OBM Genetics is an international Open Access journal published quarterly online by LIDSEN Publishing Inc. It accepts papers addressing basic and medical aspects of genetics and epigenetics and also ethical, legal and social issues. Coverage includes clinical, developmental, diagnostic, evolutionary, genomic, mitochondrial, molecular, oncological, population and reproductive aspects. It publishes research articles, reviews, communications and technical notes, etc. There is no restriction on the length of the papers and we encourage scientists to publish their results in as much detail as possible.

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Open Access Review
Airborne Interindividual Transmission of Pneumocystis jirovecii

Laurence Pougnet 1, 2, *, Solène Le Gal 1, 3, Gilles Nevez 1, 3, *

1. Groupe d’Étude des Interactions Hôte-Pathogène (GEIHP), EA 3142, Angers-Brest, Université de Bretagne Loire, Brest, France

2. Laboratoire de biologie médicale, Hôpital d’Instruction des Armées Clermont-Tonnerre, CC41, 29240 Brest Cedex 9, France

3. Laboratoire de Mycologie et Parasitologie, CHRU de Brest, Brest, France

Correspondences: Gilles Nevez and Laurence Pougnet

Academic Editors: Andrés Moya, Enrique J. Calderón and Luis Delaye

Special Issue: Pneumocystis: A Model of Adaptive Coevolution

Received: December 17, 2018 | Accepted: May 15, 2019 | Published: May 22, 2019

OBM Genetics 2019, Volume 3, Issue 2, doi:10.21926/obm.genet.1902080

Recommended citation: Pougnet L, Le Gal S, Nevez G. Airborne Interindividual Transmission of Pneumocystis jirovecii. OBM Genetics 2019;3(2):15; doi:10.21926/obm.genet.1902080.

© 2019 by the authors. This is an open access article distributed under the conditions of the Creative Commons by Attribution License, which permits unrestricted use, distribution, and reproduction in any medium or format, provided the original work is correctly cited.

Abstract

Pneumocystis pneumonia (PCP) is the most frequent AIDS-defining disease among HIV-infected individuals in developed countries, and also affects immunocompromised non-HIV patients. Experimental studies on rodent models carried out in the early eighties have shown that Pneumocystis spp. can be transmitted via the airborne route. Unfortunately, this mode of acquisition and transmission has long been overlooked by physicians because PCP in immunosuppressed patients was considered to result from reactivation of a latent endogenous infection. This hypothesis was further investigated and, at present, PCP is considered to frequently result from the de novo acquisition of the fungus. This paradigm shift is correlated with the development of highly sensitive detection techniques and molecular characterization of Pneumocystis spp. in animal models and humans. This review article describes the milestones that have been achieved on the knowledge on the airborne interindividual transmission of Pneumocystis jirovecii.

Keywords

Pneumocystis jirovecii; hospital hygiene; airborne transmission; outbreaks; Pneumocystis pneumonia

1. Introduction

Pneumocystis jirovecii is an opportunistic, transmissible fungus that infects humans [1]. It causes severe pneumonia (Pneumocystis pneumonia or PCP) in immunocompromised patients. PCP is the most frequent AIDS-defining disease in developed countries and approximately 30% of the AIDS cases (1,200) in France were related to PCP during 2013 [2]. These data are consistent with the report on opportunistic infections in a multicohort analysis of 63,541 North-American HIV-infected patients between 2000 and 2010. During this period, PCP was the most frequent AIDS-defining disease. There were about 1,000 PCP cases per 100,000 person-years between 2000 and 2004 regardless of the immune status or antiretroviral therapy. This incidence decreased gradually to about 250 PCP cases per 100,000 person-years in 2010 [3]. PCP incidence in the world might have exceeded 400,000 cases per year in 2012 with more than 52,000 deaths per year [4]. Patients with other immune deficiencies also develop PCP. The patients who are receiving cytostatic and immunomodulatory treatments and those with solid organ transplants or with malignancies are at the highest risk [5]. The number of PCP cases in France is estimated to be 300 per year in HIV-infected patients and 600 per year in other immunocompromised patients [2,6]. The fatality rate of PCP in France increased from 5% to 15% between 2001 and 2010 [7]. Moreover, according to the national database of the Medicalization of Information Systems in Medicine, Surgery, and Obstetrics, the number of inpatient hospitalizations due to PCP increased by 60% between 2010 and 2017, from 526 to 846, mostly due to PCP in non-HIV patients [8]. Torpid P. jirovecii infections may occur in patients with chronic bronchial and pulmonary diseases, such as chronic obstructive pulmonary disease (COPD). Moreover, P. jirovecii infections have been linked to severe COPD [9]. Therefore, P. jirovecii infection is a public health issue.

