You are viewing the site in preview mode

Skip to content

Advertisement

  • Case report
  • Open Access
  • Open Peer Review

Case of disseminated histoplasmosis in a HIV-infected patient revealed by nasal involvement with maxillary osteolysis

BMC Infectious DiseasesBMC series – open, inclusive and trusted201717:328

https://doi.org/10.1186/s12879-017-2419-4

  • Received: 19 November 2016
  • Accepted: 25 April 2017
  • Published:
Open Peer Review reports

Abstract

Background

Disseminated Histoplasmosis (DH) is a rare manifestation of Acquired Immune Deficiency Syndrome (AIDS) in European countries. Naso-maxillar osteolysis due to Histoplasma capsulatum var. capsulatum (Hcc) is unusual in endemic countries and has never been reported in European countries. Differential diagnoses such as malignant tumors, cocaine use, granulomatosis, vasculitis and infections are more frequently observed and could delay and/or bias the final diagnosis.

Case presentation

We report the case of an immunocompromised patient infected by Human Immunodeficiency Virus (HIV) with naso-maxillar histoplasmosis in a non-endemic country. Our aim is to describe the clinical presentation, the diagnostic and therapeutic issues. A 53-year-old woman, originated from Haiti, was admitted in 2016 for nasal deformation with alteration of general condition evolving for at least 6 months. HIV infection was diagnosed in 2006 and classified at AIDS stage in 2008 due to cytomegalovirus infection associated with pulmonary histoplasmosis. At admission, CD4 cell count was 9/mm3. Surgical biopsies were performed and ruled out differential or associated diagnoses. Mycological cultures identified Hcc and Blood Polymerase Chain Reaction (PCR) for Hcc was positive. The patient was given daily Amphothericin B liposomal infusion during 1 month. Hcc PCR became negative in the blood under treatment, and then oral switch by itraconazole was introduced. Antiretroviral treatment was reintroduced after a 3-week histoplasmosis treatment. Normalization of naso-maxillar mucosa enabled a palatal prosthesis.

Conclusion

Naso-maxillar histoplasmosis is extremely rare; this is the first case ever reported in a non-endemic country. Differential diagnoses must be ruled out by conducting microbiologic tools and histological examinations on surgical biopsies. Early antifungal treatment should be initiated in order to prevent DH severe outcomes.

Keywords

  • Case report
  • Histoplasmosis
  • HIV
  • Maxillary osteolysis
  • Immunocompromized

Background

Histoplasmosis is caused by a dimorphic saprophytic fungus, Histoplasma capsulatum which presents two variants: Histoplasma capsulatum var. capsulatum (Hcc) and Histoplasma capsulatum var. duboisii (Hcd). Hcc is commonly found in soil contaminated with bird or bat droppings. Primary infection occurs through inhalation of spores [1].

Hcc can take different clinical forms including Disseminated Histoplasmosis (DH) in immunocompromised individuals, such as patients with Acquired Immune Deficiency Syndrome (AIDS). DH is associated with AIDS in 70% to 90% of cases in endemic countries such as South American countries; however, it remains extremely rare in European countries. DH can involve various organs and naso-oral histoplasmosis is an uncommon manifestation of DH [2, 3].

This article reports the first case of nasal-oral histoplasmosis with naso-maxillar osteolysis in a patient infected by Human Immunodeficiency Virus (HIV) at AIDS stage, in a non-endemic country. Naso-maxillar osteolysis can be observed in tumors, infections, granulomatosis, vasculitis or drug exposure.

Our aim is to describe the clinical presentation, the diagnoses issues and the etiologic and functional treatments of naso-oral histoplasmosis.

Case presentation

We report the case of a 53 year-old woman, originally from Haiti, living in France since 1989. She was hospitalized in the infectious diseases department of Bichat Claude Bernard University Hospital in Paris in March 2016 for alteration of general condition, fever and nasal deformity evolving for at least 6 months.

