The Open Allergy Journal




(Discontinued)

ISSN: 1874-8384 ― Volume 11, 2020
RESEARCH ARTICLE

Chronic Obstructive Pulmonary Disease (COPD) and Asthma-Chronic Obstructive Pulmonary Disease Overlap Syndrome (ACOS) are Risk Factors for Cryptococcosis



Aline B. Mahler Pereira1, Alexandre P. Rogerio1, *
1 Departamento de Clínica Médica, Universidade Federal of Triângulo Mineiro, Laboratory of Experimental Immunopharmacology, Rua Manoel Carlos, Uberaba – MG, Brazil

Abstract

Cryptococcosis is a fungal infection of global importance affecting the central nervous system and other organs such as the lungs. The severity of cryptococcosis is largely dependent on the integrity of the host immune system. The protection to cryptococcosis is associated with Th1 immune response while Th2 results in susceptibility to Cryptococcus infection. Asthma is a chronic inflammatory disease commonly coordinated by Th2 immune response. The airway inflammation in Chronic Obstructive Pulmonary Disease (COPD) patients is characterized by increased neutrophils, macrophages, proteases, IL-6, IL-8, and Th1 cytokines. Asthma-Chronic Obstructive Pulmonary Disease Overlap Syndrome (ACOS) patients present phenotype that shares Th1 (COPD) and Th2 (asthma). There are several risk factors associated with Cryptococcus infection, including smoking, that cause airway remodeling and dysregulated and damaging airway inflammation.

Keywords: Cryptococcosis, Smoking, Inflammation, COPD, ACOS, Cryptococcus infection.

Article Information


Identifiers and Pagination:

Year: 2020
Volume: 11
First Page: 1
Last Page: 4
Publisher Id: TOALLJ-11-1
DOI: 10.2174/1874838402011010001

Article History:

Received Date: 08/10/2019
Revision Received Date: 26/03/2020
Acceptance Date: 12/04/2020
Electronic publication date: 04/06/2020
Collection year: 2020

© 2020 Pereira and Rogerio.

open-access license: This is an open access article distributed under the terms of the Creative Commons Attribution 4.0 International Public License (CC-BY 4.0), a copy of which is available at: https://creativecommons.org/licenses/by/4.0/legalcode. This license permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.


* Address correspondence to this author at the Departamento de Clínica Médica, Universidade Federal of Triângulo Mineiro, Laboratory of Experimental Immunopharmacology, Universidade Federal do Triângulo Mineiro, Rua Manoel Carlos, 162, 38025-380 – Uberaba – MG, Brazil; Phone: +55 34 3318 5814; E-mail: alexandre.rogerio@uftm.edu.br



1. CRYPTOCOCCOSIS IN THE LOWER RESPIRATORY SYSTEM

Cryptococcosis is an infection of global importance with cryptococcal meningoencephalitis being the most deadly symptom mainly in patients with Human Immunodeficiency Viruses (HIV) [1Beardsley J, Sorrell TC, Chen SC-A. Central nervous system cryptococcal infections in non-HIV infected patients. J Fungi (Basel) 2019; 5(3): E71.
[http://dx.doi.org/10.3390/jof5030071] [PMID: 31382367] ]. The genus Cryptococcus comprises over 30 yeast- like fungal species. However, the majority of human infections are caused by C. neoformans and C. gattii [2Negroni R. Cryptococcosis. Clin Dermatol 2012; 30(6): 599-609.
[http://dx.doi.org/10.1016/j.clindermatol.2012.01.005] [PMID: 23068147] ]. C. neoformans is commonly present in avian droppings while C. gattii is found mainly in decayed woods inside trunk hollows of diverse tree species. Both C. neoformans and C. gattii infections start with inhalation of the fungus in the airways. From the lungs, the fungus can spread to other organs of the body especially to the central nervous system [3Taylor-Smith LM, May RC. New weapons in the Cryptococcus infection toolkit. Curr Opin Microbiol 2016; 34: 67-74.
[http://dx.doi.org/10.1016/j.mib.2016.07.018] [PMID: 27522351] ]. C. neoformans and C. gattii have several virulence factors, especially the capsule that consists of high molecular weight polysaccharides, mainly glucuronoxylomannan (GXM) and, to a lesser extent, galactoxylomannan (GalXM) and mannoproteins (MP). Other virulence factors include melanin production, which protects the C. neoformans and C. gattii against phagocytosis, and the production of various enzymes such as proteases, ureases, superoxide dismutase and phospholipase B, which facilitates fungal invasion of tissues [4Chayakulkeeree M, Perfect JR. Cryptococcosis. Infect Dis Clin North Am 2006; 20(3): 507-544, v-vi. [v-vi.].
[http://dx.doi.org/10.1016/j.idc.2006.07.001] [PMID: 16984867] -7Andrade JCBN, Gatto M, Rodrigues DR, Soares ÂMVC, Calvi SA. Cryptococcus neoformans and gattii promote DNA damage in human peripheral blood mononuclear cells. Med Mycol 2018; 56(3): 344-49.
[PMID: 28633410] ]. The severity of cryptococcosis is largely dependent on the integrity of the host immune system and the characteristics of each variety of C. neoformans and C. gattii [8Wormley FL Jr, Perfect JR. Immunology of infection caused by Cryptococcus neoformans. Methods Mol Med 2005; 118: 193-8.
[http://dx.doi.org/10.1385/1-59259-943-5:193] [PMID: 15888944] ].

