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Table of Contents
REVIEW ARTICLE
Year : 2022  |  Volume : 4  |  Issue : 1  |  Page : 40

Parinaud's oculoglandular syndrome by sporotrichosis: Red flag


1 Department of Ophthalmology, Federal University of Rio de Janeiro, Rio de Janeiro; Federal University of Goiás Reference Center of Ophthalmology – CEROF, Goiania, Brazil
2 Department of Ophthalmology, Federal University of Rio de Janeiro, Rio de Janeiro, Brazil
3 Federal University of Goiás Reference Center of Ophthalmology – CEROF, Goiania, Brazil

Date of Submission28-Jan-2022
Date of Decision19-Apr-2022
Date of Acceptance08-Jun-2022
Date of Web Publication24-Aug-2022

Correspondence Address:
Romulo Piloni-Parreira
Primeira Avenida, 355-447 – setor Leste Universitario, Goiania – GO, 74605020
Brazil
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/pajo.pajo_8_22

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  Abstract 


Parinaud's Oculoglandular Syndrome (POGS) is a rare and atypical form of granulomatous conjunctivitis, classically composed of a triad: fever, unilateral granulomatous follicular conjunctivitis and preauricular satellite lymphadenopathy or ipsilateral submandibular, commonly related to cat scratch disease caused mainly by Bartonella henselae, or also caused, even if not tipically, by Sporothrix schenckii. In endemic areas, such as in South America, especially Brazil and Peru, ocular sporotrichosis, associated with POGS, should be considered a diagnostic hypothesis of ophthalmic diseases especially if this patient has a history of contact with cats . Itraconazole must be the first choice of medication for treatment and this patient would need assistance until complete clinical improvement, with family members oriented about possible sources of contamination, being important the early and appropriate treatment, due to the risk of eye sequelae . As a neglected public health problem in Brazil, where there has been a large increase in cases in the last decades, an accurate understanding of this disease is essential, with focus in the southeast region, mostly in the state of Rio de Janeiro.

Keywords: Parinaud's syndrome, Sporothrix schenckii infections, sporotrichosis


How to cite this article:
Piloni-Parreira R, Pinheiro BM, Cartagenes Santos AC, Neves LL, de Melo Junior IR, Mendonca Silva JR. Parinaud's oculoglandular syndrome by sporotrichosis: Red flag. Pan Am J Ophthalmol 2022;4:40

How to cite this URL:
Piloni-Parreira R, Pinheiro BM, Cartagenes Santos AC, Neves LL, de Melo Junior IR, Mendonca Silva JR. Parinaud's oculoglandular syndrome by sporotrichosis: Red flag. Pan Am J Ophthalmol [serial online] 2022 [cited 2022 Oct 4];4:40. Available from: https://www.thepajo.org/text.asp?2022/4/1/40/354533




  Introduction Top


Parinaud's oculoglandular syndrome (POGS), described by Henri Parinaud, in 1889, is a rare and atypical form of granulomatous conjunctivitis (GC). Described primarily as related to cat scratch disease (CSD), it is classically presented as a unilateral granulomatous follicular conjunctivitis and preauricular satellite lymphadenopathy (LP) or ipsilateral submandibular.[1],[2],[3],[4]

The GC has a variety of differential diagnoses, including isolated and systemic ocular causes. Currently, numerous vectors are known, other than that classically described by Parinaud, and the CSD is the classic and most commonly associated form.[3] It is common to present a great challenge to ophthalmologists, due to the a wide variety of etiologies, which may include inflammatory, allergic, neoplastic, and infectious pathologies. It is useful, therefore, to differentiate granuloma alone, or even initial, from rarer diseases such as granulomatous with polyangiitis, lymphoma, or sarcoidosis and infectious diseases. Another useful factor for correct etiological diagnosis is the systemic involvement. The presence of signs such as fever, pulmonary nodules, adenopathies, and tumors suggest systemic disease, and when they present the classic triad, they are even more suggestive of POGS.[5]

Descriptions of POGS related to Sporothrix spp. are rare in the literature, with the majority of cases related to epidemics in Brazil, especially in Rio de Janeiro (RJ), showing that the atypical presentation of sporotrichosis may be related to zoonosis. As observed in [Table 1], in the first column the case reports and in the second the epidemiological bulletins, both providing a better understanding of the disease.
Table 1: Case reports and epidemiological bulletins cited in this review

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  Literature Review Top


We reviewed published studies with the theme on the websites PubMed and SciELO, using the terms in English and Portuguese: Parinaud's Oculoglandular Syndrome or Síndrome Oculoglandular de Parinaud or Ocular Sporotrichosis or Esporotricose Ocular.