Her medical history is characterized by an HIV infection diagnosed in 2006, which was classified at AIDS stage in 2008 due to cytomegalovirus infection. At the same time, she suffered from pulmonary histoplasmosis that was treated with itraconazole. CD4 cell count nadir amounted to 7/mm3 in 2008. A first line of Highly Active Antiretroviral Therapy (HAART) was started 3 weeks after those diagnoses consisting in Efavirenz (EFV), Tenofovir Disoproxil Fumarate (TDF) and Emtricitabine (FTC). After 1,5 months the patient decided to interrupt this treatment, a second line of HAART was initiated 6 months later with nevirapine and TDF/FTC. She only took secondary prophylaxis with itraconazole for 6 months and then stopped being compliant with any treatment and was lost to follow-up over 7 years. No history of recent travel to endemic areas or contact with neither birds nor bats was reported. She never smoked, did not have excessive alcohol consumption and did not inhale any nasal drugs.

At hospital admission, physical examination revealed a nasal tip collapse, a disappearance of the nasal septum and a large perforation of the hard palate, resulting in naso-oral communication. Facial skin, alar and triangular cartilages were undamaged. However, maxillary teeth [4, 5] were loose, and teeth 11, 21 and 22 fell spontaneously. Mucosa of the nasal cavity was ulcerated with crusts and partially necrotic (Fig. 1). The sinus CT-scan and the magnetic resonance imaging performed showed: a complete loss of the nasal septum, a maxillar osteolysis, a communication between oral and nasal cavities and bilateral maxillary sinus opacities (Fig. 2). The chest X-ray showed an interstitial pneumonia. She did not manifest dyspnea, cough, cutaneous eruption, neurologic deficit, visceromegaly or lymphadenopathy. HIV viral load was 56,943 copies/ml and CD4 cell count was 9/mm3 (2%). In blood: Treponema Pallidum Hemagglutination Assay and Veneral Disease Research Laboratory, Cryptococcus antigen, Toxoplasma polymerase chain reaction (PCR), Leishmania PCR, galactomannan antigen, blood and mycological (×4) cultures were all negative. β-D-Glucane was positive at 338 pg/ml. Blood Hcc PCR was positive. In bronchoalveolar fluid: cultures, Cryptococcus antigen were negative, Pneumocystis jirovecii PCR level was barely positive (18,000 copies/mL), After 3 months, Mycobacterium tuberculosis sputum cultures were negative.
Fig. 1
Fig. 1

Clinical presentation of the case. a: Three-quarter picture of the face; b: Profile picture of the face; c: Face picture of the face showing lack of teeth 11, 21 and 22 which fall spontaneously; d: Bottom view of the face: nasal tip collapse, hard palate lysis and remaining nasal septum through the hole

Fig. 2
Fig. 2

Imaging exploration. a: Sinus CT-scan showing bony nasal septum lysis and bilateral maxillary sinus opacities; b and c: Gadolinium-enhanced T1 weighted MRI (b: axial section; c: frontal section) showing bony nasal septum lysis and maxillar lysis without enhanced tumor mass

Surgical biopsies of oral, nasal and maxillary mucosa were performed and analyzed. Microscopic examination revealed fungal yeasts (Fig. 3), mycological cultures identified the presence of Hcc then confirmed by PCR.
Fig. 3
Fig. 3

Histological analysis of naso-maxillar biopsy. a and c: Grocott staining; b: Gram Wegert staining; d: PAS staining

Those tests enabled a final diagnosis of DH with naso-oral involvement in an AIDS-stage patient.

The patient received 200 mg per day of intravenous Amphotericin B (AmphoB) liposomal for 1 month. In the follow-up, we observed: negativation of blood histoplasmosis PCR in 10 days and clinical stabilization of naso-maxillary osteolysis with normalization of mucosa. Treatment was switched to 400 mg of oral itraconazole per day for a minimum of 1 year, in accordance with international guidelines [6].

HAART by ritonavir-boosted darunavir and TDF/FTC was reintroduced after 3 weeks of positive response to DH treatment. After 6 months, HIV viral load was undetectable and CD4 cell count at 40/mm3. At 9 months, biological results were stable and she had gained 17 k. Strategy of directly observed therapy permitted full compliance and the patient didn’t report any side effect with any treatment. Blood levels of itraconazole and HAART were both in the standards.