2. ASTHMA, COPD AND ACOS

Asthma is a chronic inflammatory disease common worldwide, which is coordinated by Th2 immune response. Of the numerous smoking-related disorders, the most common is chronic obstructive pulmonary disease (COPD) and the most deadly is lung cancer [9Houghton AM. Mechanistic links between COPD and lung cancer. Nat Rev Cancer 2013; 13(4): 233-45.
[http://dx.doi.org/10.1038/nrc3477] [PMID: 23467302] ]. COPD is characterized by chronic airway obstruction leading to a progressive and irreversible decline in lung function as a consequence of activation of airway inflammation with release of inflammatory mediators (IL-6, IL-8, and Th1 cytokines) and proteolytic enzymes (metalloproteinases), and continuous cells recruitment (neutrophils, macrophages and others). Of note, COPD patients can also present a Th2 phenotype with an increase of eosinophils in sputum and blood. The allergic phenotype in COPD patients has been associated with an increased risk of airways exacerbations [10Gibson JF, Johnston SA. Immunity to Cryptococcus neoformans and C. gattii during cryptococcosis. Fungal Genet Biol 2015; 78: 76-86.
[http://dx.doi.org/10.1016/j.fgb.2014.11.006] [PMID: 25498576] , 11Blanco JL, Garcia ME. Immune response to fungal infections. Vet Immunol Immunopathol 2008; 125(1-2): 47-70.
[http://dx.doi.org/10.1016/j.vetimm.2008.04.020] [PMID: 18565595] ]. In smokers with asthma, the sputum airway inflammation is often reported to be eosinophilic, neutrophilic or mixed granulocytic [12Slats A, Taube C. Asthma and chronic obstructive pulmonary disease overlap: Asthmatic chronic obstructive pulmonary disease or chronic obstructive asthma? Ther Adv Respir Dis 2016; 10(1): 57-71.
[http://dx.doi.org/10.1177/1753465815617082] [PMID: 26596632] -14Mackay AJ, Hurst JR. COPD exacerbations: Causes, prevention, and treatment. Med Clin North Am 2012; 96(4): 789-809.
[http://dx.doi.org/10.1016/j.mcna.2012.02.008] [PMID: 22793945] ]. However, it is possible to have no association between smoking and inflammatory phenotypes in asthma [15Hastie AT, Martinez FJ, Curtis JL, et al. Association of sputum and blood eosinophil concentrations with clinical measures of COPD severity: An analysis of the SPIROMICS cohort. Lancet Respir Med 2017; 5(12): 956-67.
[http://dx.doi.org/10.1016/S2213-2600(17)30432-0] [PMID: 29146301] ]. Asthma-chronic obstructive pulmonary disease overlap syndrome (ACOS) patients present a mixture of Th1 immune response (characteristic of COPD) and Th2 (characteristic of asthma) immune response [16Prince JE, Kheradmand F, Corry DB. 16. Immunologic lung disease. J Allergy Clin Immunol 2003; 111(2)(Suppl.): S613-23.
[http://dx.doi.org/10.1067/mai.2003.124] [PMID: 12592307] , 17Jamieson DB, Matsui EC, Belli A, et al. Effects of allergic phenotype on respiratory symptoms and exacerbations in patients with chronic obstructive pulmonary disease. Am J Respir Crit Care Med 2013; 188(2): 187-92.
[http://dx.doi.org/10.1164/rccm.201211-2103OC] [PMID: 23668455] ].