Considering the scarce literature, we also selected clinical cases and epidemiological bulletins for this review. The titles and references of these articles are specified in the [Table 1].

Infectious etiologies

There are several infectious etiologies of POGS, classically related to CSD, caused mainly by Bartonella henselae and less commonly by Francisella tularensis and Sporothrix schenckii or Sporothrix ssp., as listed in the [Table 2].
Table 2: Presentation of the main infectious etiologies and their respective causative agents of Parinaud's oculoglandular syndrome, subdivided into prevalence: More common, common, less common and rare

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Definition of the syndrome

Sporotrichosis is a cosmopolitan mycotic infection and subacute or chronic granulomatous; it could be acquired by traumatic inoculation.[6] Described by Benjamin Schenck in 1898,[7] it is typically characterized by nodular lesions. It is caused by the Sporothrix schenckii complex, a thermodimorphic fungus existing in the mycelial and yeast phase.[8] This is subcutaneous mycosis of tropical and subtropical regions, being more common in South America (SA), where it is endemic,[9] mainly in Brazil and Peru.[10] The predominant subtype in these regions is the brasiliensis.[11] Easily found in the organic matter of plants, soil, and water[12] and also in skins, feces and oral cavities of some animals (cats, horses, dogs, rabbits, and rats).[13]

World distribution

Although it is a disease reported more than a century ago, further studies are still needed. The form of distribution is not well understood in the literature.[14],[15] As a worldwide disseminated mycosis, it is endemic in certain regions such as Japan, North America and SA, especially Mexico, Brazil, Uruguay, Peru and Colombia and also can be frequently found among Far East and Europe, especially in France.[16],[17]

Geographical distribution in Brazil

The cosmopolitan aspect of sporotrichosis is related to human involvement in all age groups, without predilection for sex or race, therefore, without predisposing individual factors.[18] However, most reports in SA come from Brazil.[19]



Differences in distribution are mainly due to professional occupation, particularly to individuals who deal with soil, but may also be related to scratching or biting animals, such as felines.[16],[17],[18],[19],[20],[21] Despite presenting a global distribution, it is a sporadic disease, with cases in several countries,[22],[23],[24] except in Brazil, where there has been an alarming increase in recent decades,[25] particularly in RJ. Although cases of sporotrichosis have been published in Amazonas, Pará, Minas Gerais, Espírito Santo, São Paulo, Paraná, and Rio Grande do Sul, the large majority are concentrated in the Southeast and south regions, with a substantial increase in the number of cases in recent years.[8],[17] By correlating the number of hospitalizations due to sporotrichosis, important data are obtainable about the distribution of the disease in the Brazilian territory. Although certain regions such as Goiás do not present reports of outbreaks in the literature or in the databases of health surveillance information, the high number of hospitalizations in the period stands out, especially in the municipality of Anápolis.[20],[26] Between 1986 and 2017, 4788 cases of human sporotrichosis were recorded at the Evandro Chagas National Institute of Infectious Diseases of the Oswaldo Cruz Foundation in RJ.[27]

It is, therefore, an emerging and neglected disease. In Brazil, It is a major public health problem, resulting from the absence of a national control program or control actions.[28],[29]

The specific case of the state of Rio de Janeiro

There is an inadequate understanding of why sporotrichosis has become a zoonosis of emerging proportions in RJ.[30] It is necessary, therefore, to understand the space where it manifests itself and its particularities. It is assumed that sporotrichosis is strongly related to socio-environmental and behavioral conditions specific to certain locations, which contributes and determines the variation of the transmission of the fungus. The disease's spread is related to the dynamics of occupation. Less commonly in case of Brazil, is related to soil use, as well as to the life style and work activities of certain social groups. Infected or sick animals at home environment are associated with areas with poor socioeconomic conditions. Given this scenario, due to the high incidence of feline sporotrichosis, RJ is currently considered hyperendemic to the disease[31] and the number of cases diagnosed in humans and felines represents only the “tip of the iceberg” of the pathology,[28] therefore, it is necessary to develop new epidemiological and environmental studies to understand the current situation. For public health purposes, measures involving health and care for these animals, as public awareness and general public health measures should be promoted, contributing to the control of the disease.

