Pulmonary Nocardiosis in Pemphigus Vulgaris Patients from Tehran, Iran

Author(s): Hossein Ali Rahdar, Abass Bahador, Shahram Shahraki-Zahedani, Morteza Karami-Zarandi, Tahereh Soori, Sirous Jafari, Mohammad Mehdi Feizabadi*

Journal Name: Infectious Disorders - Drug Targets
Formerly Current Drug Targets - Infectious Disorders

Volume 21 , Issue 1 , 2021

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Objective: Nocardiosis is an opportunistic infection in individuals who had organ transplants and in patients with immunosuppressive diseases such as pemphigus Vulgaris (PV), diabetes mellitus, and HIV. Nocardiosis rate has not been assessed in Iranian PV patients, and this was the first study to estimate nocardiosis rate in these patients.

Methods: In this study, 103 patients with PV were examined. BAL samples were obtained and direct smear was prepared and visualized by microscopy after PAS staining. Samples were cultured on antibiotic-containing blood and chocolate agar media. DNA extraction and PCR were performed on positive cultures, and final identification was done by 16S rRNA gene sequencing. Drug susceptibility testing was done by microbroth dilution method.

Results: Four positive cultures (3.88%) were found in the samples (n = 103). According to sequence analysis, 2 isolates were identified as Nocardia cyriacigeorgica and 2 as Nocardia otitidiscaviarum and Nocardia cerradoensis. Nocardia cerradoensis was isolated from an invasive brain infection. Isolated bacteria were susceptible to majority of the tested antibiotics, except for 2 strains of Nocardia cyriacigeorgica and Nocardia cerradoensis. This was the first isolation of Nocardia cerradoensis of human infection in Asia. Patients with PV are susceptible to nocardiosis, similar to other immunocompromised patients.

Conclusion: Pemphigus Vulgaris is a severe autoimmune disease which is treated by a high dosage of corticosteroids. Opportunistic infections are one of the greatest challenges of these patients. One of the neglected agents of opportunistic infection in this disorder is Nocardiosis which can cause a high mortality rate in PV patients.

Keywords: Nocardiosis, 16S rRNA, pemphigus vulgaris, immunocompromised, Nocardia cyriacigeorgica, Nocardia cerradoensis.