3. SMOKING AND CRYPTOCOCCOSIS

C. neoformans can cause infection in individuals with normal but preferentially immunocompromised hosts such as HIV-infected patients [18Chuang YM, Ho YC, Chang HT, Yu CJ, Yang PC, Hsueh PR. Disseminated cryptococcosis in HIV-uninfected patients. Eur J Clin Microbiol Infect Dis 2008; 27(4): 307-10.
[http://dx.doi.org/10.1007/s10096-007-0430-1] [PMID: 18157678] ]. On the other hand, C. gattii infection occurs mainly in healthy individuals [19Franco-Paredes C, Womack T, Bohlmeyer T, et al. Management of Cryptococcus gattii meningoencephalitis. Lancet Infect Dis 2015; 15(3): 348-55.
[http://dx.doi.org/10.1016/S1473-3099(14)70945-4] [PMID: 25467646] -23Barnes PJ. Cellular and molecular mechanisms of asthma and COPD. Clin Sci (Lond) 2017; 131(13): 1541-58.
[http://dx.doi.org/10.1042/CS20160487] [PMID: 28659395] ]. HIV-infected patients with the cryptococcal infection have shown increase of IL-6, IFN-γ, TNF-α and IL-8 production in the cerebrospinal fluid from survivors compared to nonsurvivors [24Siddiqui AA, Brouwer AE, Wuthiekanun V, et al. IFN-gamma at the site of infection determines rate of clearance of infection in cryptococcal meningitis. J Immunol 2005; 174(3): 1746-50.
[http://dx.doi.org/10.4049/jimmunol.174.3.1746] [PMID: 15661940] , 25Jarvis JN, Meintjes G, Bicanic T, et al. Cerebrospinal fluid cytokine profiles predict risk of early mortality and immune reconstitution inflammatory syndrome in HIV-associated cryptococcal meningitis. PLoS Pathog 2015; 11(4)e1004754
[http://dx.doi.org/10.1371/journal.ppat.1004754] [PMID: 25853653] ]. The protection to cryptococcosis is associated with Th1 immune response while Th2 results in susceptibility to infection [10Gibson JF, Johnston SA. Immunity to Cryptococcus neoformans and C. gattii during cryptococcosis. Fungal Genet Biol 2015; 78: 76-86.
[http://dx.doi.org/10.1016/j.fgb.2014.11.006] [PMID: 25498576] , 11Blanco JL, Garcia ME. Immune response to fungal infections. Vet Immunol Immunopathol 2008; 125(1-2): 47-70.
[http://dx.doi.org/10.1016/j.vetimm.2008.04.020] [PMID: 18565595] ]. Studies on asthmatics demonstrated controversial results, while the IgA reactivity to C. neoformans in the Bronchoalveolar Lavage Fluid (BALF) was found to be greater in asthmatic children compared with non-asthmatic children [26Goldman DL, Li X, Tsirilakis K, Andrade C, Casadevall A, Vicencio AG. Increased chitinase expression and fungal-specific antibodies in the bronchoalveolar lavage fluid of asthmatic children. Clin Exp Allergy 2012; 42(4): 523-30.
[http://dx.doi.org/10.1111/j.1365-2222.2011.03886.x] [PMID: 22092749] ]. In non-asthmatic and asthmatic adults, no significant alteration was observed in IgG seroreactivity against C. neoformans [27Grahnert A, Müller U, von Buttlar H, Treudler R, Alber G. Analysis of asthma patients for cryptococcal seroreactivity in an urban German area. Med Mycol 2015; 53(6): 576-86.
[http://dx.doi.org/10.1093/mmy/myv024] [PMID: 26026172] ]. More studies are needed to demonstrate the susceptibility to cryptococcosis asthma patients. There are several factors associated with C. neoformans and C. gattii infections such as rheumatic disorders, malignancy, diabetes mellitus, cirrhosis, hepatitis B virus infection as well as smoking [1Beardsley J, Sorrell TC, Chen SC-A. Central nervous system cryptococcal infections in non-HIV infected patients. J Fungi (Basel) 2019; 5(3): E71.
[http://dx.doi.org/10.3390/jof5030071] [PMID: 31382367] , 28Barnes PJ. Inflammatory mechanisms in patients with chronic obstructive pulmonary disease. J Allergy Clin Immunol 2016; 138(1): 16-27.