From 2015 to 2019, 1097 suspected cases of sporotrichosis were reported in RJ, with confirmation percentages above 60%, compared to the Metropolitan Region, especially the Capital and Nova Iguaçu. This reflects greater circulation of the disease in these areas or greater sensitivity of surveillances. Other important aspect is related to the fact that there are multiple areas of low socioeconomic status, with poor health and health systems, associated with high demographic density.[32],[33],[34]

Forms of contamination

For a long time, sporotrichosis was known as “rose bush mycosis” or “gardener's mycosis,” because the infection usually resulted from inoculation of the agent on the skin or mucous, due to the trauma with contaminated plants' material. In the early twentieth century, sporotrichosis was already common in France, however, with few cases of zoonotic transmission. Sporotrichosis can occasionally be transmitted through traumatic inoculation of the skin with organic matter, associated with soil manipulation activities. Occupations or activities that have been associated with infection include the handling of plants or soil and contact with sick or healthy animals, in addition to direct contact with infected animal fluids[35] or respiratory secretions.[10] Liborio Neto et al. described a case of transmission through contaminated blood of a cat.[36] Outbreaks of infection related to forestry and gardening in the Mississippi Valley were reported in the United States in the 1980s and also as microepidemics such as the one that occurred in the early 1990s, with people infected by contact with hay stored in an abandoned house. In addition to major epidemics, such as the occurred in the 1940s, when 3000 prospectors were contaminated in South Africa. and reported cases of zoonotic transmission.[8],[13],[37] Contaminated cats with sporotrichosis may present facial lesions, especially nose, which can be spread by licking. Healthy individuals may contract sporotrichosis from infected cats, even if they cat don't scratch or bite them. There are reports only of contact followed by the act of scratching the eyes. The best way is still to prevent, trough control of the zoonotic sporotrichosis, treating and isolating infected animals[11], in addition maintaining cautious contact with foreign cats by limiting the contact of domestic cats with wild or street cats.[38]

The fungus

Sporothrix species are dimorphic fungi, which present in two different phases, saprophytic phase of mycelium at room temperature (25°C–28°C) and pathogenic phase similar to yeast, at 36°C -37°C.[24] More recently, through genetic and molecular tools, it was possible to modify some classic points of view, especially those related to the description of species with pathogenic potential.[33] Historically, after the first clinical case report of cutaneous sporotrichosis has been published,[7] many others have appeared in humans and animals, especially in the last decades of the twentieth century.[33] As recently described species, S. brasiliensis and S. globosa, which have a higher incidence in SA and East Asia, respectively.[24],[39] The fungus usually enters the host through small skin trauma, through plants contaminated with debris, or through scratches or animal bites. It is important to point out that the classic species S. schenckii is more related to benign chronic subcutaneous mycosis, with moderate virulence profile, while S. brasiliensis is highly virulent and is associated with severe clinical forms of sporotrichosis.[40] Unlike the other ones, S. brasiliensis has been presenting itself since the 1990s, with a greater preponderance of transmission through the cat.

Signs and symptoms classic for sporotrichosis

The clinical presentation of sporotrichosis is polymorphic and the ocular form has rarely been described in immunocompetent patients or without previous ocular trauma. Most of them seek medical attention due to the complaint of palpable LP, present in 54% of the cases, which is the most frequent clinical presentation.[10],[27] Sporotrichosis is a implantation or inoculation mycosis that can be caused by numerous species of Sporothrix and may also occasionally result in rarer intraocular infections, including endophthalmitis, retinal granuloma, necrotizing granulomatous retinochoroiditis, and granulomatous uveitis.[35] It can present basically in two distinct ways, the intraocular form, by hematogenous dissemination, usually associated with immunocompromised patients or as external eye disease, basically affecting ocular appendage, by (self) inoculation, such as conjunctivitis, sclerite, episcleritis, corneal ulcer, dacryocystitis, and/or eyelid granulomas. It is a rare pathology in ocular appendages; however, when present, it manifests itself typically in eyelids and eyebrows and also as GC, typical of POGS, with conjunctival edema, hyperemia, purulent ocular secretion, yellowish nodules grouped with smooth and bright surface, accompanied by satellite LP.[27]

