Synchronous nasal rhinosporidiosis and inverted papilloma in a paediatric patient in Dodoma, Tanzania: Case report

Abstract

Introduction

Nasal rhinosporidiosis refers to a rare chronic granulomatous disease caused by Rhinosporidium seeberi. It affects the mucous membrane of sites such as nasopharynx, conjunctiva and palate. Inverted papillomas are relatively rare and are benign epithelial tumors of the nasal cavity that are locally aggressive, exhibit recurrence tendency and malignant transformation. Both entities are very rare in our setting and this is perhaps the first documented case in Tanzania.

Case presentation

The patient was a 7-year old boy with a 1-year history of left-sided nasal obstruction and intermittent epistaxis for 6 months. He had no history of cheek swelling, pain or numbness, loss or loosening of teeth or alveolar ridge fullness. There were no ophthalmological, otological or neurological complaints reported. Endoscopic excision of the nasal mass was done and histopathological analysis confirmed co-existence of rhinosporidiosis and inverted papilloma. Postoperatively, the patient was kept on oral dapsone at a dose of 50 mg/day for 6-months and with no residual disease recurrence noted after 6-months follow up.

Clinical discussion

The patient underwent endoscopic excision of the nasal mass and histopathological analysis confirmed co-existence of rhinosporidiosis and inverted papilloma. Postoperatively, the patient was kept on oral dapsone at a dose of 50 mg/day for 6-months and with no residual disease recurrence noted after 6-months of follow up.

Conclusion

Nasal rhinosporidiosis and inverted papilloma lesions may resemble the routinely encountered nasal polyps thus important for both clinicians and pathologists to have a high index of suspicion when managing patients with nasal masses even from non-endemic areas.

Highlights

• •Nasal rhinosporidiosis is a chronic granulomatous disease caused by Rhinosporidium seeberi
• •Rhinosporidiosis affects mucous membrane of nasopharynx, conjunctiva and palate.
• •Inverted papillomas are relatively rare, benign tumors of the nasal cavity
• •Inverted papillomas are locally aggressive, have recurrence rate in 14-78% of cases and undergo malignant transformation.
• •Transnasal endoscopic resection remains to be the treatment of choice for rhinosporidiosis and inverted papilloma

1. Introduction

Nasal rhinosporidiosis refers to a chronic granulomatous disease of the nose that is caused by Rhinosporidium seeberi [[1], [2], [3], [4]]. Both human beings and animals are affected by rhinosporidiosis. It has been reported more commonly in hot tropical climates even though it is endemic in India and Sri Lanka [1,[5], [6], [7], [8]]. On the other hand, sporadic occurrence has been reported in Brazil, Africa and Argentina [6,7,9,10]. Despite the disease being very rare in Tanzania, there are some countries that have reported an appreciable number of cases [8].

There is no racial predominance reported in nasal rhinosporidiosis and in terms of sex predilection, males outnumbered females with male to female ratio being 4:1 [1,[9], [10], [11]]. Regarding the commonly affected age, the disease affects those individuals aged 15–40 years [1,2,12].

The mode of transmission of rhinosporidiosis may be by direct contact with spores and this can be through dust, infected clothing and swimming in stagnant water [1,8,[12], [13], [14]].

Diagnostic evaluation of nasal rhinosporidiosis involves observing the hallmark features of the involved etiology in nasal tissue biopsies like presence of sporangia. The sporangia when examined in nasal tissue biopsies may be visible at variable stages of maturation. Moreover, rhinosporidiosis has a tendency of mimicry where it may resemble other polypoidal nasal masses [1,7,[15], [16], [17]]. A high index of diagnostic suspicion by clinicians is important in guiding the management of patients with nasal masses particularly in this era where the disease is on surge [1].

Patients with nasal rhinosporidiosis may present with an indolent nasal mass, nasal obstruction, intermittent epistaxis, nasal itching, sneezing, blood stained and occasional yellowish purulent nasal discharge [1,9,10].

Despite high recurrence rate, the treatment of choice for nasal rhinosporidiosis is usually surgical excision of the nasal mass [3,16,18]. On the other hand, there are reported deaths in patients who are not immunocompetent despite being amenable to surgery [19]. During surgery, electro cauterization of the base of the excised site should be done though cryosurgery can also be used [20]. Systemic therapy with dapsone is a recommended adjuvant therapy in patients with nasal rhinosporidiosis [1,20].

To the best of our knowledge, this is perhaps the second reported case of nasal rhinosporidiosis in Central Tanzania and the first case of its unique nature due to synchronicity with inverted papilloma.