[http://dx.doi.org/10.1016/j.jaci.2016.05.011] [PMID: 27373322] , 29Drannik AG, Pouladi MA, Robbins CS, Goncharova SI, Kianpour S, Stämpfli MR. Impact of cigarette smoke on clearance and inflammation after Pseudomonas aeruginosa infection. Am J Respir Crit Care Med 2004; 170(11): 1164-71.
[http://dx.doi.org/10.1164/rccm.200311-1521OC] [PMID: 15317669] ]. HIV-infected patients who were current smokers demonstrated an increased risk for C. neoformans infection [30Khan ZU. Smoking, melanization, and cryptococcosis: Is there a connection? J Clin Microbiol 2006; 44(3): 1207.
[http://dx.doi.org/10.1128/JCM.44.3.1207.2006] [PMID: 16517935] , 31Olson PE, Earhart KC, Rossetti RJ, Newton JA, Wallace MR. Smoking and risk of cryptococcosis in patients with AIDS. JAMA 1997; 277(8): 629-30.
[http://dx.doi.org/10.1001/jama.1997.03540320031029] [PMID: 9039878] ]. In another study, MacDougall et al. [32MacDougall L, Fyfe M, Romney M, Starr M, Galanis E. Risk factors for Cryptococcus gattii infection, British Columbia, Canada. Emerg Infect Dis 2011; 17(2): 193-9.
[http://dx.doi.org/10.3201/eid1702.101020] [PMID: 21291588] ] observed an increase of C. gattii infection in smokers with an immunosuppressive state, induced by oral corticosteroid use or with invasive cancers. Nicotine, a component identified in cigarette tobacco smoke, demonstrated immunosuppressive effects and could be associated with an increase of susceptibility to cryptococcal infections [22Mehta H, Nazzal K, Sadikot RT. Cigarette smoking and innate immunity. Inflamm Res 2008; 57(11): 497-503.
[http://dx.doi.org/10.1007/s00011-008-8078-6] [PMID: 19109742] ]. Additionally, tobacco contains a large number of chemicals and the consequent absorption of these compounds directly into the lungs or bloodstream, during smoking, could serve as precursors for the synthesis of several substances including melanin [28Barnes PJ. Inflammatory mechanisms in patients with chronic obstructive pulmonary disease. J Allergy Clin Immunol 2016; 138(1): 16-27.
[http://dx.doi.org/10.1016/j.jaci.2016.05.011] [PMID: 27373322] , 33Pryor WA, Stone K, Zang LY, Bermúdez E. Fractionation of aqueous cigarette tar extracts: Fractions that contain the tar radical cause DNA damage. Chem Res Toxicol 1998; 11(5): 441-8.
[http://dx.doi.org/10.1021/tx970159y] [PMID: 9585474] ]. Melanization of C. neoformans is associated with more virulent, increased resistance to host defenses [34] and reduced susceptibility to antifungal agents [35van Duin D, Casadevall A, Nosanchuk JD. Melanization of Cryptococcus neoformans and Histoplasma capsulatum reduces their susceptibilities to amphotericin B and caspofungin. Antimicrob Agents Chemother 2002; 46(11): 3394-400.
[http://dx.doi.org/10.1128/AAC.46.11.3394-3400.2002] [PMID: 12384341] ]. Taken together, the increased susceptibility to C. neoformans and C. gattii infections induced by smoking could be associated to its effects on the respiratory system (impairments of the protective barriers, inhibition of mucociliary clearance, airway remodeling, excessive and continuous airway inflammation and destruction of the lung parenchyma) [36Hajjeh RA, Conn LA, Stephens DS, et al. Cryptococcosis: Population-based multistate active surveillance and risk factors in human immunodeficiency virus-infected persons. J Infect Dis 1999; 179(2): 449-54.
[http://dx.doi.org/10.1086/314606] [PMID: 9878030] , 37Boelaert JR, Blasi E. Cryptococcosis and smoking: The potential role of iron. J Infect Dis 1999; 180(4): 1412-3.
[http://dx.doi.org/10.1086/315045] [PMID: 10479189] ]. Besides, smoking can provide substances with immunosuppressive effects or with the potential to melanize fungus cells, thus increasing the virulence and burden of fungus in the airways and consequently in other tissues such as the central nervous system (Fig. 1).