Forms of diagnosis

There are numerous forms of mycological examination for the diagnosis of sporotrichosis, among them: direct mycological examination using potassium hydroxide, low sensivity and Gram, Giemsa, Periodic-Schiff (PAS), in addition to Grocott-Gomori staining (silver staining), successfully used in disseminated manifestations. However, the gold standard for the diagnosis of Sporothrix is the conventional culture of clinical specimens obtained, whether from active lesion, pus, secretion, or biopsy. The samples are grown in Sabouraud Agar and later antifungal susceptibility tests and additional phenotypic characterization can be performed. Typically, cultures will become postive in the first 2 weeks after incubation, however, in some cases, it is necessary to observe them for up to 30 days before considering them negative. Crops maintained at 25° C develop fine hyphae arranged in flower form and can be shared by various environmental species of Sporothrix. The demonstration of dimorphism is important to confirm the agent.[41],[42]


  The Specific Case of Parinaud's Oculoglandular Syndrome By Sporotrichosis Top


When related to sex

There is no consensus in the literature; however, an epidemiological report of the Brazilian state of RJ in 2019 showed that there was a predominance of female involvement (62.15%) in relation to males.[34] In ophthalmological evaluation and its annexes, there was a prevalence of males (54%) in relation to females.[10] In another recent study,[27] only with patients with POGS, there was a predominance of females, aged over 40 years.

When age related

In a 2019 report,[34] the most affected age group was from 50 years for women. In other study of 2016,[10] considering mainly the ocular appendages, the highest prevalence of ocular involvement (78%) occurred among individuals from 1 to 15 years. In a 2020 study[27] with 26 cases of POGS, age ranged from 6 to 80 years. Individuals over 60 years of age were the least affected (7.7%).

When related to the initial clinical picture

In the same study published in 2016,[10] five cases of sporotrichosis dacryocystitis were described, but was not associated with POGS out of these, two presented associated conjunctivitis and one nodular lesion ulcerated in appendage. As observed 82% of the patients surveyed in the same study presented some type of associated eyelid lesion and 11.4% presented lacrimal gland involvement. The study also differentiates that eyelid and glandular lesions are more recurrent in individuals under 15 years of age, while lesions associated with conjunctivitis are more recurrent in individuals older than 15 years. Regarding the aspect of adjacent LP, it was observed in 77.3% of patients, with a prevalence of preauricular LP, around 75%, either in isolation or associated with submandibular LP or cervical involvement.

As for the start and the time of diagnosis

As for the onset of symptoms, It is difficult to establish because it is a disease of difficult diagnosis. There are reports of numerous previous treatments without improvement and with mistaken diagnosis, due to the polymorphism of clinical presentations of sporotrichosis, its lesions, for the most part, are not suggestive of the disease.[35] When only eyelid lesions occur, they are often easily confused with nonfungal lesions, especially with the chalazion.[43],[44] If the condition is underdiagnosed, the treatment may become nonspecific and the clinical course may evolve to major ocular complications and sequelae, such as dacryocystitis resulting from the healing process of a juxtapose skin lesion, conjunctival fibrosis, symblepharon, ectropion, paracentral leukoma, and pannus in the limbus.[2],[27],[45] The time lapse between the onset of the disease to the diagnosis varies from three to 122 days, with a median of 29.[27]

Treatment

First-choice treatment is itraconazole. The dose of 100 mg/day, successfully in 73.1% of patients, but 23.1% increased the dose of oral itraconazole to 200 mg/day, with 88.5% showing improvement in the condition, with duration of therapy ranging from eight to 20 weeks and median of 14.[27] Therefore, more recent studies suggest that 200 mg/day is more appropriate.[11] This may be due to greater virulence and association with more severe clinical forms of sporotrichosis, with consequent lower susceptibility to itraconazole, as suggested by study models with S. brasiliensis.[39] In Ramírez-Oliveros et al., initially, patients were treated for 3 months. However, one patient presented with relapse culture-confirmed after 2 months after the finish of the treatment, being necessary additional 5 months to cure.[46] The literature reports a clinical improvement rate of 76.92% for general ocular conditions, of which 47.69% treated only with iodine potassium (KI) therapy, 24.61% with itraconazole, and only 4.61% with KI, itraconazole, and fluconazole;[35] however, 81.8% of patients had previous treatment with numerous other medicines[27] before starting itraconazole.