Ulceration and inflammation of the mucus decreased, enabling a palatal prosthesis to be implemented. A reconstructive surgery will be proposed to the patient upon completion of antifungal therapy and stabilization of HIV infection.

Discussion

In immunocompromised individuals such as AIDS patients, especially when CD4 cell count is under 150/mm3, Hcc can produce a DH involving various organs, such as: liver, spleen, bone marrow, lymphnodes, gastrointestinal tract and central nervous system [2, 7]. Oral histoplasmosis is a rare lesion in DH and is hardly documented even in endemic regions. Palate, gingiva and tongue are the most frequently locations [3, 8]. Naso-maxillar histoplasmosis is extremely rare; we report the first case in a non-endemic country. It has previously been described that the lower CD4 T cell count is, the higher the probability of nasal and mucous lesion as manifestation of DH [7, 9, 10]. Our patient‘s very low CD4 T cell counts supports this hypothesis.

Other etiologies of naso-maxillar osteolysis have to be discussed and ruled out: i) non-infectious etiologies (malignant tumors, Wegener’s granulomatosis, sarcoidosis and consequences of drug exposure) and ii) other infectious etiologies (tuberculosis, leprosy, leishmaniosis, paracoccidioidomycosis and mucormycosis). The most frequent infectious cause of nasal lesion in AIDS patients is leishmaniosis.

The issue is that histoplasmosis can be confused with leishmaniosis for the following reasons: first of all Histoplasma yeasts could be interpreted as Leishmania amastigotes in direct examination; second, leishmaniosis frequently affects nasal mucosa [11, 12].

Because of its severity, mucormycosis must be explored and ruled out in this context, since very similar cases of maxillary osteolysis have been reported [13].

Chronic nasal ulcerations and nasal septum perforation can be symptoms of vasculitis, especially granulomatosis with polyangiitis (GPA) also known as Wegener’s granulomatosis. Unfortunately, the histological results show the classical triad of granulomatous inflammation, necrosis and vasculitis in up to 16% of cases of GPA. Diagnosis of GPA is based on a combination of clinical symptoms, histology and positive c-ANCA serology [14]. One case of naso-septal perforation related to Takayashu’s arteritis is reported [4]. In Behçet disease, patients with nasal mucosa involvement do not have more nasal manifestations than those without [15]. However no case of maxillary osteolysis caused by vasculitis has been reported in the literature so far.

An increasing cause of midface destructive lesions is cocaine exposure. Ischemia, mucociliar clearance modification, bacterial infection and lesions due to intranasal consumption lead to septal and hard palate perforation [16, 17]. In this context, a rise of c-ANCA may be possible, and may lead to a misdiagnosis with GPA. Nevertheless, necrosis and inflammation without vasculitis would be observed at histology examination [18].

At last, maxillary osteolysis can be observed in malignant tumors like mucoepidermoid carninoma, squamous-cell carcinoma and lymphoma [19, 20]. Extranodal NK/T-cell lymphoma associated with Epstein-Barr virus infection has to be highlighted because of its severity and the difficulties to diagnose it. It can lead to a misdiagnosis such as GPA [21, 22].

In literature only 18 cases of nasal mucosa involvement due to Hcc have been reported (Table 1). Three of them died because of delay in introducing treatment or non-adherence to treatment. Treatment was either AmphoB or itraconazole. Among patients, 12 had HIV related immunodeficiency, when it was reported, CD4 cell counts was always <150/mm3.
Table 1

Clinical characteristics of nasal and oral histoplasmosis in 18 patients

N°/Ref

Sex

Age (years)

Risk Factor

CD4 (/mm3)

Clinical Presentation

Diagnosis

Location

Treatment

Follow up (M: months)

Country

1 [31]

M

32

HIV infection

60

Pain

Histology

Nasal septum perforation

Amphotericin B then itraconazole

6 M, Improvement

Colombia

2 [31]

F

37

HIV infection

133

Nasal itch, epistaxis, nasal discharge

Histology

Nasal septum perforation

Itraconazole

2 M, Improvement

Colombia

3 [32]

