Surgical Ciliated Cyst Secondary to Orthognathic Surgery: Report of three cases and review of the literature


 Background: Surgical ciliated cysts (SCC) of the maxilla appear as a delayed complication after surgery in the maxillary sinus, midface osteotomies, traumatic tooth extraction, and maxillary fractures. They are defined as a lytic lesion with entrapment of the pseudostratified columnar epithelium.Report of three cases: We present three patients in which after orthognathic surgery a slowly enlarging asymptomatic swelling mass was developed. On CT, all the cases presented lytic expansive lesions in the alveolar ridge. In the three cases, lesions were completely excised, and upon histological examination, ciliated pseudostratified columnar epithelium with goblet cells was found so they were diagnosed as SCC. An exhaustive review of the medical literature was conducted. The PubMed database was searched for PubMed Central (PMC). 44 references were found, reporting 1555 cases: 11 series and 33 case reports, being the largest series from the Asian countries. The mean age was 46.5 years, and more frequently described in male patients. The most frequent form of presentation was as unilateral unilocular cysts in the posterior maxilla. They were described most frequently after a Caldwell-Luc approach. The average latency time was of 19.9 years.Conclusion: SCC is a rare complication after orthognathic surgery, but large series have been published, so maybe it could be interesting to include these cysts in the next Edition of the World Health Organization Classification of the Head and Neck Tumors: Odontogenic and Maxillofacial Bone Tumors, making clear the difference between SCC and mucoceles to avoid future confusions.


Introduction
Surgical ciliated cysts (SCC) were rst described by Kubo et al. In 1927 [1] as a maxillary cyst secondary to a chronic maxillary sinusitis surgery. These cysts have also been termed as postoperative maxillary cysts and as postoperative paranasal cysts [2]. The clinical presentation may be variable, with some patients showing poorly de ned pain, a painless mass, or even completely asymptomatic patients. They can be unilateral or bilateral and have been described as unilocular or multilocular lytic lesions. No side predominance has been found. The latency from the causal previous surgery to the appearance of the cyst ranges from months to several decades, making sometimes the diagnosis di cult.
Most of the reports and scienti c papers come from the Asian literature and most often from Japan [3][4][5], but in the last years, many authors all over the world have described this entity. However, there are important differences about the size of the series (larger series coming from Asia and shorter ones from Occidental countries) and about the given details of the cases (scarce in Asian papers and thorough in Occidental reports. This difference may come from the exact de nition and/or classi cation of SCC, so a deeper study is needed.
The aim of this paper is to review the existing literature and report the experience of our centers with this entity.

Case Report
In the last 7 years, there have been three cases of SCC in our hospital. An overview of the characteristics of our series is shown in Table 1.

Case 1
A 31-year-old female with severe skeletal class III malocclusion underwent orthognathic surgery. A Le Fort I maxillary osteotomy with horizontal advancement of 10 mm and a 5 mm vertical augmentation combined with autogenous iliac bone graft was performed in 2007 ( Figure 1). One year later, in 2008, 8 implants were placed in the upper maxilla, and in 2009 two implants were explanted on the left side, and cranial vault bone graft was placed and xed with screws.
Five years later, in 2013, she developed a slow-growing progressive swelling on the left posterior maxillary region of two months of evolution.
A dual-Energy CT after intravenous contrast administration was performed ( Figure 1). On the right maxilla, a newly unilocular lytic expansive lesion was found, with marked thinning of the cortical bone. On the left posterior maxilla alveolar region, a smaller lytic expansive lesion could also be detected. On the iodine map, no enhancement was proved inside the lesions. Neither periosteal reaction nor cortical disruption was present. The surrounding tissues and the underlying dental pieces had a standard appearance.
With the radiological diagnosis of SCC, the patient underwent surgery, whereby the cyst of the right upper maxilla was completely enucleated and lled with lyophilized bone.
The lytic lesion of the left upper maxillary was conservatively treated with careful observation during follow-up.
Histopathological examination of the surgical specimen showed ciliated pseudostrati ed columnar epithelium with goblet cells and with an underlying capsular brous tissue partially hyalinised ( Figure 1). These ndings were compatible with SCC.
The patient remained asymptomatic for 6 years, but in 2019 she appeared with pain and swelling on the left upper maxilla, with signs and symptoms of maxillary infection. CT scan revealed that the pre-existing lytic lesion in the left side had increased substantially in size; consequently, a new surgical procedure was required; the cyst was enucleated and lled with lyophilized bone (images not shown).
The patient was scheduled for surgery, in which the surgical hardware was removed and the cyst was enucleated and lled with demineralized lyophilized bone matrix.
The histological analysis showed a cystic cavity lined exclusively by respiratory epithelial tissue, containing scarce mucous and ciliated cells. The cyst wall contained chronic in ammatory in ltrate and the cystic content contained a varied amount of in ammatory cells represented by neutrophils.
The patient has had no symptoms up till now.

