Preservation of Palatal Mucosa in Rhinomaxillary Mucormycosis Cases

Abstract

Introduction

Mucormycosis is an aggressive, life-threatening infection that requires prompt diagnosis and early treatment. Depending on the severity of the disease, rhinomaxillary mucormycosis (RMM) may necessitate maxillectomy, ranging from partial to total removal. The implementation of primary closure leads to improved functional ability by creating a separation between the oral and nasal cavities, which facilitates oral intake and reduces the duration of nasogastric feeding. This, in turn, enhances the patients' quality of life. The objective of this study was to evaluate the effectiveness of primary closure using palatal mucosa (PM) following maxillectomy in patients with RMM.

Methodology

We conducted a retroprospective study to analyze the outcomes of 32 operated cases of rhinomaxillary mucormycosis (RMM). After maxillectomy, we preserved highly vascular uninfected palatal mucosa to close the maxillary defect. The study spanned 4 months, encompassing 4 months of retrospective data collection and 3 months of prospective data collection.

Results

During the 3rd month follow-up, complete closure and uptake of the flap were observed in 22 patients. At the 6-month follow-up, 28 participants exhibited total uptake of PM, with no oro-antral/nasal communication.

Conclusion

This study concludes that in most circumstances, employing a PM flap to close the defect after maxillectomy and surgical debridement is a successful approach as it reduces the occurrence of oro-antral/oro-nasal communication.

Introduction

Mucormycosis, previously referred to as Zygomycosis, stands as a rare and severe fungal infection resulting from a collection of molds termed Mucormycetes. The typical mode of infection in immunocompromised individuals involves inhaling fungal spores, predominantly affecting the sinuses and/or lungs [1, 2]. Subsequent to sinus involvement, the fungus advances to rhinomaxillary/sino-maxillary/rhino-orbitomaxillary mucormycosis through angioinvasion. Swift diagnosis and concurrent application of surgical and medical interventions play a pivotal role in effectively managing this life-threatening ailment. Given mucormycosis' primary engagement with bone, the palatal mucosa (PM) is frequently unscathed or experiences minimal involvement. During surgical debridement, disease-free vascularized palatal mucosa can be conserved for primary closure, creating a barrier between the nasal/maxillary sinus and oral cavity, thus enhancing overall quality of life.

While a handful of surgeons have adopted this practice, the success rate of primary closure utilizing palatal mucosa has not been subjected to comprehensive study. One contributing factor is the infrequency of the ailment until the recent surge in cases of COVID-19-associated mucormycosis. Having managed over 150 instances of COVID-19-associated mucormycosis with varying degrees of involvement, our institution could scrutinize cases of rhinomaxillary mucormycosis (RMM) involving the use of PM. This study aimed to assess the efficacy of primary closure through palatal mucosa subsequent to maxillectomy in patients with RMM. The primary objective was to ascertain the presence of oro-antral/oro-nasal communication subsequent to the closure of the maxillary defect employing a palatal flap. Secondary outcomes under scrutiny included:

• Continuity of the palatal flap–alveolar mucosa junction

• Vascularity of the palatal flap (pinprick test)

• Requirement for secondary surgical closure

Our hypothesis postulated complete integration of the PM flap with the absence of oro-antral/oro-nasal communication.

Materials and Methods

Study Design and Aim

The study was designed as an ambispective investigation conducted over a span of 3 months within the Department of Dentistry at AIIMS, Raipur. The research aimed to explore the outcomes of primary closure using preserved palatal mucosa in patients who underwent surgery for rhinomaxillary, sino-maxillary, or rhino-orbito-maxillary mucormycosis. Ethical clearance was obtained prior to commencing the study through Institutional Ethics Committee approval (AIIMSRPR/IEC/2022/1168).

Operational Definitions

Operational definitions included “Primary Closure,” denoting the direct side-to-side apposition of a skin defect or laceration; “Palatal Mucosal Flap,” referring to the uninfected, keratinized, highly vascular mucoperiosteum over the bony palate used for defect closure; and “Dehiscence,” indicating the separation of facial layers shortly after surgery. Additionally, “Oro-Antral Fistula” was defined as an epithelialized pathological communication between the oral cavity and maxillary sinus.

Study Encompassment and Exclusions

The study included patients who met specific inclusion criteria, diagnosed and operated for the mentioned mucormycosis types with palatal involvement where primary closure of the defect was performed. Exclusion criteria encompassed patients who were not willing to participate or were lost to follow-up.

Clinical Parameters Evaluated

The clinical parameters evaluated in the study included the success of primary closure, occurrence of dehiscence or oro-antral fistula, and positive pinprick test results. The latter was defined as the appearance of a drop of blood on the flap surface within a maximum of 5 s after a full needle extraction.