M

59

HCV infection

 

Nose wound with crust

Not available

Nasal ulceration covered by crusts

Itraconazole

1 M, Improvement

Brazil

4 [33]

M

27

HIV infection

20

Fatigue, fever, skin lesions, dyspnea

Histology

Disseminated (nasal ulceration and cutaneous)

Amphotericin B then itraconazole

Improvement

Argentina

5 [34]

M

37

HIV infection

Not available

Fever, dysphagia, inflammatory and hemorrhagic nasal process

Histology

Destruction of nasal septum

No treatment

Death

Brazil

6 [35]

M

30

None

 

Nasal swelling

Histology

Nasal crusts

Itraconazole

Lost follow-up

India

7 [23]

F

79

Farmer

 

Fatigue, nasal obstruction

Histology

Nasal ulceration and crusts

Itraconazole

Lost follow-up

USA (Ohio)

8 [36]

M

37

Renal transplant, HBV/HCV coinfection

 

Nose septal destruction

Not available

Ulceration in mouth and nose

Amphotericin B then itraconazole

1 M, Improvement

Brazil

9 [37]

F

32

HIV infection

69

Fatigue, fever, nasal pain, nasal pyramid collapse

Histology

Destruction of the cartilaginous septum, columella and left nasal wing, and ulcerations

Amphotericin B

12 M, Improvement

Brazil

10 [38]

M

39

HIV infection

20

Nasal congestion, post nasal rhinorrhea, cough

Histology

Sinusitis, Skin rash, pulmonary involvement

Itraconazole

Improvement

USA (La)

11 [39]

F

49

HIV infection

Not available

Nasal obstruction

Histology and culture

Lesion on the nasal vestibule and septum

Not available

Death

Brazil

12 [39]

F

23

HIV infection

Not available

Not available

Histology

Crusts

Amphotericin B then itraconazole

Improvement

Brazil

13 [40]

M

43

HIV infection, farmer

15

Nasal regurgitation

Histology

Complete destruction of the nasal architecture, palatal perforation

Itraconazole

Improvement

Brazil

14 [41]

M

39

HIV infection

120

Nasal obstruction, post nasal rhinorrhea, headache, epistaxis

Histology

Papular and nodular rash, polypoid and inflammatory nasal mucosa in the right nasal fossa, bulging posterior wall of the nasopharynx

Amphotericin B

Improvement

Morocco

15 [42]

M

30

Adrenal insufficiency

 

Visual acuity impairment, nasal, septum and soft palate lesions

Histology

Endophtalmitis, nasal, septum and soft palate lesions

Amphotericin B (intraocular injection), itraconazole

12 W, Improvement

Argentina

16 [43]

NA

NA

HIV infection

Not available

Not available

Not available

Mouth, gingivae, hard palate, right maxillary sinus, right nasal cavity

Not available

Not available

South Africa

17 [44]

M

76

Chronic lymphocytic leukemia

 

Epistaxis and facial pain, facial erythema, swelling, and fever

Histology and culture

Ethmoïdal, sphenoidal and maxillary sinusitis

Amphotericin B then itraconazole

Improvement

Brazil

18 [45]

M

36

HIV infection, drug abuse

Not available

Fever, orodynia

Histology

Ulceration on the nasal bridge, necrotizing gingivitis and granulomatous oral lesion

Ketoconazole

4 M, Death

Brazil

Rizzi and al. reported a case of nasal histoplasmosis in an immunocompetent 79-year-old woman with nasal obstruction. Based on the histopathological examination, it was misdiagnosed with sarcoidosis and aggravation was observed on corticosteroids [23].

Generally speaking, diagnosis of histoplasmosis can be difficult because of its low frequency, its non-specific clinical presentation and some histological similarities with others causes of nasal damage [5, 11].

A review of literature reported only 72 patients with AIDS having presented histoplasmosis in Europe between 1984 and 2004 [24]. The diagnosis of histoplasmosis is based on mycological examination, antigen detection or detection of Histoplasma DNA by PCR. The limits are: the unlikelihood to see yeast with GIEMSA staining, the duration of the culture (up to 4 weeks) and its lack of sensitivity [25].