Pneumocystis is an atypical fungus that cannot be routinely cultured, and therefore, animal models are to be used to study the transmission mode and pathogenicity. Moreover, animal models are worth investigating since the clinical presentation of PCP is similar in animals and in humans. The experimental studies on rodent models have shown that Pneumocystis spp. can be transmitted via the airborne route [10,11]. Despite these studies, this mode of acquisition and transmission has long been overlooked by physicians due to PCP infection in immunocompromised adult patients was believed to be mostly from endogenous latent P. jirovecii organisms that are carried within alveoli since childhood [12]. However, recent studies have indicated that PCP occurs due to de novo acquisition rather than reactivation of latent infection [12]. Host specificity of Pneumocystis spp. has led to the naming of different species in the genus according to the binominal system [13]. For instance, Pneumocystis carinii, Pneumocystis murina, and Pneumocystis jirovecii infects rats, mice, and humans, respectively [13]. Considering this host specificity, an animal reservoir for P. jirovecii was excluded.

In this context, our aim was to compile the latest available information on the epidemiology of Pneumocystis spp. established in rodent models and humans, specifically on the airborne interindividual transmission of the fungus and to provide a rationale for hygiene measures to prevent P. jirovecii transmission in hospitals.

2. Contribution of Rodent Models

The results of the main studies on Pneumocystis sp. airborne acquisition and/or transmission using rodent models are summarized (Table 1).

Airborne acquisition and transmission of P. carinii were established in the 1980s [11,14]. Later, Choukri and colleagues  described the kinetics of P. carinii exhalation by the immunocompromised rats developing PCP [15]. A correlation between lung fungal burdens of rats and air fungal burdens was highlighted during the first month of PCP development with a ratio of approximately 106:1. The kinetics of P. carinii exhalation in immunocompetent rats developing primary infection and reinfection was also investigated, which suggested that the immune response impacts the pulmonary fungal burden as well as P. carinii exhalation [16]. Further investigation on the relationship between P. carinii pulmonary burden and the immune status [17] suggested a correlation between the airborne acquisition of P. carinii and the level of immunosuppression.

Some experiments in mice [11,18,19] revealed that immunocompromised mice developing PCP can transmit P. murina via the airborne route to other susceptible immunosuppressed mice and to immunocompetent mice. Immunocompetent mice can be colonized by P. murina that can transmit P. murina to immunosuppressed susceptible mice as well as to other immunocompetent mice [18,19]. In order to identify the putative infectious stage of Pneumocystis sp., experiments were conducted with echinocandin-treated mice, and the findings showed that ascus is necessary for P. murina transmission [20]. A recent study on Pneumocystis life cycle suggested that the ascospores located in the asci could be the putative infectious stage [21].

In summary, both immunosuppressed rodents and immunocompetent rodents can acquire Pneumocystis sp. and exhale the fungus into the surrounding air. Nonetheless, the level of Pneumocystis sp. acquisition and exhalation seems to be correlated to the level of immunosuppression and the severity of the infection. The putative infectious stage may be the ascus or the ascospore.

Table 1 Main studies on Pneumocystis sp. airborne acquisition and/or transmission using rodent models.

3. Transmission of Pneumocystis jirovecii in Hospitals

PCP outbreaks occurring in hospitals over the past 60 years favor the hypothesis of interindividual transmission of P. jirovecii. Between 1968 and 2019, almost 60 outbreaks were described worldwide, mainly in renal transplant recipients as well as in HIV-infected and cancer patients [22–41]. Although interindividual transmission of P. jirovecii was suggested, it remained hypothetical until 1998 due to the absence of genotyping methods. Several other studies of outbreaks, which combined the concordance of P. jirovecii genotypes in index patients and susceptible patients with the analysis of patient encounters, supported the nosocomial acquisition and interindividual transmission of the fungus. In 2012, Le Gal and colleagues showed that both PCP patients and P. jirovecii colonized patients may be possible infectious sources of the fungus [23]. These results were confirmed by two other investigations on P. jirovecii outbreaks, one in renal transplant recipients and another in heart transplant recipients [29,32]. Interestingly, during the course of the latter outbreak, a P. jirovecii cytochrome b mutant was observed exclusively in the heart transplant recipients and not in the control patients; the mutation may provide putative resistance to atovaquone, an anti-infectious agent targeting the cytochrome b [28]. Outbreaks in liver transplant recipients have also been investigated, which provided additional information on the putative interindividual transmission of P. jirovecii [35,42].

The main findings on P. jirovecii exhalation from PCP patients and colonized patients into the surrounding air in hospitals are summarized in Table 2.

By the end of the 1990s, two important studies detected and identified P. jirovecii genotypes from patient rooms [43,44]. A perfect or partial similarity was observed in P. jirovecii genotypes of clinical and air samples. These results are consistent with the findings on P. jirovecii exhalation from PCP patients and the subsequent putative airborne transmission of P. jirovecii. Another study demonstrated P. jirovecii exhalation in an intubation system by a patient developing PCP and monitored in an Intensive Care Unit [49].