Being a rare benign tumor, inverted papilloma was described initially in 1854 by Ward and in 1855 by Billroth [20,22]. Inverted papilloma accounts for 0.5–4 % of all nasal tumors [20,23]. The disease has a peak in the 5th to 6th decade [23] with male to female ratio being between 3:1 and 10:1 [20]. It is unique among paediatric patients by its rarity due to limited reported cases [24]. Inverted papilloma exhibit a tendency of malignant transformation to carcinoma, local aggressiveness, high risk for synchronous or metachronous malignancy and also has higher chances of local recurrence especially upon incomplete surgical excision [[22], [23], [24]].

The most common anatomical location for inverted papilloma is the lateral nasal wall and the paranasal sinuses though there are other involved rare extra-sinonasal sites such as skull base [25], nasolacrimal duct [26], oropharynx [27,28] and nasopharynx [29,30].

The exact implicated etiology for inverted papilloma is still unknown to date though it has been hypothesized that Human papillomavirus may be implicated in its aetiopathogenesis; particularly type 11 [[31], [32], [33], [34], [35]]. Other implicated etiology includes chronic inflammation, allergy and occupational exposures [23,33]. The treatment of choice for inverted papillomas has been surgical excision of the nasal mass [23,26]. However, local recurrence in about 30–60 % of cases has been reported for inverted papilloma despite adequate surgical treatment [20].

We are therefore reporting a paediatric patient who presented with a synchronous nasal rhinosporidiosis and inverted papilloma and was managed by transnasal endoscopic surgical excision of the nasal mass and kept on oral dapsone for 6 months postoperatively. The work has been reported in line with the SCARE criteria [21].

2. Case presentation

We are presenting a seven (7) year old male boy who presented at our outpatient otorhinolaryngology clinic while escorted by his mother and came by using public transport. The boy had a 1-year history of left-sided nasal obstruction and intermittent epistaxis for 6 months. He had no history of cheek swelling, pain or numbness, loss or loosening of teeth or alveolar ridge fullness. There were no ophthalmological, otological or neurological complaints reported by the patient. On the other hand, he was attended in other peripheral health facilities and prescribed antibiotics, nasal decongestants, antihistamines and antileukotrienes without relief.

On physical examination, he had no external nose deformity but rather a friable isolated left-sided obstructive nasal mass was found following diagnostic nasal endoscopy. Upon nasal endoscopy, it was found to be an isolated left nasal mass. Due to poor financial status of the patient, no computerized tomography scan was ordered and this was mainly supported by localization of the mass in the nasal cavity thus no surgical complexity was expected intraoperatively. Further exploration of the nasopharynx by nasopharyngoscopy was found to be free from the mass.

He was not pale and had no any palpable peripheral lymph nodes. Laboratory results showed hemoglobin 11 g/dl and elevated erythrocyte sedimentation rate (35 mm/h). A provisional diagnosis of pyogenic granuloma was made and consequently the patient was planned for surgery. Intraoperatively the patient was kept in neutral position with both nostrils being fully exposed and nasal endoscopy was done and through transnasal endoscopic approach surgical excision of the nasal mass was done under general anaesthesia. The surgically excised specimen in piece meals was sent for histopathology and thus biopsies were multiple in numbers.

Histopathological analysis revealed thick-walled sporangium containing numerous endospores (daughter spores) (Fig. 1) and with further sections showing thick walled sporangium with endospores in different stages of development accompanied by mixed inflammatory cells mainly plasma cells (Fig. 2). Another cross-section showed a papilla with delicate fibrovascular core admixed with thick walled sporangium, lined by stratified squamous epithelium with minimal surface keratinization (Fig. 3). On the other hand, low power micrographs showed papillary arrangement with delicate fibrovascular core admixed with thick-walled sporangium and the papillae are lined by stratified squamous epithelium with no surface keratinization (Fig. 4). More than one qualified anatomical pathologist reviewed histopathology results and then shared with more than one otorhinolaryngologist at the zonal hospital due to rarity of synchronous nasal rhinosporidiosis and inverted papilloma.

Fig. 1.

Intermediate power view of thick-walled sporangium containing numerous endospores (daughter spores).

Fig. 2.

A high-power view of large, thick walled sporangium with endospores in different stages of development accompanied by mixed inflammatory cells mainly plasma cells and lymphocytes.

Fig. 3.

A cross-section showing a papilla with delicate fibrovascular core admixed with thick-walled sporangium, lined by stratified squamous epithelium with minimal surface keratinization.

Fig. 4.

Low power micrographs showing papillary arrangement with delicate fibrovascular core admixed with thick-walled sporangium and the papillae are lined by stratified squamous epithelium with no surface keratinization.