Fatahi-Bafghi, M. Nocardiosis from 1888 to 2017. Microb. Pathog., 2018, 114, 369-384.
[http://dx.doi.org/10.1016/j.micpath.2017.11.012] [PMID: 29146497]
Rahdar, H.A.; Azadi, D.; Shojaei, H.; Daei-Naser, A. Molecular analysis and species diversity of Nocardia in the hospital environment in a developing country, a potential health hazard. J. Med. Microbiol., 2017, 66(3), 334-341.
[http://dx.doi.org/10.1099/jmm.0.000436] [PMID: 28100300]
Brown-Elliott, B.A.; Brown, J.M.; Conville, P.S.; Wallace, R.J. Jr Clinical and laboratory features of the Nocardia spp. based on current molecular taxonomy. Clin. Microbiol. Rev., 2006, 19(2), 259-282.
[http://dx.doi.org/10.1128/CMR.19.2.259-282.2006] [PMID: 16614249]
Blümel, J.; Blümel, E.; Yassin, A.F.; Schmidt-Rotte, H.; Schaal, K.P. Typing of Nocardia farcinica by pulsed-field gel electrophoresis reveals an endemic strain as source of hospital infections. J. Clin. Microbiol., 1998, 36(1), 118-122.
[PMID: 9431933]
Subhash, H.S.; Christopher, D.J.; Roy, A.; Cherian, A.M. Pulmonary nocardiosis in human immunodeficiency virus infection: a tuberculosis mimic. J. Postgrad. Med., 2001, 47(1), 30-32.
[PMID: 11590288]
Yamada, S.M.; Nakai, E.; Toyonaga, S.; Nakabayashi, H.; Park, K.C.; Shimizu, K. A rapidly enlarging nocardial brain abscess mimicking malignant glioma. J. Nippon Med. Sch., 2005, 72(5), 308-311.
[http://dx.doi.org/10.1272/jnms.72.308] [PMID: 16247233]
Rahdar, H.A.; Salehi, M.R.; Bahador, A.; Jasemi, S.; Karami-Zarandi, M.; Nejad, M.H.; Amani, J.; Feyisa, S.G.; Kardan-Yamchi, J.; Feizabadi, M.M. Detection of Nocardia, Streptomyces and Rhodococcus from bronchoalveolar lavage specimens of patients with HIV by Multiplex PCR Assay. Ethiop. J. Health Sci., 2019, 29(6)
Ahmed, A.R.; Spigelman, Z.; Cavacini, L.A.; Posner, M.R. Treatment of pemphigus vulgaris with rituximab and intravenous immune globulin. N. Engl. J. Med., 2006, 355(17), 1772-1779.
[http://dx.doi.org/10.1056/NEJMoa062930] [PMID: 17065638]
Amagai, M.; Hashimoto, T.; Shimizu, N.; Nishikawa, T. Absorption of pathogenic autoantibodies by the extracellular domain of pemphigus vulgaris antigen (Dsg3) produced by baculovirus. J. Clin. Invest., 1994, 94(1), 59-67.
[http://dx.doi.org/10.1172/JCI117349] [PMID: 8040292]
Chams-Davatchi, C.; Valikhani, M.; Daneshpazhooh, M.; Esmaili, N.; Balighi, K.; Hallaji, Z.; Barzegari, M.; Akhiani, M.; Ghodsi, Z.; Mortazavi, H.; Naraghi, Z. Pemphigus: analysis of 1209 cases. Int. J. Dermatol., 2005, 44(6), 470-476.
[http://dx.doi.org/10.1111/j.1365-4632.2004.02501.x] [PMID: 15941433]
Harman, K.E.; Albert, S.; Black, M.M. British Association of Dermatologists. Guidelines for the management of pemphigus vulgaris. Br. J. Dermatol., 2003, 149(5), 926-937.
[http://dx.doi.org/10.1111/j.1365-2133.2003.05665.x] [PMID: 14632796]
Martín, F.J.; Pérez-Bernal, A.M.; Camacho, F. Martيn FJ. Pemphigus vulgaris and disseminated nocardiosis. J. Eur. Acad. Dermatol. Venereol., 2000, 14(5), 416-418.
[http://dx.doi.org/10.1046/j.1468-3083.2000.00114.x] [PMID: 11305389]
Eichold, S.; Wright, R.D. Nocardia asteroides effectively treated with concurrent steroid management of pemphigus vulgaris. J. Med. Assoc. State Ala., 1959, 28(11), 333-334.
[PMID: 13655010]
Millar, B.C.; Jiru, X.; Moore, J.E.; Earle, J.A. A simple and sensitive method to extract bacterial, yeast and fungal DNA from blood culture material. J. Microbiol. Methods, 2000, 42(2), 139-147.
