasal septum and inferior turbinoplasty were necessary to create an adequate access pathway to the left sphenoid sinus and to improve nasal respiration. The particular features of the sphenoid sinus pneumatization in the presented case imposed a meticulous and prudent approach of the left sphenoid sinus cavity and its content. The choice of the adequate surgical technique and technology is adapted for every patient taking into account the effect of the technology on the healthy tissue surrounding the lesion and surgical risk elements in the vicinity [25].

The recurrence rate found in the literature varies from 0 to 42%; it depends on the study and follow-up period [20,26]. Bradshaw et al. consider that the recurrence rate depends on the technique and technology used for resection—8% recurrence rate for open excision and 40% recurrence rate for biopsy or electrocauterization—and advocate for complete resection of the tumor with a margin of healthy tissue to prevent recurrence [13]. The aforementioned authors also reported the possibility of spontaneously regression of the capillary hemangioma especially in adolescents, young adults, and pregnant women, but the regression process is not fully understood [13]. Smith et al. reported a 41.9% rate of recurrence for a mean follow-up interval of 58.6 months with a mean interval of 5.7 months between the surgery and the appearance of the recurrent tumor [26]. In their study, the presence of sinus capillary hemangiomas was limited: only one case of ethmoid lesion and no sphenoid sinus tumors. The same authors demonstrated a correlation between the age of the patient and recurrence; the mean age of the patients who developed recurrent capillary hemangioma of the nose and paranasal sinus was 50.1 years, whereas the mean age for non-recurrent tumor was 31.5 years [26]. Some authors state a 3.66% recurrence rate, but the follow-up period was relatively short (mean of 9 months) [27]. The management of recurrent capillary hemangioma is not standardized. Different approaches are available: surgical excision under general anesthesia, tumor ablation with local anesthesia, biopsy sampling, and electrocauterization. The study of Al-Ani et al., on 82 patients, demonstrated a left-side predilection of nasal capillary hemangiomas [27]. The case presented in this article was also a left-side tumor. In our case, at four months after surgery, both the endoscopic examination and brain MRI showed no residual tumor or recurrence. Taking into consideration the possibility of recurrence, we will continue follow up (clinic and endoscopic assessment every three to six months, and imagistic assessment after one year after surgery). An important aspect related to hemangioma recurrence is the lack of malignant transformation of the lesion [26].

The long-term prognosis of capillary hemangioma depends on the site of the lesion, the complete or incomplete removal of the tumor, and specific particularities of the patient (for example, pregnancy or other endocrinologic features) [8]. Given the complete removal of the tumor (assessed with enhanced head MRI four months after surgery), a favorable long-term prognosis is expected in this case. Nevertheless, the follow up will be realized as described above. The quality of life of the patient was improved after surgical resection of the tumor due to symptomatic relief. Improved nasal patency and absence of headaches were reported by the patient. The correct histologic diagnosis (histopathological examination and immunohistochemical analysis), according to the International Society for the Study of Vascular Anomalies, should be kept in mind when managing such cases [28,29].

#### **4. Conclusions**

Capillary hemangiomas are rare, benign vascular tumors encountered in the nose and paranasal sinuses. The clinical manifestations are not particular for this type of tumor, but the imagistic assessment can guide the surgeon to the correct diagnosis. The ENT specialist should have a high index of suspicion to diagnose capillary hemangioma within the nasal sinuses properly. Surgical resection of the tumor is the treatment of choice. Nowadays, endoscopic sinus surgery provides a good visualization of the surgical field and allows proper identification of the risk factors and correct assessment of the tumor. Complete resection of the tumor and the absence of malignant transformation (even for recurrences) are the two main features that advocate a favorable long-term prognosis for capillary hemangiomas.

Although this article represents a report of a single case of capillary hemangioma of the sphenoid sinus, the small number of cases reported in the literature make it relevant for the diagnosis and management of such tumors. Due to the lack of extensive studies of this diagnosis, there is no general consensus in its management nor in the postoperative rate of recurrence. The authors suggest that all encountered cases should undergo surveillance for a longer period of time in order to establish accurate statistical data.

**Author Contributions:** Conceptualization, R.H.; resources, A.V.D.; writing—original draft preparation, I.-G.I.; writing—review and editing, C.V., R.O.A.; visualization, C.D.S., C.A.P.; supervision, V.Z.; All authors have read and agreed to the published version of the manuscript.

**Funding:** This research received no external funding.

**Institutional Review Board Statement:** The study was conducted according to the guidelines of the Declaration of Helsinki in the current version and was approved by the local institutional ethics committee of "Prof. Dr. D. Hociota" Institute of Phonoaudiology and Functional ENT Surgery (protocol code 1764 and approved by 15 February).

**Informed Consent Statement:** Informed consent was obtained from all subjects involved in the study.

**Data Availability Statement:** Not applicable.

**Conflicts of Interest:** The authors declare no conflict of interest.

#### **References**


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