Review Of The Literature
In order to carry out a systematic review, the Prisma protocol was approached. The questions that have been answered in this study are: (a) what are speci cally surgical ciliated cysts?, (b) how often do they appear?, (c) is there a race predominance? A search was carried out among articles in electronic databases of Pubmed, Embase, Cochrane Library, Scopus, and Google Scholar. The search strategy was based on Mesh vocabulary and the combination of these words was done with logical operators, "AND" and "OR" in search phrases, including the keywords "postoperative maxillary cyst", "secondary mucocele", "surgical ciliated cyst", "respiratory epithelium lined cyst", "postoperative mucocele", and "ectopic ciliated cyst", with no date lter. No language lter was used, and therefore papers in English, Japanese, German, Portuguese, and Polish, among others, were reviewed. First, the articles were screened based on title, abstract, and objective of the study, and their texts were retrieved. Then the whole text was analyzed and investigated and nally, 61 articles were selected.
Data collected from the papers were: country, age, location of the cyst, etiologic previous surgery, latency from the previous surgery to the appearance of the cyst, and recurrence.

Results Of The Literature
A total of 61 articles describing surgical ciliated cysts were found, describing 1857 patients. Of these articles, 44 were case reports (including 47 patients) and 17 series (with 1810 patients), in both single-center and multi-center studies ( Table 2). Papers were from 19 different countries, being Japan the country where most of the cases were registered (1779 cases described in 18 articles). The United Kingdom (with 28 patients in 6 papers) and the USA (with 16 cases in 12 papers) were the followings by frequency. The rest of the countries published a short local series or case reports.
The location of the cysts was analyzed per side and affected part of the maxilla. 160 patients were reported to have a unilateral cyst, 25 patients presented bilateral cyst, and 7 patients had a midline cyst. Unfortunately, the speci c affected side was not described in larger series, so no there are no available data from the rest of the cases. The affected part of the maxilla was described in 437 patients; among these, the most referred affected part was the maxillary sinus and the posterior and lateral part of the maxilla (Table 3). 1420 records did not show the exact location in the maxilla or any location at all.
The previous surgery was speci ed only in 96 cases, being the Caldwell-Luc procedure the most common one, comprising 58.3% of the cases. In all the other cases, the initial surgery was described as "antral surgery" (in the largest series, the Japanese one from Nishioka et al [6]), "undescribed" (in the second largest series, the one by Kimizuka et al [7]), "maxillary radical surgery", or "maxillary surgical intervention". Of these patients, only 20 cases developed the SCC speci cally after orthognathic surgery, 16 cases after a LeFort I osteotomy (alone or combined with other procedures) [3][4][5][8][9][10][11][12][13], 3 cases after a bimaxillary orthognathic surgery [14,15], and 1 patient after a LeFort II naso-maxillary advancement (Henderson-Jackson technique) [11] The average time of latency for SCC after the rst surgery was 20.1 years (range: 0.5 -60.0 years). Only 3 papers described relapses (a British case from the paper of Sugar et al [11], one of the cases of Kimizuka et al [7], and 3 cases from the series of Higuchi et al [16]), describing no recurrence of 32 cases in 24 papers (mostly in case reports), but the remaining 34 papers did not mention anything about relapsing.