[http://dx.doi.org/10.1016/S0167-7012(00)00174-3] [PMID: 11018270]
NCCLS. Susceptibility testing of mycobacteria, Nocardia, and other aerobic actinomycetes; approved standard NCCLS document M24-A[ISBN 1-56238-500-3]. NCCLS, 940 West Valley Road, Suite 1400,Wayne, Pennsylvania 2003.
McTaggart, L.R.; Doucet, J.; Witkowska, M.; Richardson, S.E. Antimicrobial susceptibility among clinical Nocardia species identified by multilocus sequence analysis. Antimicrob. Agents Chemother., 2015, 59(1), 269-275.
[http://dx.doi.org/10.1128/AAC.02770-14] [PMID: 25348540]
Larruskain, J.; Idigoras, P. Marimَn JM, Pérez-Trallero E. Susceptibility study of 186 Nocardia spp. isolates to 20 antimicrobial agents. Antimicrob. Agents Chemother., 2011, 55(6), 2995-2998.
[http://dx.doi.org/10.1128/AAC.01279-10] [PMID: 21402847]
Rahdar, H.A.; Salehi, M.R.; Bahador, A.; Jasemi, S.; Karami-Zarandi, M.; Nejad, M.H.; Shahraki-Zahedani, S.; Amani, J.; Feyisa, S.G.; Kardan-Yamchi, J.; Feizabadi, M.M. Detection of Nocardia, Streptomyces and Rhodococcus from bronchoalveolar lavage specimens of patients with HIV by Multiplex PCR Assay. Ethiop. J. Health Sci., 2019, 29(6), 737-744.
[PMID: 31741644]
Minero, M.V.; Marín, M.; Cercenado, E.; Rabadán, P.M.; Bouza, E.; Muñoz, P. Nocardiosis at the turn of the century. Medicine (Baltimore), 2009, 88(4), 250-261.
[http://dx.doi.org/10.1097/MD.0b013e3181afa1c8] [PMID: 19593231]
MacIsaac, J.; Siddiqui, R.; Jamula, E.; Li, N.; Baker, S.; Webert, K.E.; Evanovitch, D.; Heddle, N.M.; Arnold, D.M. Systematic review of rituximab for autoimmune diseases: a potential alternative to intravenous immune globulin. Transfusion, 2018, 58(11), 2729-2735.
[http://dx.doi.org/10.1111/trf.14841] [PMID: 30244480]
Ali, A. AliReza Y, Gita F. Pemphigus vulgaris in Iran: epidemiology and clinical profile. Skinmed, 2006, 5(2), 69-71.
Esmaili, N.; Chams-Davatchi, C.; Valikhani, M.; Daneshpazhooh, M.; Balighi, K.; Hallaji, Z.; Barzegari, M.; Akhyani, M.; Ghodsi, Z.S.; Mrotazavi, H.; Naraghi, Z.S.; Toosi, S. Pemphigus vulgaris in Iran: a clinical study of 140 cases. Int. J. Dermatol., 2007, 46(11), 1166-1170.
[http://dx.doi.org/10.1111/j.1365-4632.2007.03334.x] [PMID: 17988336]
Lever, W.F.; Schaumburg-Lever, G. Immunosuppressants and prednisone in pemphigus vulgaris: therapeutic results obtained in 63 patients between 1961 and 1975. Arch. Dermatol., 1977, 113(9), 1236-1241.
[http://dx.doi.org/10.1001/archderm.1977.01640090084013] [PMID: 900969]
Ahmed, A.R.; Shetty, S. A comprehensive analysis of treatment outcomes in patients with pemphigus vulgaris treated with rituximab. Autoimmun. Rev., 2015, 14(4), 323-331.
[http://dx.doi.org/10.1016/j.autrev.2014.12.002] [PMID: 25499920]
Kandi, V. Human Nocardia infections: a review of pulmonary nocardiosis. Cureus, 2015, 7(8)e304
[http://dx.doi.org/10.7759/cureus.304] [PMID: 26430578]
Keikha, M. Comment on: Disseminated Nocardia cyriacigeorgia causing pancreatitis in a haploidentical stem cell transplant recipient. IDCases, 2017, 12, 169.
[http://dx.doi.org/10.1016/j.idcr.2017.08.013] [PMID: 29942782]
Keikha, M. Comment on a primary cutaneous nocardiosis of the hand. Open Access Maced. J. Med. Sci., 2018, 6(1), 226-227.
[http://dx.doi.org/10.3889/oamjms.2018.091] [PMID: 29484029]
Hashemi-Shahraki, A.; Bostanabad, S.Z.; Heidarieh, P.; Sheikhi, N.; Biranvand, M.; Alavi, S.M.; Titov, L.P.; Khosravi, A.D.; Nojoumi, S.A. Species spectrum of Nocardia spp. isolated from suspected tuberculosis patients. Health, 2015, 7(07), 847.