In 2010, P. jirovecii DNA was detected at 1, 5, and 8 m distance from PCP patients and P. jirovecii DNA burdens in air samples decreased with the distance of sampling [45]. A perfect or partial similarity was observed in P. jirovecii genotypes of clinical and air samples [46]. The spread of P. jirovecii from both PCP patients and colonized patients was investigated using the same method [47,48]. P. jirovecii burdens in the air samples from colonized patients appeared lower than those collected from the air surrounding PCP patients. This indicates that P. jirovecii can be exhaled and spread from both PCP patients and colonized patients. However, whether colonized patients represent infectious sources at the same level as PCP patients is still an open question considering the difference in pulmonary fungal burden [47,50]. The major findings of P. jirovecii genotyping clinical samples and air samples are summarized (Table 2).

Table 2 Main studies on Pneumocystis jirovecii genotyping in clinical and air samples.

4. Prevention of Pneumocystis jirovecii Transmission in Hospitals

High pulmonary tropism of P. jirovecii combined with the data on P. jirovecii exhalation from infected patients as well as the occurrence of clusters of PCP cases are consistent with the airborne acquisition in humans and emphasize the risk of patient-to-patient transmission through this mode. Chemoprophylaxis is essential to prevent P. jirovecii infection. However, the measures based on chemoprophylaxis alone may not be sufficient to ensure PCP prevention.

Measures to prevent healthcare-associated infections are usually classified as standard, droplet, or airborne. This classification is based on transmission mode, transmitted particle size, and microorganism infectivity over time and distance. Droplet precaution procedures consist of i) placing the patient in a single room, ii) use of surgical masks by health-care workers and visitors, iii) limiting patient movement out of the room, and iv) use of masks by patients when out of their rooms [51]. Airborne precaution procedures consist of i) placing the patient in a single room with doors closed or with special air treatment, ii) use of respirator masks (e.g., N95) by health-care workers, iii) limiting patient movement out of the room, and iv) use of masks by patients when out of their rooms [51].

Centers for Disease Control and Prevention recommend chemoprophylaxis for susceptible persons to prevent PCP [52]. It is also recommended to implement standard precautions and avoid placement of a PCP patient with an immunocompromised patient in the same room [51]. Considering the knowledge gained on Pneumocystis transmission over the past ten years, these recommendations should be updated. The transmissible stage of P. jirovecii is assumed to be the ascus or the ascospores [20,21]. Unfortunately, the median size of the ascus (5 µm) is precisely the threshold value for distinguishing droplet and air precaution measures. Moreover, whether Pneumocystis transmission occurs through Flügge droplets or because Pneumocystis aerosolizes itself through the ascospores remains unknown.

Nonetheless, the data pertaining to the transmission of Pneumocystis spp. in rodent models and humans are now sufficient to recommend preventive measures, either airborne or droplet. P. jirovecii detection in the surrounding air at 5 m (or even 8 m) distance [45,47] favors air precautions. However, air precautions are tough to implement. When the engineering resources are limited, preventing airborne transmission consists of placing a patient in a single room with doors closed and wearing respirator masks when in contact with the patient [51].

The application of droplet precautions was proposed in France in the late nineties [53,54]. However, these recommendations have been poorly applied and at least 10 clusters of PCP cases occurred in France over the past two decades [23,29,30,32,33,35,40,41,55,56]. Since the exhalation of P. jirovecii by infected patients can be observed beyond 1 m distance [45,47,48], airborne precautions may be more suitable.

Nonetheless, whichever precaution is implemented, no study has reported their duration. As an initial approach to address this issue, we investigated the longitudinal P. jirovecii air exhalation by a patient developing PCP and efficiently treated with cotrimoxazole [57]. Five air samples were collected after treatment initiation on five consecutive days in the patient's room at 1 m distance from the patient head. P. jirovecii DNA was detected in the five air samples. This study showed that PCP treatment dramatically decreased P. jirovecii exhalation, which suggests maintaining preventive measures, whatever they may be, for at least five days following PCP treatment initiation [57].

Further, precautions should be proposed to prevent P. jirovecii transmission from patients developing PCP who may be highly contagious. Whether precautionary measures should be implemented for colonized patients or healthcare workers who may have a role in the transmission chain remains a subject of debate [33,50,58]. Through In a different approach, the French Hygiene Society recommends that susceptible patients should wear a mask when encountering all other patients [59].

In conclusion, P. carinii and P. murina transmission via the airborne route has been clearly established in rodents, and P. jirovecii airborne transmission is highly probable in humans. Chemoprophylaxis is essential in susceptible patients; however, it may not be sufficient to completely prevent P. jirovecii infection. Measures must be implemented to prevent interindividual transmission of P. jirovecii specifically from PCP patients in hospitals who seem to be highly infectious. At present, there are strong arguments in favor of air precautions. However, considering the challenges in their implementation, at least droplet precautions must be implemented. Nonetheless, these measures are still subject to debate; therefore, an update through a consensus conference is recommended.

Author Contributions

The three authors contributed equally to this work.

Competing Interests

The authors have declared that no competing interests exist.

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