Antigen detection is quick (within 24 h) and allows monitoring response to treatment [26]. Unfortunately, this test is not available in non-endemic countries. Besides, false negatives results can occur especially in immunocompromised patients, as well as false positives results because of cross-reaction with other fungal infections [27]. In European countries, galactomannan antigen is usually used as a surrogate marker of histoplasmosis, especially on HIV patients. The sensitivity of this test is proportional to fungal load [28]. The negative result in our case study may be explained by the fact that it was conducted after treatment initiation.

Thanks to development of genetic diagnostic tools, histoplasmosis DNA can be detected by PCR either on blood sample or on tissue specimens. Its very good sensitivity, its 100% of specificity, and the rapidity to obtain the results make it the most reliable test as of today [29, 30]. Thus, if available, PCR must be performed on blood and tissue samples as soon as the diagnosis of histoplasmosis is suggested.

Conclusion

Nasal histoplasmosis should be suspected for patients coming from endemic region, with deep immunosuppression (especially in AIDS patients).

Our patient is the first case of nasal architecture destruction by Hcc reported to date in a non-endemic region. After 1 year of treatment, she has had a really encouraging clinical course with good compliance illustrated by: controlled HIV infection, controlled DH and significant weight gain.

Given the very wide range of etiologies, the non-specific symptoms and the difficulty of histological analysis, a reliable diagnosis requires a thorough knowledge of maxillary osteolysis causes and an efficient cooperation and communication between surgeon, infectious disease clinician, mycologist and pathologist.

Abbreviations

AIDS: 

Acquired immune deficiency syndrome

AmphoB: 

Amphotericin B

CMV: 

Cytomegalovirus

DRV: 

Darunavir

DH: 

Disseminated Histoplasmosis

EFV: 

Efavirenz

FTC: 

Emtricitabine

F: 

Female

GPA: 

Granulomatosis with Polyangiitis

HBV: 

Hepatitis B virus

HCV: 

Hepatitis C virus

HAART: 

Highly active antiretroviral therapy

Hcc

Histoplasma capsulatum var. capsulatum

Hcd

Histoplasma capsulatum var. duboisii

HIV: 

Human Immunodeficiency Virus

M: 

Male

M: 

Months

NVP: 

Nevirapine

PCR: 

Polymerase chain reaction

RTV: 

Ritonavir

TDF: 

Tenofovir disoproxil fumarate

VDRL: 

Veneral disease research laboratory

Declarations

Acknowledgements

Not applicable.

Funding

Not applicable.

Availability of data and materials

The data that support the findings of this study are available from the corresponding author (DV) upon reasonable request.

Authors’ contributions

A.C.L., J.P. have been involved in the acquisition and analysis of data and then drafting of the infectious part of the manuscript. They took care of the patient during hospitalization in the infectious diseases department. M.Z. have been involved in the acquisition and analysis of data and then drafting the surgical and Otorhinolaryngology part of the manuscript. M.Z. and A.P. were the surgeons of the patient. V.G., S.D., A.B., C.R., A.P., D.V. have been involved in revising critically the manuscript (A.P. for the Otorhinolaryngology part and others for the infectious part). A.B., C.R., A.P., D.V have given the final approval of the version to be published. They all took care of the patient during hospitalization. D.V. and A.P. did the submission.

Competing interests

The authors declare that they have no competing interests.

Consent for publication

Consent of the patient was obtained.

Ethics approval and consent to participate

Not applicable.

