Oral pulse or hyaline ring granuloma: A case report and a brief review

Abstract

Pulse or hyaline ring granulomas are rare but are well-defined oral and extraoral lesions due to implantation of the cellulose moiety of plant foods in contrast starch components. A unique form as reactive gingival growth showing histologic features of oral pulse or hyaline ring granuloma (OPHRG) which had resulted from implantation of food particles of plant or vegetable origin into the periodontium has been illustrated. Such a presentation is attributable to compromised periodontal health and poor oral hygiene favoring the implantation of food particles has been described here along with a literature update on OPHRG.

INTRODUCTION

The term pulse granuloma (PG) (pulse is defined as edible seeds of leguminous crops, such as peas, beans, and lentils), has been applied to the foreign body reaction to vegetable material.[1] It is a distinct oral entity characterized as a foreign body reaction occurring either centrally or peripherally.[2] It is usually seen in the periapical or the sulcus area. Occasionally, the lesions occur in the wall of the cyst, most common being inflammatory odontogenic cyst.[3] However, a similar condition described as PG is usually observed in lungs and alimentary tract, usually in infants and severely debilitated persons.[2,4]

The term PG illustrates a granulomatous response. The term oral pulse granuloma (OPG) is used for the lesions occurring in the oral cavity. Histologically, they appear as eosinophilic hyaline mass with giant cell inclusions and inflammatory cells.[3] The granulomas may assume different histologic characteristics, possibly related to the length of time in the tissue (evolution) and location. Adequate recognition is important to avoid misdiagnosis.[3] Several terminologies are used in the literature to describe this entity such as chronic mandibular periostitis, giant cell hyaline angiopathy (GCHA), hyaline bodies and giant cells associated with a radicular cyst, PG, oral vegetable granuloma (OVG), hyaline ring granuloma (HRG), food-induced granuloma, and oral pulse or hyaline ring granuloma (OPHRG).[5]

CASE REPORT

A 59-year-old female patient reported with a growth in the upper left back teeth region from 25 to 28, since 3 months. It was small in size initially and increased to present size with a dull aching pain. Extraoral examination revealed a diffuse swelling present on the left side of the face extending superiorly from the inferior border of the orbit till the line joining the tragus to left corner of the mouth. Swelling was approximately 5 cm × 5 cm, roughly round in shape. The skin over the swelling was stretched, and facial asymmetry noted [Figure 1]. On palpation swelling was nontender, firm in consistency; skin over the swelling was pinchable. The swelling was fixed to the underlying structure and immobile. There was no local rise in temperature or discharge. On intraoral examination, dental findings include the several teeth missing, root stumps w.r.t 28, 37, 46, decayed 11, 21, 22, 34, gingival recession in relation to anterior teeth, pockets in relation to posterior teeth, tooth mobility w.r.t 11, 26, 27, 31, 41, 47, with presence of spacing, stains, and calculus. On intraoral lesional finding consists of an oval, nodular, lobulated, smooth contoured pedunculated growth on the upper left gingiva, and extending and obliterating the buccal vestibule. Growth was measuring approximately 3 cm × 4 cm and was extending from 24 to 28 teeth region anteroposteriorly, superiorly from the buccal vestibule till the line of occlusion [Figure 2]. Surface appeared smooth and pale pink in color. The swelling was nontender, firm in consistency, smooth and lobulated. The presence of true pockets w.r.t 24–27 in relation to the growth was noted. No discharge and bleeding from the growth. Provisionally, the case was diagnosed as benign or reactive growth on the gingiva of the left maxilla. Differential diagnoses considered were gingival fibroma, pyogenic granuloma, peripheral ossifying fibroma, peripheral giant cell granuloma, and peripheral odontogenic tumors. Orthopantomograph revealed a periapical radiolucency w.r.t 21, 22, 23 with a sclerotic rim indicating periapical pathology and a radiolucency w.r.t 26 region [Figure 3]. Intraoral periapical radiograph revealed radiolucency interdentally between 25 and 26 and in the periapical region of 26 [Figure 4]. Excision of proliferative growth, extraction of 25, 26, 27, 28 (root stumps) along with curettage of periapical region w.r.t 26 was done under general anesthesia with reconstruction with buccal pad fat and buccal flap advancement [Figure 5]. Figure 6 shows the gross specimen and cut surface of the proliferative growth.

Figure 1.

Extraoral examination shows a diffuse swelling on the left side of the face

Figure 2.

Intraoral examination reveals a pedunculated growth on the upper left gingiva, obliterating the buccal vestibule

Figure 3.

Oral pulse granuloma reveals a periapical radiolucency w.r.t 21, 22, 23 with a sclerotic rim indicating periapical pathology and a radiolucency w.r.t 26 region

Figure 4.