Study Duration and Data Collection

The total study duration extended over 4 months, spanning from November 2021 to February 2022. Within this timeframe, our study employed an ambispective approach. Initially, 3 months of retrospective data were meticulously collected from hospital medical records, covering the postoperative period for the same cohort of patients. Subsequently, an additional 3-month prospective follow-up was conducted for these patients, allowing for a comprehensive evaluation of outcomes and observations within the same cohort. This integrated ambispective design facilitated a thorough analysis of both retrospective and prospective data within a unified patient group. A list of patients operated for KOH/histopathological-proven RMM under the Department of Dentistry, AIIMS, Raipur, was compiled. From this list, patients who were in regular follow-ups were selected. Subsequently, the intraoperative notes of each case were collected.

Participant Count

A total of thirty-two participants were deemed eligible for the study.

Operative Procedure

A biopsy and nasal endoscopic examination were performed on patients with a provisional diagnosis of mucormycosis. Once the diagnosis was histopathologically confirmed, amphotericin injection was initiated and continued for a duration of approximately 1000–2000 mg over 3–8 weeks. The operative procedure comprised meticulous steps. Lignocaine with vasoconstrictor was administered into the maxillary vestibule and palatal mucosa for local anesthesia. A crevicular incision, accompanied by a 45-degree releasing incision at the distal end, was precisely made buccally. The mucoperiosteal flap was then carefully elevated to provide a clear view of the extent of necrotic maxillary and zygomatic bone, tailored to the unilateral or bilateral disease spread. Palatally, another crevicular incision was created, elevating the palatal mucosal (PM) flap to expose the diseased palatal bone. When a sinus opening was present in the palatal or bucco-labial mucosa, the sinus lining was removed. In cases of extensive palatal mucosa involvement, necrotic tissue was skillfully debrided, preserving only intact PM for later closure (Fig. 6). Complete or partial maxillectomy and surgical debridement were performed as needed. Using a curette, the necrotic layer on the sinus or nasal side of the palatal flap was removed. By meticulously undermining the tissue surrounding the area of interest, we aimed to alleviate the constraints imposed by the tissue's natural resistance. This method allowed for greater flexibility and maneuverability during the procedure, facilitating the required extension and manipulation of the palatal mucosa. To ensure healthy mucosa preservation, a tissue biopsy was taken from the preserved mucosal margins. The PM and buccal/labial flap were meticulously approximated, achieving closure using Vicryl 3-0 horizontal mattress sutures (Fig. 7). Postoperatively, patients were placed on strict nasogastric tube feeding for 3 weeks or more, based on healing progress and overall patient condition. Patients were provided with comprehensive instructions for oral hygiene maintenance, including the potential need for daily irrigation and dressing procedures if necessary.

Fig. 6.

Intraoperative photo showing uninvolved palatal mucosa being preserved for primary closure after maxillectomy

Fig. 7.

Primary closure using palatal flap

Study Initiation and Progress Tracking

The study was initiated during the 3-month follow-up period of most patients. Informed consent was obtained, and retrospective data collection was conducted, including detailed disease extent, surgical procedure, and initial healing process. Thus, the study was considered a retroprospective study. Daily progress during the recovery period was recorded for all patients, focusing on wound dehiscence, oro-antral/nasal communication, and the extent of any present defect.

Prospective Clinical Evaluations

Prospective clinical evaluations were conducted during the 3-month and 6-month follow-up visits. Clinical evaluation included assessing the vascularity of palatal mucosa, continuity of the flap–alveolar mucosal junction, and the presence of oro-antral/nasal communication.

Confirmation of Oro-Antral/Nasal Communication

• History: During each follow-up visit, patients were asked if they experienced nasal regurgitation of fluid.

• Clinical inspection: A thorough clinical examination was conducted.

• Confirmation of oro-antral communication: The Valsalva method was used to confirm the presence of oro-antral communication. The patient was instructed to expel air against closed nostrils while the health-care professional checked for any hissing sound indicating air leakage from the fistula into the mouth, which suggested a positive test.

Data regarding the need for any secondary surgery were collected, including the reason for the surgery and the specific surgical procedure performed. The collected data entries were tabulated and further subjected to statistical analysis.

Results

The primary outcome assessed was the presence of oro-antral/oro-nasal communication following the closure of the maxillary defect with a palatal flap. The secondary outcomes studied were the continuity of the palatal flap–alveolar mucosa junction, vascularity of the palatal flap (pinprick test), and the need for secondary surgical closure.