Fig. (1)
Smoking can increase susceptibility to C. neoformans and C. gattii infections in COPD and ACOS patients as a consequence of its effect on the airway inflammation and the fungus.


CONCLUSION

Smoking weakens pulmonary function and provides substances associated with fungal resistance mechanisms that can contribute towards the enhanced risk of cryptococcosis in smokers or ex-smokers mainly those individuals with COPD and ACOS.

AUTHORS' CONTRIBUTIONS

All authors contributed to critiquing the manuscript. All authors have read and approved the final manuscript.

CONFLICT OF INTEREST

The authors declare that there is no conflict of interest, financial or otherwise.

ACKNOWLEDGEMENTS

Declared none.

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Debomoy K. Lahiri
(Indiana University School of Medicine, USA)

"Open access journals represent a major break-through in publishing. They provide easy access to the latest research on a wide variety of issues. Relevant and timely articles are made available in a fraction of the time taken by more conventional publishers. Articles are of uniformly high quality and written by the world's leading authorities."


Robert Looney
(Naval Postgraduate School, USA)

"Open access journals have transformed the way scientific data is published and disseminated: particularly, whilst ensuring a high quality standard and transparency in the editorial process, they have increased the access to the scientific literature by those researchers that have limited library support or that are working on small budgets."


Richard Reithinger
(Westat, USA)

"Not only do open access journals greatly improve the access to high quality information for scientists in the developing world, it also provides extra exposure for our papers."


J. Ferwerda
(University of Oxford, UK)

"Open Access 'Chemistry' Journals allow the dissemination of knowledge at your finger tips without paying for the scientific content."


Sean L. Kitson
(Almac Sciences, Northern Ireland)

"In principle, all scientific journals should have open access, as should be science itself. Open access journals are very helpful for students, researchers and the general public including people from institutions which do not have library or cannot afford to subscribe scientific journals. The articles are high standard and cover a wide area."


Hubert Wolterbeek
(Delft University of Technology, The Netherlands)

"The widest possible diffusion of information is critical for the advancement of science. In this perspective, open access journals are instrumental in fostering researches and achievements."


Alessandro Laviano
(Sapienza - University of Rome, Italy)

"Open access journals are very useful for all scientists as they can have quick information in the different fields of science."


Philippe Hernigou
(Paris University, France)

"There are many scientists who can not afford the rather expensive subscriptions to scientific journals. Open access journals offer a good alternative for free access to good quality scientific information."


Fidel Toldrá
(Instituto de Agroquimica y Tecnologia de Alimentos, Spain)

"Open access journals have become a fundamental tool for students, researchers, patients and the general public. Many people from institutions which do not have library or cannot afford to subscribe scientific journals benefit of them on a daily basis. The articles are among the best and cover most scientific areas."


M. Bendandi
(University Clinic of Navarre, Spain)

"These journals provide researchers with a platform for rapid, open access scientific communication. The articles are of high quality and broad scope."


Peter Chiba
(University of Vienna, Austria)

"Open access journals are probably one of the most important contributions to promote and diffuse science worldwide."


Jaime Sampaio
(University of Trás-os-Montes e Alto Douro, Portugal)

"Open access journals make up a new and rather revolutionary way to scientific publication. This option opens several quite interesting possibilities to disseminate openly and freely new knowledge and even to facilitate interpersonal communication among scientists."


Eduardo A. Castro
(INIFTA, Argentina)

"Open access journals are freely available online throughout the world, for you to read, download, copy, distribute, and use. The articles published in the open access journals are high quality and cover a wide range of fields."


Kenji Hashimoto
(Chiba University, Japan)

"Open Access journals offer an innovative and efficient way of publication for academics and professionals in a wide range of disciplines. The papers published are of high quality after rigorous peer review and they are Indexed in: major international databases. I read Open Access journals to keep abreast of the recent development in my field of study."


Daniel Shek
(Chinese University of Hong Kong, Hong Kong)

"It is a modern trend for publishers to establish open access journals. Researchers, faculty members, and students will be greatly benefited by the new journals of Bentham Science Publishers Ltd. in this category."


Jih Ru Hwu
(National Central University, Taiwan)

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