Rahdar, H.A.; Gharabaghi, M.A.; Bahador, A.; Shahraki-Zahedani, S.; Karami-Zarandi, M.; Mahmoudi, S.; Feizabadi, M.M. Pulmonary Nocardia ignorata Infection in Gardener, Iran, 2017. Emerg. Infect. Dis., 2020, 26(3), 610.
Miller, R.C.; Felman, Y.M. Pemphigus vulgaris and pulmonary nocardiosis. Arch. Dermatol., 1967, 96(5), 548-551.
[http://dx.doi.org/10.1001/archderm.1967.01610050070011] [PMID: 6054230]
Murdock, D.K.; Lookingbill, D.P. Immunosuppressive therapy of pemphigus vulgaris complicated by Nocardia pneumonia. Gold as an alternate therapy. Arch. Dermatol., 1990, 126(1), 27-28.
[http://dx.doi.org/10.1001/archderm.1990.01670250031003] [PMID: 2105086]
Asilian, A.; Yoosefi, A.; Faghihi, G. Cutaneous and pulmonary nocardiosis in pemphigus vulgaris: a rare complication of immunosuppressive therapy. Int. J. Dermatol., 2006, 45(10), 1204-1206.
[http://dx.doi.org/10.1111/j.1365-4632.2006.02738.x] [PMID: 17040442]
Fatahi-Bafghi, M.; Soori, T.; Heidarieh, P.; Rasouli-nasab, M.; Habibnia, Sh.; Eshraghi, S.S. Isolation and Phenotypic Identification of Nocardia nova Complex from Breast Abscess of a Patient with pemphigus vulgaris: The first case report from Iran. Iranian Journal of Breast Disease., 2012, 5(2), 44-49.
Wallace, R.J., Jr; Steele, L.C. Susceptibility testing of Nocardia species for the clinical laboratory. Diagn. Microbiol. Infect. Dis., 1988, 9(3), 155-166.
[http://dx.doi.org/10.1016/0732-8893(88)90025-9] [PMID: 3293892]
Woodworth, M.H.; Saullo, J.L.; Lantos, P.M.; Cox, G.M.; Stout, J.E. Increasing Nocardia incidence associated with bronchiectasis at a tertiary care center. Ann. Am. Thorac. Soc., 2017, 14(3), 347-354.
[http://dx.doi.org/10.1513/AnnalsATS.201611-907OC] [PMID: 28231023]
Keikha, M. Comment on “Extensive cutaneous botryomycosis with subsequent development of nocardia-positive wound cultures”. J. Cutan. Med. Surg., 2018, 22(4), 447.
[http://dx.doi.org/10.1177/1203475418771609] [PMID: 29927312]
Corti, M.E.; Villafañe-Fioti, M.F. Nocardiosis: a review. Int. J. Infect. Dis., 2003, 7(4), 243-250.
[http://dx.doi.org/10.1016/S1201-9712(03)90102-0] [PMID: 14656414]
Pintado, V.; Gómez-Mampaso, E.; Cobo, J.; Quereda, C.; Meseguer, M.A.; Fortún, J.; Navas, E.; Moreno, S. Nocardial infection in patients infected with the human immunodeficiency virus. Clin. Microbiol. Infect., 2003, 9(7), 716-720.
[http://dx.doi.org/10.1046/j.1469-0691.2003.00588.x] [PMID: 12925115]
Lebeaux, D.; Morelon, E.; Suarez, F.; Lanternier, F.; Scemla, A.; Frange, P.; Mainardi, J.L.; Lecuit, M.; Lortholary, O. Nocardiosis in transplant recipients. Eur. J. Clin. Microbiol. Infect. Dis., 2014, 33(5), 689-702.
[http://dx.doi.org/10.1007/s10096-013-2015-5] [PMID: 24272063]
Leshem, Y.A.; Gdalevich, M.; Ziv, M.; David, M.; Hodak, E.; Mimouni, D. Opportunistic infections in patients with pemphigus. J. Am. Acad. Dermatol., 2014, 71(2), 284-292.
[http://dx.doi.org/10.1016/j.jaad.2014.03.020] [PMID: 24815564]
Esmaili, N.; Mortazavi, H.; Noormohammadpour, P.; Boreiri, M.; Soori, T. Pemphigus vulgaris and infections: a retrospective study on 155 patients. Autoimmune Dis., 2013, 2013834295

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Year: 2021
Published on: 31 December, 2019
Page: [78 - 83]
Pages: 6
DOI: 10.2174/1871526520666191231144607
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