Intraoral periapical radiograph reveals radiolucency interdentally w.r.t 25, 26 and in the periapical region of 26

Figure 5.

Intraoperative photograph shows surgical excision of the growth along with extraction of teeth

Figure 6.

The gross specimen and cut surface of the proliferative growth

Microscopic examination revealed discontinuous stratified squamous parakertinized atrophic epithelium with areas of ulceration covered with fibrinopurulent membrane. Beneath, the ulceration stroma was edematous and showed numerous capillaries, dense collection of acute and chronic inflammatory cells, and dispersed multinucleated giant cells. Deep connective tissue stroma showed multiple granuloma formation [Figure 7]. Eosinophilic hyaline material with hyaline ring (HR) surrounded by lymphocytes, macrophages, and giant cells were evident inducing a foreign body granulomatous response. Hyaline material in some area showed retractile basophilic material [Figure 8]. Multinucleated giant cells of varying sizes were noted. Both foreign body type and Langhan's type giant cells were seen. Few giant cells showed engulfed retractile foreign matter [Figure 9]. Homogenous brownish structures (inclusion of vegetable matter) associated with giant cell reaction in focal sites along with multiple HRGs were noted [Figure 10]. Deep computed tomography stroma showed interlacing fascicles of fibroblasts and collagen fibers with diffuse inflammatory infiltrate. Histochemical staining with periodic Schiff stain demonstrated vegetable matter stained as pale eosinophilic, double-layered refractile membranes with granulomatous reaction encasing them along with HRG [Figures 11 and 12].

Figure 7.

Photomicrograph shows areas of ulceration covered with fibrinopurulent membrane. Stroma is edematous with a dense collection of acute and chronic inflammatory cells. Deep connective tissue stroma shows multiple granulomas (H and E, ×4)

Figure 8.

Photomicrograph shows eosinophilic hyaline material with hyaline ring surrounded by macrophages and giant cells (arrow). Hyaline material in some area shows retractile basophilic material (*) (H and E, ×10)

Figure 9.

Photomicrographs show multinucleated giant cells of varying sizes. Both foreign body type and Langhan's type giant cells were seen. Few giant cells show engulfed retractile foreign matter (H and E, ×10)

Figure 10.

Photomicrographs reveal multiple periodic Schiff stain (PAS) positive hyaline ring granulomas and homogenous brownish structures associated with giant cell reaction (PAS, ×10) Inset shows refractile vegetable material with giant cell response (arrow)

Figure 11.

Photomicrograph shows vegetable matter stained pale eosinophilic, double layered retractile membranes with a granulomatous reaction encasing them (periodic Schiff stain, ×40)

Based on clinical and histopathological features, the present case was concluded as OPHRG in a reactive gingival growth, secondary to implantation of food particles of plant origin, through the periodontal pockets due to severe interdental bone loss.

DISCUSSION

Oral pulse granuloma is an uncommonly reported oral finding having controversial etiopathogenesis. Many authors consider a vegetable origin; although others deny this possibility.[3] The histopathological features of OPG described in the literature are alike, irrespective of the clinical presentations. Constant features are the presence of structureless HRs or amorphous hyaline masses lying within a fibrous connective tissue stroma. The hyaline material can appear as homogenous, eosinophilic material may be spherical, ovoid, irregular bodies surrounded by fibroblasts, inflammatory cells, and giant cells as illustrated in Figures 8–10.[6] Occasionally, there may be the presence of small calcified basophilic bodies within the amorphous hyaline material as noted in Figure 8.[3,6] OPG is a histopathological diagnosis for localized lesion resulting from the implantation of food particles of plant origin. It often occurs in the posterior regions of edentulous mandible in association with a full denture but it may also be found in periapical areas of grossly decayed teeth or retained roots and teeth with a history of endodontic therapy, associated with impacted lower third molar teeth with history of pericoronitis, in postextraction tissue reaction or as part of a cyst wall where there has been a communication with oral cavity or as a complication of periodontal surgery or associated with deep periodontal pockets due to compromised periodontal health as in this case.[3,4,6]

Dunlap and Barker were among the first authors to evaluate this entity and considered it to be an acute vasculitis, naming it “GCHA.”[5] Some investigators consider HRs as degenerated collagen fibers or fibrosed extravasated proteins of unknown origin.[7] Chou et al. proposed the descriptive term “HRG,” which seems more suitable and also avoids misunderstanding.[4] Two theories for etiopathogenesis have been proposed: (i) The origin of the HRs is due to a foreign material (pulse and legumes) having penetrated the oral mucosa or gastrointestinal tract and lungs (exogenous theory) and (ii) the rings are due to hyaline degenerative changes in walls of blood vessels (endogenous theory).[5]