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

Authors’ Affiliations

(1)
Infectious and Tropical Diseases Department, University Hospital Bichat-Claude Bernard, APHP, 46 rue Henri Huchard, 75018 Paris, France
(2)
Otorhinolaryngology Department, University Hospital Bichat-Claude Bernard, APHP, Paris, France
(3)
Hematology Department, Meaux Hospital, Meaux, France
(4)
General Medecine and Infectious Diseases Department, Melun Hospital, Melun, France

References

  1. Sarosi G, Deepe J. Histoplasma capsulatum (Histoplasmosis). In: Mandell, Douglas, and Bennett’s principles and practice of infectious diseases. Eighth ed. Edinburgh: Elsevier Science Limited and W.B. Saunders; 2015. p. 2949–62.Google Scholar
  2. Sarosi G, Johnson P. Disseminated Histoplasmosis in patients infected with human immunodeficiency virus. Clin Infect Dis. 1992;14(Suppl 1):S60–7.View ArticlePubMedGoogle Scholar
  3. Wheat LJ, Conolly-Stringfield P. Disseminated histoplasmosis in the acquired immune deficiency syndrome: clinical findings, diagnosis and treatment, and review of the literature. Medicine (Baltimore). 1990;69(6):361–74.View ArticleGoogle Scholar
  4. Akar S, Dogan E, Goktay Y, Can G, Akkoc N, Sarioglu S, et al. Nasal septal perforation in a patient with Takayasu’s arteritis; a rare association. Intern Med Tokyo Jpn. 2009;48(17):1551–4.View ArticleGoogle Scholar
  5. Talvalkar GV. Histoplasmosis simulating carcinoma: a report of three cases. Indian J Cancer. 1972;9(2):149–53.PubMedGoogle Scholar
  6. Wheat LJ, Freifeld AG, Kleiman MB, Baddley JW, McKinsey DS, Loyd JE, et al. Clinical practice guidelines for the Management of Patients with Histoplasmosis: 2007 update by the Infectious Diseases Society of America. Clin Infect Dis. 2007;45(7):807–25.View ArticlePubMedGoogle Scholar
  7. Silva TC, Treméa CM, Zara ALSA, Mendonça AF, Godoy CSM, Costa CR, et al. Prevalence and lethality among patients with histoplasmosis and AIDS in the Midwest region of Brazil. Mycoses. 2017;60(1):59–65.View ArticlePubMedGoogle Scholar
  8. Goodwin R, Shapiro J, Thurman G. Disseminated histoplasmosis: clinical and pathologic correlations. Medicine (Baltimore). 1980;59:1–33.View ArticleGoogle Scholar
  9. Couppie P. Acquired immunodeficiency syndrome related oral and/or Cutaneous Histoplasmosis: a descriptive and comparative study of 21 cases in French Guiana. Int J Dermatol. 2002;41:571–6.View ArticlePubMedGoogle Scholar
  10. Cunha V. Mucocutaneous manifestations of disseminated Histoplasmosis in patients with acquired immunodeficiency syndrome: particular aspects in a Latin-American population. Clin Exper Dermatol. 2007;32:250–5.View ArticleGoogle Scholar
  11. Jaimes A, Muvdi S, Alvarado Z, Rodríguez G. Perforation of the nasal septum as the first sign of histoplasmosis associated with AIDS and review of published literature. Mycopathologia. 2013 Aug;176(1–2):145–50.View ArticlePubMedGoogle Scholar
  12. Pérez C, Yoanet S, Rodríguez G. Diffuse cutaneous leishmaniasis in a patient with AIDS. Biomedica. 2006;26(4):485–97.View ArticlePubMedGoogle Scholar
  13. Selvamani M, Donoghue M, Bharani S, Madhushankari GS. Mucormycosis causing maxillary osteomyelitis. J Nat Sci Biol Med. 2015;6(2):456–9.View ArticlePubMedPubMed CentralGoogle Scholar
  14. Greco A, Marinelli C, Fusconi M, Macri GF, Gallo A, De Virgilio A, et al. Clinic manifestations in granulomatosis with polyangiitis. Int J Immunopathol Pharmacol. 2016;29(2):151–9.View ArticlePubMedGoogle Scholar