Discussion
In this paper, three patients with surgical ciliated cysts (two female and one male) have been described. The ciliated cysts appeared after a 2, 5, 12, and 20 years period, respectively, after orthognathic surgery. In one case, there was a small cyst in the contralateral maxilla that was considered initially to be observed, but it increased signi cantly its size after 6 years, so 4 SCC have been included in our series in 7 years.
Our series is a short one, with four SCC in three patients. Given that the usual way to communicate cases in the occidental area is one of the single case reports, we think our series will help in increasing the database of SCC and maybe clarifying some of the previous concerns.
The mean age of our three patients was about 10 years lower than the described in the literature. The location of the cysts was the posterior maxilla in all cases, tie in with the reported cases all over the world. Most of the SCC described in the literature were unilocular, but also, much less commonly, multilocular, with no differences in the evolution of both types; we presented two unilocular cysts and one bilobulated.
The previous surgery was a LeFort I procedure previous in all the cases, as described in other SCC in the literature [3][4][5][8][9][10][11][12][13], where it is not clear why there are so few cases associated with orthognathic surgery.
The term "postoperative maxillary cyst" or "SCC" refers to a delayed complication arising years after surgery involving the maxillary sinus. They are most commonly associated with a history of surgery for maxillary sinusitis, particularly Caldwell-Luc procedure, but may also result from gunshot injuries, fractures of the malar-maxillary complex, midface osteotomies and after orthognathic surgery and traumatic tooth extraction in the mandible [12,15,[17][18][19][20][21][22][23]. A comprehensive patient medical record is of particular importance in guiding towards the nal diagnosis, as it played a signi cant role in the diagnosis of the three cases here presented.
It is commonly found in the literature that the rst author that described the surgical ciliated cyst was Kubo in 1927 [1]. He described a frequent cyst in the Japanese population, that represented as much as 20% of all the oral cysts, being uncommon in occidental areas [1,24]. After that rst publication, we have found 60 articles referring to surgical ciliated cysts.
Cystic lesions found in the maxillary sinuses can be pseudocysts (with no epithelium in their walls) or real cysts (with a lining epithelium). Among the last ones, mucoceles, odontogenic cysts, bone cysts, ssural cysts, postsurgical maxillary cysts, and other non-odontogenic cysts are included. Pseudocysts do not show a wall of the epithelium, but a cavity lled with an in ammatory exudate, surrounded by a dense compact layer of connective tissue under the sinus mucosa, originating from the accumulation of that in ammatory exudate of the bone and pushing the periosteum and the sinus epithelium into the sinus cavity. Mucoceles, otherwise, show a lining of respiratory epithelium (pseudostrati ed ciliated epithelium with goblet cells) and can be classi ed as primary (retention mucous cysts without a known etiology) and secondary (originate from a known cause, like a chronic obstruction of the ostium of the sinus, an in ammation of the mucosa, previous surgeries on the sinus or close to it, chronic infections…) [9,[24][25][26].
Surgical ciliated cyst can be considered a secondary mucocele. Simply, the difference between SCC and a secondary mucocele should be based on the growing pattern: mucoceles grow from the inside of the sinus in a centrifugal way, expanding the walls of the maxillary sinus; on the other hand, surgical ciliated cysts grow inside the trabecular bone, and from there they expand centrifugally. Since the epithelium of both lesions is respiratory, that is to say, a pseudostrati ed ciliated cylindrical epithelium, lesions where the real origin cannot be determined except for the surgical episode can be found [9,[27][28][29][30].
A wrong interpretation of the histologic ndings should also be considered. For instance, if an odontogenic cyst grows enough to protrude over the maxillary sinus mucosa, and in the resection surgery the cyst is obtained in several parts, the pathoanatomic study can mislead the respiratory mucosa of the sinus with the wall of the cyst, thus classifying the lesion as a SCC. The nding of respiratory epithelium in a cyst does not make it a surgical ciliated cyst even if the patient could have received previous surgery.
Japanese literature offers a very high incidence of SCC. There are some reasons for these comparatively high gures: (1) a publication bias, where the reported cysts were not real SCC, and it could be considered if they were expansive mucoceles [27][28][29][30]33,40]. (2); differences when performing a Caldwell-Luc procedure, but we consider it less probable since the procedure is a worldwide standard one [32,33]; (3) a different pattern of the facial bone structure of the Japanese population compared with the Occidental one [6,37]; (4) a different bacterial ora colonizing the paranasal sinuses in the Japanese population [6,11,37,45]; (5) the more common surgical treatment of the chronic sinusitis during the II World War when antibiotics were scarce, although this nding would not support the persistent high gures in the past decades until today [10,11,31]. That is why we hypothesize that the real difference in the incidence of SCC should not be so striking between Asian and Occidental countries; a possible mistake in the interpretation of the histologic ndings, as previously referred, or a classi cation bias, should be rethought.
Regarding treatment, symptomatic SCC has a surgical indication. Some different techniques have been proposed: simple cystectomy, cystectomy, and antrostomy, marsupialization… being all of them effective. The recurrence rate is extremely low.
The surgical ciliated cyst in the maxillary territory, although it is an entity described in the scienti c literature, is neither included nor classi ed in the "4 th Edition of the World Health Organization Classi cation of the Head and Neck Tumors: Odontogenic and Maxillofacial Bone Tumors" [25,26,46,47]. Since there are more than 1850 cases reported in the literature and 61 papers, maybe it could be interesting to include these cysts in the next edition, with a new de nitive classi cation of the cysts that would not lead to confusion, making clear the difference between SCC and mucoceles to avoid future confusions.