Adkins considered the lesion to be a foreign body granuloma, with hyaline material being the foreign body. Philipsen and Reichart have mentioned in their review that the foreign body reaction is due to legume cells, which contain starch, and also that legume parenchymatous cells in various stages of breakdown are as a result of the disruption by cooking and attempted degradation by host phagocytic cells, which produced the ring-like structures seen in the oral lesions.[5] Gueiros et al., have reported the classification of the HRs as inclusion of cooked vegetable particles, calling it “PGs.” Other terms such as “OVG” and “legume associated lesion,” also addressed its vegetable origin.[2]

The pathogenesis of OPG has also been evaluated by inducing its formation in animal models.[8,9] Talacko and Radden hypothesized that once the food gains access to tissues; it is rapidly digested and altered by the host responses. The cellulose moiety of plant foods is indigestible and persists in the form of hyaline material, inciting a chronic granulomatous response.[8] Harrison and Martin supported the theory of a vegetable nature of the HRs on the basis of ultrastructural investigation. Thus, the term “OVG” was proposed.[4] Based on histochemical and immunochemical analyses, Gueiros et al., concluded that oral lesions are caused by traumatic implantation of vegetable particles in an extraction socket or oral ulcer with cellulose being responsible for granuloma formation. Once a granulomatous response has occurred, chronic exposure to inflammatory enzymes probably modifies the morphological aspects of the HRs without compromising its anti-genic potential.[2] The HRs were identified as structures originating from fragments of pulses, and the above lesion is thereafter termed OPHRG.[5] Investigators have stated that histologically implanted lentils, peas, and navy beans showed the characteristic features of PGs encountered in human beings. The remaining vegetable substances failed to show the large, compartmentalized ovoid structures seen with pulses as depicted in the Figures 11 and 12.[5,9]

Figure 12.

Photomicrograph reveals periodic Schiff stain-positive hyaline ring and vegetable matter stained pale eosinophilic, double layered retractile membranes with a granulomatous reaction (PAS, ×40)

Table 1 summarizes 35 publications where the data related to the source of origin, location and diagnosis of 208 cases with OPHRGs has been tabulated and reviewed.[1,2,3,4,5,6,10,11,12,13,14,15,16] Including a total of 173 patients OPHRGs that were reviewed by Philipsen and Reichart, those reported from 1971 to 2008.[5] 28 reports favor an exogenous origin, where food particles of plant or vegetable have been considered as source origin in 26 reports. In five publications, the source of origin is unclear/and unknown. Endogenous origin has been favored by three reports, and those authors have concluded their cases as GCHA. Regarding the location of the lesion, the mandibular edentulous ridge has been the frequently encountered site followed by wall of cyst approximately in 90 cases. Among cysts, most frequently OPHRG are demonstrated in inflammatory odontogenic cyst either residual cyst or periapical cyst. Periapical area, extraction socket, and pericoronitis associated with the impacted tooth were the other sites to be reported. Reports that support exogenous origin have concluded the diagnosis as either chronic periostitis or HRG or OPG or OPHRG.

Table 1.

Brief review of OPHRG reported in the literature (1971-2014) related to the origin, location, and diagnosis

The present case is unique because such a clinical form has not been cited in the literature. In a review by Chou et al., of 64 cases, 53 had a history of tooth extraction. Of the remaining 11 patients, seven had a history of a deep periodontal pocket, trauma, or surgery. Three lesions were found in the wall of odontogenic cysts and one below the root of a resorbed primary tooth.[4]

Most reports that include histopathologic descriptions of OPHRG comment upon HRs as the main histomorphologic findings. However, other vegetable parts like the pericarp which is pigmented and may mimic the cuticle or mouth apparatus of the maggot are hardly ever mentioned. Oral myiasis has occasionally been reported in the literature, involving the lip, the palate, the floor of the mouth, or the periodontal areas.[16] The presence of round cells (albumin cells) with distinct cell walls, pigmented cover structure (pericarp) which are birefringent [Figure 10] and HRs are indicative of OPHRG; present case shows all these features thus excluding oral myiasis.[16]

Treatment for OPHRG is complete surgical excision of the lesion. The recurrence of OPHRG is rare and if recurs it is probably due to incomplete excision.[4] Maintenance of oral hygiene is very important to avoid embedding of vegetable matter into the extraction socket during the healing phase, or through grossly decayed teeth and into deep periodontal pockets.

CONCLUSION

Oral pulse or hyaline ring granuloma are rare but is a well-described entity with distinct histopathology. OPHRG has distinct histopathological aspects from PG of the lungs and gut as starch cells are often absent, and giant cells may be scant. This case report was presented to emphasize the occurrence of OPHRG in reactive gingival growth, which is mainly due to implantation of food particles into the periodontium due to compromised periodontal health and poor oral hygiene. The cellulose moiety of plant foods is in contrast to the starch component indigestible and persists in the human tissues in the form of hyaline material, inciting a chronic granulomatous response.