  15. Shahram F, Zarandy MM, Ibrahim A, Ziaie N, Saidi M, Nabaei B, et al. Nasal mucosal involvement in Behçet disease: a study of its incidence and characteristics in 400 patients. Ear Nose Throat J. 2010;89(1):30–3.PubMedGoogle Scholar
  16. Silvestre FJ, Perez-Herbera A, Puente-Sandoval A, Bagán JV. Hard palate perforation in cocaine abusers: a systematic review. Clin Oral Investig. 2010;14(6):621–8.View ArticlePubMedGoogle Scholar
  17. Tartaro G, Rauso R, Bux A, Santagata M, Colella G. An unusual oronasal fistula induced by prolonged cocaine snort. Case report and literature review. Minerva Stomatol. 2008;57(4):203–10.PubMedGoogle Scholar
  18. Stahelin L, Fialho SC, De MS NFS, Junckes L, Werner De Castro GR, Pereira IA. Cocaine-induced midline destruction lesions with positive ANCA test mimicking Wegener’s granulomatosis. Rev Bras Reumatol. 2012;52(3):431–7.View ArticlePubMedGoogle Scholar
  19. Kolude B, Lawoyin JO, Akang EE. Mucoepidermoid carcinoma of the oral cavity. J Natl Med Assoc. 2001;93(5):178–84.PubMedPubMed CentralGoogle Scholar
  20. Becker C, Kayser G, Pfeiffer J. Squamous cell cancer of the nasal cavity: new insights and implications for diagnosis and treatment. Head Neck. 2016;38(Suppl 1):E2112–7.View ArticlePubMedGoogle Scholar
  21. Vasil’ev VI, Sedyshev SK, Gorodetskiĭ BP, Probatova NA, Gaĭduk IV, Logvinenko OA, et al. Differential diagnosis of Wegener’s granulomatosis and extranodal NK/T-cell lymphoma, nasal type. Ter Arkh. 2012;84(7):79–83.PubMedGoogle Scholar
  22. Aozasa K, Takakuwa T, Hongyo T, Yang W-I. Nasal NK/T-cell lymphoma: epidemiology and pathogenesis. Int J Hematol. 2008;87(2):110–7.View ArticlePubMedPubMed CentralGoogle Scholar
  23. Rizzi MD, Batra PS, Prayson R, Citardi MJ. Nasal histoplasmosis. Otolaryngol--Head Neck Surg Off J Am Acad Otolaryngol-Head Neck Surg. 2006;135(5):803–4.View ArticleGoogle Scholar
  24. Antinori S, Magni C, Nebuloni M, Parravicini C, Corbellino M, Sollima S, et al. Histoplasmosis among human immunodeficiency virus-infected people in Europe: report of 4 cases and review of the literature. Medicine (Baltimore). 2006;85(1):22–36.View ArticleGoogle Scholar
  25. Wheat LJ. Current diagnosis of histoplasmosis. Trends Microbiol. 2003;11(10):488–94.View ArticleGoogle Scholar
  26. Wheat LJ. Histoplasmosis: a review for clinicians from non-endemic areas. Mycoses. 2006;49(4):274–82.View ArticlePubMedGoogle Scholar
  27. Durkin M, Witt J, LeMonte A, Wheat B, Connolly P. Antigen assay with the potential to aid in diagnosis of Blastomycosis. J Clin Microbiol. 2004;42(10):4873–5.View ArticlePubMedPubMed CentralGoogle Scholar
  28. Rivière S, Denis B, Bougnoux M-E, Lanternier F, Lecuit M, Lortholary O. Serum Aspergillus galactomannan for the management of disseminated histoplasmosis in AIDS. AmJTrop Med Hyg. 2012;87(2):303–5.View ArticleGoogle Scholar
  29. Buitrago MJ, Canteros CE, Frías De León G, González Á, Marques-Evangelista De Oliveira M, Muñoz CO, et al. Comparison of PCR protocols for detecting Histoplasma capsulatum DNA through a multicenter study. Rev Iberoam Micol. 2013;30(4):256–60.View ArticlePubMedGoogle Scholar
  30. Dantas KC, Freitas RS, Moreira APV, Da Silva MV, Benard G, Vasconcellos C, et al. The use of nested polymerase chain reaction (nested PCR) for the early diagnosis of Histoplasma capsulatum infection in serum and whole blood of HIV-positive patients. An Bras Dermatol. 2013;88(1):141–3.View ArticlePubMedPubMed CentralGoogle Scholar