Out of the 32 patients included in the study, nine were female, and 23 were male; age of patients ranged between 28 and 78 years. There was no loss of follow-up. Total maxillectomy was done in 17 patients, and rest partial maxillectomy was done. Dehiscence was observed in 6.25% of cases during the 7th day follow-up (Figs. 8 and 9), with two out of 32 patients presenting with dehiscence. Secondary surgery was performed on six cases (18.75%) between the initial surgery and the 3rd month. The secondary surgical closure was done using local and regional flap including buccal flap pad and temporalis flap. During the 3rd month follow-up, oro-nasal/oro-antral communication was identified in 10 patients, accounting for 31.25% of the patients. In contrast, 22 patients (68.75%) showed complete uptake of the flap and closure of the defect, successfully separating the oral and nasal/sinus cavities (Fig. 1). In some cases, re-suturing was required due to dehiscence. Six patients required a second surgery to close oro-antral communication, with the buccal fat pad commonly used in five participants and the temporalis flap being harvested in one participant. During the 6-month follow-up, four patients still had oro-antral communication, while complete closure was achieved in 28 cases (Figs. 10 and 11). In all the patients, the histopathological evaluation of biopsy done from margin of mucosa was negative for any fungous, thereby ensuring that the tissue was not diseased. At the 6th month follow-up, the loss of continuity of mucosa between the palatal and buccal mucosa persisted in four patients, despite secondary surgeries and other efforts to close the defect. This accounted for 12.5% of all cases (Fig. 2).

Fig. 8.

Intra-oral photo during the 3rd month follow-up showing uptake of PM flap. Oro-antral communication is noted in three different sites

Fig. 9.

Intra-oral photo showing dehiscence in the left maxilla along the suture line

Fig. 1.

Distribution of patients according to the presence of oro-nasal/oro-antral communication during 3 months follow-ups

Fig. 10.

Intra-oral photo showing complete healing during 6 months follow-up

Fig. 11.

Intra-oral photo showing complete healing following total maxillectomy during 6 months follow-up

Fig. 2.

Distribution of patients according to the need for secondary closure from the first surgery to 3rd month postoperatively

Discussion

Mucormycosis is an aggressive, life-threatening infection requiring prompt diagnosis and early treatment. It mainly affects people who are immunocompromised or patients already infected with other diseases. High-risk groups include people with diabetes (especially diabetic ketoacidosis), solid-organ transplantation, neutropenia, long-term systemic corticosteroid use, and iron overload (hemochromatosis) [2].

The incidence rate of mucormycosis globally varies from 0.005 to 1.7 per million population. In India, the prevalence of mucormycosis in the year 2021 was estimated as 140 per million population, which is about 80 times higher than the prevalence in developed countries. Following the surge of COVID-19-associated mucormycosis and the Government of India directive, several states in India made mucormycosis a notifiable disease in May 2021 [2]. Of various forms of mucormycosis, those that are common in the head and neck region are rhinomaxillary, sino-maxillary, and rhino-orbit-maxillary mucormycosis. The usual presentation of rhinomaxillary mucormycosis (RMM) is swelling, paresthesia over cheeks, nasal obstruction, mobility of teeth, multiple pus-draining sinuses in the buccogingival sulcus and palate, palatal perforation, and bone exposure (Figs. 3, 4, 5, 6, 7, 8, 9, 10, and 11).

Fig. 3.

Pre-operative photos of a patient infected with mucormycosis, showing necrotic bone exposure intraorally

Fig. 4.

NCCT image of patient with mucormycosis. The left maxillary sinus obliteration and erosion of the left maxillary can be appreciated

Fig. 5.

Clinical photo of a histopathologically proven case of mucormycosis, showing edematous palatal mucosa. The patient had multiple mobile teeth and a history of SARS-CoV infection 1 month before reporting to us

Successful management of this deadly disease is early diagnosis, concurrent surgical and medical management, including antifungal therapy, and correction of underlying medical disorders such as ketoacidosis. A definitive diagnosis of Zygomycosis caused by Mucorales is made by histopathological examination with or without isolation of the fungus from the same site. Antifungal medications commonly administered are amphotericin B and posaconazole. Surgical management in rhinomaxillary mucormycosis involves maxillectomy ranging from limited maxillectomy to total maxillectomy depending upon the extension of the disease, along with paranasal sinus debridement [4]. Extra-oral or intra-oral vestibular incision is given for access, followed by blunt dissection to expose diseased bone, which is osteotomized and removed.

As the mainstay management, maxillectomy and aggressive surgical debridement lead to a large open defect, depending upon the extent of fungal involvement, exposing the maxillary sinus, zygomatic bone, nasal cavity, floor of the orbit, and/or orbital cavity; primary closure will lead to better functional ability as separation of the oral and nasal cavity will be restored, facilitating oral intake and thereby reducing the duration of nasogastric feed. It eliminates the need for an obturator following maxillectomy. Arterial thrombosis, occlusion, and vascular extension of the disease in mucormycosis may affect the versatile use of flaps for reconstruction [3].