The patient was then kept on oral dapsone at a dose of 50 mg/day for 6-months and with no residual disease recurrence noted after 6-months of follow up. The patient was attended on the 7th-day and 14th day and after 6 months post transnasal endoscopic nasal mass excision and the visits were uneventful. The work has been reported in line with the SCARE criteria [21].

3. Discussion

This case report from central Tanzania at the largest zonal referral hospital has documented a case of synchronous nasal rhinosporidiosis and inverted papilloma in a paediatric patient and so far the first documented case of synchronous nasal rhinosporidiosis and inverted papilloma both in Central Tanzania and countrywide.

Rhinosporidiosis is known to be predominantly sporadic and on the other hand it has been reported in about 70 countries [12]. Migration has attributed to the infrequently isolated cases in other parts of the world [37,38].

Nasal rhinosporidiosis is more common in younger age groups and with male predominance where male to female ratio has been 4:1 [1,[9], [10], [11]]. Such male predominance has been observed in our case report since the affected patient was a 7-year old boy.

Nasal rhinosporidiosis and its causative organism, Rhinosporidium seeberi have been known for over ten decades and it's a rare infective chronic granulomatous disease of the nose [1,3]. Attempts to isolate the causative organism in vitro to date has never been successful and its taxonomic rank remains unclear [39].

Rhinosporidium seeberi has been related to a group of fish parasites referred to as the DRIP clade and most pathologists and microbiologists initially considered it to be fungus based on its characteristic features upon being stained by fungal stains such as Gomori methenamine silver (GMS) and periodic acid-Schiff (PAS) [1,17].

Available literatures have proposed the class of Rhinosporidium seeberi to be Mesomycetozoa [14,40]. Being supported by fluorescent in-situ-hybridization techniques, the natural habitat for Rhinosporidium seeberi has been reported to be water reservoirs and soil contaminated by wastes [40]. On the other hand, other aquatic microorganisms play a synergistic role in the establishment of natural habitat for rhinosporidiosis [40].

The class Mesomycetozoa has two orders, which are the Dermocystida and Ichthyophonida. In the order Dermocystida is the family Rhinosporideaceae that includes Rhinosporidium seeberi, Dermocystidium spp. and the rosette agent [1,40].

Pertaining the route of transmission for Rhinosporidium seeberi, it is still unclear to date. Despite unclear route of its transmission there is a presumed mode of infection from the natural aquatic habitat of Rhinosporidium seeberi through a traumatized epithelium commonly called trans epithelial infection and this is most common in the nasal cavity [1,10]. On the other hand the various modes of spread of Rhinosporidium seeberi includes; auto-inoculation through spillage of endospores from polyps after trauma or surgery, haematogenous spread to distant sites, lymphatic spread and sexual transmission [10,40].

Rhinosporidiosis is more prevalent in rural settings particularly among people working or in contact with contaminated soil, stagnant water (ponds, or lakes) or sand [40]. The patient we are hereby reporting resides in a rural area and with a history of being in contact with contaminated pond water. Moreover, the patient reported a history of contact with feces of infected livestock. Reviewed literatures have documented similar risk factors [17,40].

The possibility of nonspecific immune reactivity in the host, blood group and HLA types has been suggested as important in the pathogenesis of Rhinosporidium seeberi and also in the establishment of an initial focus of infection [1,17].

Rhinosporidiosis manifests as tumor-like masses, usually of the nasal mucosa or conjunctivae of humans and animals. Patients with rhinological involvement manifests with nasal obstruction or bleeding due to polyp formation and it can spread to the nasopharynx, oropharynx, and the maxillary antrum [4,10]. The patient we are hereby reporting had an isolated friable mass localized in the nasal cavity.

The diagnosis of Rhinosporidiosis is established by observing the characteristic appearance of the organism in tissue biopsies and computerized tomography (CT) scans. The lesion appears friable, vascular, pedunculated or sessile polyp with a surface studded with tiny white dots due to spores beneath the epithelium, giving a ‘strawberry-like’ appearance [1]. The lesion in our case report was similarly friable.

Despite its rarity in terms of multisystem involvement by rhinosporidiosis, it may include multiple mucocutaneous, hepatic, renal, pulmonary, splenic or bone lesions associated with fever, wasting and even death [1,16,17].

Spontaneous regression of nasal rhinosporidiosis has been reported in rare occasion in animals and humans but generally, medical and/or surgical intervention is/are necessary as the available treatment options [16,17].

The treatment of choice for nasal rhinosporidiosis is surgical excision as it reduces recurrence rate [1,12]. Surgical removal of the lesion with cauterization of the attachment base is almost curative in at least 90 % of the cases [12,41]. Surgical excision of rhinosporidial growths may be associated with remarkable morbidity due to hemorrhage and septal perforation and therefore limited surgical excision and adjuvant medical therapies that are endospore-static rather than endosporicidal are recommended and they include antifungals such as griseofluvin and amphotericin B, trimethoprim-sulphadiazine, and sodium stibogluconate [1,17].