How much the side of an involvement

In the study by Arinelli et al.,[27] 96.15% of the patients presented with unilateral eye disease and only one bilateral; however, this patient had been diagnosed with acquired immunodeficiency syndrome.

Possible aspects and forms of human contamination

Regarding the aspects and forms of contamination, in 2019,[34] for sporotrichosis in general, regarding the type of contact with the animal, the scratching of felines represented 71.82% of the occurrences and it was observed that 75.60% of the animals were sick, and only 30.36% of them had been treated or were under treatment. Emphasizes the importance of the knowledge of the patient and of the community, in relation to the possibility of transmission occures by the felines, since that, studies suggest cats the main transmitting agent. Therefore, the adult cat, young, male, uncastrated, and without defined breed, becomes a central part of the process, because it is the main one involved in the dispersion of the fungus, completing the transmission to other animals and humans.[47],[48] The same report[34] shows that the vast majority of affected cases, 78.5%, reported a history of contact with animals, of these, cats represented 97.62%. As for the history of contact or manipulation of soil/land/garden, 18.7%, as noted in the graph below.

In a series of 21 cases in Peru with ophthalmologic involvement,[10] 23% of the patients had contact with felines, 33.33% of them were sick, and only 3% had or a clear history of traumatic inoculation by plant material. Nevertheless, 72.5% of the patients did not clearly present any determining risk factor. There is a single case report in literature that considers human ocular sporotrichosis transmitted by felines, a rare infection.[45] However, in a recent study with 26 cases of POGS, 96% of patients reported home or professional contact with cats with sporotrichosis and total 47.4% reported having suffered traumatic lesion of felines with sporotrichosis that preceded the symptoms. According to the literature, during the last 20 years, there has been an increase in the number of cases of sporotrichosis. Since the middle of the 20th century, the cases has occurred in isolation or in small outbreaks, with few reported cases of zoonotic transmission. The highest incidence is located in the Southeast region of Brazil[17],[49] with RJ being a hyperendemic locality.

Prognosis

The prognosis of POGS syndrome is generally good, with cases lasting for 5–7 days.[3] Although, is described some complications of the sporotrichosis infection like suppurative chronic dacryocystitis, scleritis, iridocyclitis, retinochoroiditis and e endophthalmitis.[1]


  Conclusion Top


POGS, although classically related to CSD, mainly by Bartonella henselae, can be caused by Sporothrix sp. GC is the most important presentation of the condition. When associated with ipsilateral LP, it is even more relevant due to the difficulty in diagnosis. If not performed early or if the individual is not treated properly, it may develop ocular sequelae. In endemic areas and especially in hyperendemic areas, ocular sporotrichosis associated with POGS, should be considered a differential diagnosis of external ophthalmologic diseases, especially if this patient presents a history of contact with felines or gardening. Regardless of the initial dosage, itraconazole should be the medication of choice for treatment and this patient should be followed up for complete clinical improvement, with family members oriented on possible sources of contamination. Because it is a neglected public health problem in Brazil, it is essential to understand this disease properly, especially in the southeast region, particularly in RJ. The substantial increase in cases in southern Brazil, especially in Rio Grande do Sul, turns on an important red light for the countries of the Southern Cone of SA, as we can see in [Figure 1], which demonstrates the geographic distribution in detail, especially for those bordering the Southern Cone, such as Argentina, Uruguay and Paraguay, and serves as a warning to countries with more expressive numbers, such as Peru, also shown in [Figure 1].
Figure 1: Map of South America, showing the Southern Cone and the Brazilian states of the southeastern and southern regions, as well as the countries of the Southern Cone bordering the respective states: Argentina, Uruguay and Paraguay; in addition to Peru, due to the large number of the disease

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Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
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