Our study showed that complete closure was achieved in 68.75% of the case by 3 months and 87.5% by the end of 6 months, suggesting that palatal flap gives good results when used for primary closure after maxillectomy. In the remaining 31.25% (at the end of 3 months) cases, the oro-antral/nasal communication defect size varied; on an average defect, size was 1.5 cm in diameter. Some of these defects were closed during the study (5 out of 32) by using the buccal fat pad and temporalis myofascial flap (1 in 32). Closure of oro-antral communication was carried out only after confirming that there is no recurrent/residual disease. The buccal fat pad gave a good result with complete closure in all five cases. At the end of the study, four participants had persistent communication, which was planned for later closure.

As mucormycosis infection mainly involves bone, palatal mucosa is often left disease-free/with minor involvement. Preservation of this disease-free, vascularized palatal mucosa after debridement can act as a vital option in the primary closure of maxillectomy defects, provided that the vascular supply is not violated, and infrastructure maxillectomy is carried out. Careful dissection and preservation of the greater palatine vessels and descending palatine vessels are crucial in maintaining the viability of the palatal flap [3]. The palatal flap has the advantage of being simple, with abundant blood supply and no extra surgical site or donor site morbidity. Contradictory to the common belief of obliterating dead space with some material like a roller gauge pack, we closed the dead space by PM, which provides a relatively firm separation between nasal oral and nasal cavity, aiding in later mid-face reconstruction using various options available like the zygomatic implant, basal implant, and patient-specific implant-supported prosthesis as the chance of infection of an implant is reduced by bony margins separation from the oral cavity and thus aiding in better osteointegration. In certain aggressive cases, the palatal mucosa is black in color, with necrosis involving the whole of the palatal mucosa where the pinprick test is negative; in those cases, the PM flap cannot be used but rather should be excised (Table 1).

Table 1.

Distribution of patient's age and sex with data recorded on the 3rd month follow-up

Name	Age/sex	Oro-nasal communication	Vascularity of palatal flap (prick test)	Dehiscence
A	56/M	Absent	Positive	Absent
B	68/F	Present 2 mm × 2 mm left buccal vestibule	Positive	Absent
C	76/M	Absent	Positive	Absent
D	55/M	Absent	Positive	Absent
E	48/M	Absent	Positive	Absent
F	75/M	Present 1.5 × 02 cm along the anterior maxilla	Positive	Absent
G	78/F	Present 2 mm × 3 mm along the right buccal and labial vestibule	Positive	Absent
H	57/M	Present 2 cm × 2 cm right palate, 1 cm*0.2 cm right buccal vestibule	Positive	Absent
I	65/M	Absent	Positive	Absent
J	62/F	Absent	Positive	Absent
K	51/M	Present 1 cm × 1 cm in mid-palate	Positive	Absent
L	49/M	Absent	Positive	Absent
M	55/M	Present 1 cm × 1 cm left buccal-labial vestibule	Positive	Absent
N	49/M	Absent	Positive	Absent
O	28/F	Absent	Positive	Absent
P	47/M	Present 1.5 × 1 cm along the right buccal vestibule	Positive	Absent
Q	66/M	Absent	Positive	Absent
R	50/M	Present 5 mm × 7 mm along the right buccal vestibule	Positive	Absent
S	75/F	Absent	Positive	Absent
T	38/F	Absent	Positive	Absent
U	53/M	Present 2 mm × 1 cm along the left buccal vestibule	Positive	Absent
V	48/F	Absent	Positive	Absent
W	71/M	Absent	Positive	Absent
X	58/M	Absent	Positive	Absent
W	67/M	Present 2 × 2.cm along the left buccal vestibule	Positive	Absent
Z	53/F	Absent	Positive	Absent
AA	45/M	Absent	Positive	Absent
BB	60/M	Absent	Positive	Absent
CC	54/M	Absent	Positive	Absent
DD	72/M	Absent	Positive	Absent
EE	64/M	Absent	Positive	Absent
FF	49/F	Absent	Positive	Absent

Limitations of this study are limited sample size. Also, as the patients were selected with RMM, more extensive lesions with cranial and orbital involvement were not included to maintain homogeneity, but this could lead to selection bias.

Conclusion

The study concludes in most circumstances, closing the defect with a PM flap after a maxillectomy and surgical debridement is a successful approach as it lessens oro-antral/oro-nasal communication.

Funding

None.

Declarations

Conflict of interest

The authors declare that they have no conflict of interest.

IEC approval

IEC AIIMS RAIPUR AIIMSRPR/IEC/2022/1168.