Dapsone is the available promising drug in treatment of nasal rhinosporidiosis since it arrests the maturation of sporangia and promotes fibrosis in the stroma when used as an adjunct to surgery [1,40]. Pre-surgical dapsone would minimize both hemorrhage by promotion of fibrosis as well as preventing the colonization and infection of new sites after the release of endospores from the surgically traumatized nasal masses [42,43]. Our patient was kept on dapsone for 6-months after endoscopic nasal mass excision with no recurrence noted after 6-months of follow up. On the other hand, laser treatment is becoming a promising mode of managing rhinosporidial growths in the near future [44].

Inverted papilloma describes the histological tendency of an epithelium to invert into the stroma. It has a characteristic intact basement membrane [20]. Similar to the recurrence tendency being exhibited by nasal rhinosporidiosis, inverted papilloma has also recurrence tendency coupled with local aggressiveness [45] and association with sinonasal polyposis [25]. Inverted papilloma has a tendency of malignant transformation where about 9 % of inverted papillomas transform to malignant tumors and hereby the most frequent malignant tumor derived from inverted papilloma is squamous cell carcinoma [46,47]. Although generally indolent, inverted papilloma has high recurrence rate (14–78 %) [24]. The prognosis of squamous cell carcinoma (SCC) in inverted papillomas is poor with 5- and 10-year survival rate being 39.6 % and 31.8 % respectively. The poor prognostic markers of SCC occurring following malignant transformation of inverted papillomas include elderly age, infiltration of the skull base or orbital involvement and moderate to poor differentiation histological pattern [47,48].

Human papillomavirus type 11 has been implicated in the pathogenesis of inverted papillomas though predominance of HPV type 6 and 11 has been reported in inverted papillomas compared to types 16 and 18. Low-risk or high-risk co-infections are rare [31,32]. Patients with inverted papilloma just like nasal rhinosporidiosis presents with nasal obstruction, nasal bleeding, nasal discharge and recurrent sinusitis. Computerized tomography in patients with inverted papilloma depicts chronic osteitis and hyperostosis preoperatively [49]. Other differential diagnoses for inverted papillomas to be considered by clinicians or pathologists include nasal haemangioma, angiofibroma, rhinolith, hereditary hemorrhagic telangiectasia, vestibular papilloma, fibrous histiocytoma and nasal glioma [50,51]. These were ruled out following histopathological analysis of the surgically excised specimen. The uniqueness of our case compared to other published studies is due to younger age at which our patient suffered from synchronous inverted papilloma and rhinosporidiosis since it was expected to be more common in older patients like the case reported in the United Kingdom was of a 78-year old woman. On the other hand, the nasal mass in our case report was found to be a localized mass in the nasal cavity while that from the United Kingdom was a large polyp originating from the right sphenoid sinus [20].

The main stay of treatment of inverted papilloma just like nasal rhinosporidiosis remains to be surgical excision of the nasal mass followed by postoperative follow due to risk of recurrence [36].

4. Conclusion

In Tanzania, rhinosporidiosis is non-endemic and in the central zone, the disease is uncommon thus may pose diagnostic challenges. Sinonasal inverted papillomas are also rare in our settings. Presence of synchronous rhinosporidiosis and inverted papilloma supports the inflammatory theory for pathogenesis of inverted papilloma. It is therefore important for both clinicians and pathologists to have a high index of suspicion when managing patients with nasal masses even at younger age from non-endemic areas to avoid missing such diagnosis since nasal rhinosporidiosis and inverted papilloma lesions may resemble the routinely encountered nasal polyps.

Provenance and peer review

Not commissioned, externally-peer reviewed.

Ethical approval

Ethics clearance was not necessary since the University waives ethics approval for publication of case reports involving no patients' images.

Parental consent for minors

Written informed consent was obtained from the patient's parents/legal guardian for publication and any accompanying images. A copy of the written consent is available for review by the Editor-in-Chief of this journal on request.

Funding

None.

CRediT authorship contribution statement

ZSA-Conceptualization and writing original draft of the manuscript.

FZ- Conceptualization and writing original draft of the manuscript.

BJM- Conceptualization and reviewing the prepared original draft of the manuscript.

CDM- Conceptualization and reviewing the prepared original draft of the manuscript.

AAK- Conceptualization and reviewing the prepared original draft of the manuscript.

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Guarantor

Dr. Zephania Saitabau Abraham takes full responsibility of the work.

Declaration of competing interest

The authors report no conflict of interest.