  31. Jaimes A, Muvdi S, Alvarado Z, Rodríguez G. Perforation of the nasal septum as the first sign of histoplasmosis associated with AIDS and review of published literature. Mycopathologia. 2013;176(1–2):145–50.View ArticlePubMedGoogle Scholar
  32. Manzini M, Lavinsky-Wolff M. Nasal histoplasmosis without lung involvement in an immunocompromised patient. Braz J Otorhinolaryngol. 2012;78(5):136.View ArticlePubMedGoogle Scholar
  33. Rico MF, Asensio P, Pavón G, Scasso M, Brusco J, Chabbert PM, et al. Histoplasmosis diseminada. Arch Argent Dermatol. 2010;60:105–10.Google Scholar
  34. Oikawa F, Carvalho D, Matsuda NM, Yamada AT. Histoplasmosis in the nasal septum without pulmonary involvement in a patient with acquired immunodeficiency syndrome: case report and literature review. Sao Paulo Med J. 2010;128(4):236–8.View ArticlePubMedGoogle Scholar
  35. Sood N, Gugnani HC, Batra R, Ramesh V, Padhye AA. Mucocutaneous nasal histoplasmosis in an immunocompetent young adult. Indian J Dermatol Venereol Leprol. 2007;73(3):182–4.View ArticlePubMedGoogle Scholar
  36. Motta ACF, Galo R, Lourenço AG, Komesu MC, Arruda D, Velasco FG, et al. Unusual orofacial manifestations of histoplasmosis in renal transplanted patient. Mycopathologia. 2006;161(3):161–5.View ArticlePubMedGoogle Scholar
  37. Felix F, Gomes GA, Pinto PCL, Arruda AM, Da Penha Costa Marques M, Tomita S. Nasal histoplasmosis in the acquired immunodeficiency syndrome. J Laryngol Otol. 2006;120(1):67–9.View ArticlePubMedGoogle Scholar
  38. Butt AA, Carreon J. Histoplasma capsulatum sinusitis. J Clin Microbiol. 1997;35(10):2649–50.PubMedPubMed CentralGoogle Scholar
  39. Machado AA, Coelho IC, Roselino AM, Trad ES, Figueiredo JF, Martinez R, et al. Histoplasmosis in individuals with acquired immunodeficiency syndrome (AIDS): report of six cases with cutaneous-mucosal involvement. Mycopathologia. 1991;115(1):13–8.View ArticlePubMedGoogle Scholar
  40. Mehta V, De A, Balachandran C, Monga P. Mucocutaneous histoplasmosis in HIV with an atypical ecthyma like presentation. Dermatol Online J. 2009;15(4):10.PubMedGoogle Scholar
  41. Elansari R, Abada R, Rouadi S, Roubal M, Mahtar M. Histoplasma capsulatum sinusitis: possible way of revelation to the disseminated form of histoplasmosis in HIV patients: case report and literature review. Int J Surg Case Rep. 2016;24:97–100.View ArticlePubMedPubMed CentralGoogle Scholar
  42. Schlaen A, Ingolotti M, Couto C, Jacob N, Pineda G, Saravia M. Endogenous Histoplasma capsulatum endophthalmitis in an immunocompetent patient. Eur J Ophthalmol. 2015;25(4):e53–5.View ArticlePubMedGoogle Scholar
  43. White J, Khammissa R, Wood NH, Meyerov R, Lemmer J, Feller L. Oral histoplasmosis as the initial indication of HIV infection: a case report. SADJ J South Afr Dent Assoc Tydskr Van Suid-Afr Tandheelkd Ver. 2007;62(10):452. 454–5Google Scholar
  44. Alves MD, Pinheiro L, Manica D, Fogliatto LM, Fraga C, Goldani LZ. Histoplasma capsulatum sinusitis: case report and review. Mycopathologia. 2011;171(1):57–9.View ArticlePubMedGoogle Scholar
  45. Souza Filho FJ, Lopes M, Almeida OP, Scully C. Mucocutaneous histoplasmosis in AIDS. Br J Dermatol. 1995;133(3):472–4.View ArticlePubMedGoogle Scholar

Copyright

© The Author(s). 2017

Advertisement