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Invasive fungal infections after natural disasters.

The potential for adverse health events after natural disasters is well recognized and comprises various challenges for public health (1). The World Health Organization defines a disaster as a disruption of society resulting in widespread human, material, or environmental loss that exceeds the affected society's ability to cope by using local resources (2). Natural disasters can be broadly classified into 3 groups: geophysical (e.g., earthquakes, volcanic eruptions, and tsunamis), hydrometeorological (e.g., floods, hurricanes, and tornadoes), and geomorphological (e.g., landslides and avalanches). Specific social, economic, and cultural settings create a unique set of circumstances for every disaster, and the immediate causes of illness and death (such as blunt trauma, lacerations, crush injuries, suffocation, and drowning) vary according to the type of event (1).

Infectious disease outbreaks after natural disasters are uncommon. However, features of the post-impact and recovery phases of disasters, such as population displacement, low vaccine coverage for vaccine-preventable diseases, inadequate sanitation and hygiene infrastructure, and limited access to health care services, can interact to increase the risk for transmission of infectious diseases that were previously established in the affected area (3). Disaster-associated fungal infections are similarly uncommon, but they are becoming increasingly recognized and are typically attributable to the impact phase of a disaster because such infections primarily result from inhalation or cutaneous inoculation of fungal spores directly from the environment (3,4). During a disaster, pathogenic fungi can be displaced from their natural habitats, which could increase their environmental concentration or introduce them to areas where they would not normally be found, resulting in contact with injured persons and potentially causing fungal infections. To increase awareness of these events among health care providers and public health officials, we summarize the known occurrences of fungal infections associated with natural disasters (Table).

Search Strategy and Selection Criteria

The online literature databases PubMed and Google Scholar were searched for English-language articles about fungal infections related to natural disasters that were published as of April 2013. Search terms included combinations of "disaster," "natural disaster," "tornado," "hurricane," "earthquake," "tsunami," and "flood" with "fungal infection," "fungal disease," "fungus," or "mold." References cited in relevant articles were also reviewed, and the authors' personal records were searched for conference abstracts.

Pathogenic Fungi and the Environment

Of the 1.5 million species of fungi on Earth, [approximately equal to] 300 are known human pathogens (20). Pathogenic fungi exist in a broad range of natural habitats but are believed to be more common in subtropical and tropical areas of the world, probably because of environmental restrictions on their growth or propagation (20). Known geographic habitats of some pathogenic fungi (for example, Blastomyces, Coccidioides, and Histoplasma) are well defined, but others (such as Aspergillus and other molds) are thought to be ubiquitous. The abundance and distribution (and therefore, potential to cause disease) of environmental fungi probably depend on climatic or environmental factors such as ambient temperature and moisture (20). Examples include coccidioidomycosis incidence in Arizona, which has been shown to correlate with hot, dry conditions; blastomycosis clusters observed in association with rainfall after periods of decreased precipitation; and incidence of Penicillum marneffei penicilliosis, an opportunistic infection which is endemic to Southeast Asia and increases in incidence during rainy months (21,22). Aspergillosis and other invasive mold infections have also been postulated to correlate with seasons or weather patterns in some geographic areas (23).

Although seasonal changes and weather effects probably play a role in the growth and distribution of many pathogenic fungi, environmental disruption is a key factor in the dispersal of these organisms and their resulting potential for causing infection. Both small-scale earth-disrupting activities, such as excavation or construction, and events affecting larger areas, such as earthquakes (16), tsunamis (5-7,10-15,24,25), and tornadoes (4), have been linked to the occurrence of fungal infections. Natural disasters can cause large-scale disruption of fungal habitats, which can lead to clusters of respiratory, cutaneous, or other forms of fungal disease.

Studies of clinical specimens collected from persons injured during disasters highlight the diversity of potential fungal pathogens in the natural environment. For example, after an 8.0-magnitude earthquake in Wenchuan, China, during 2008, 19 strains of fungi were identified in wound, sputum, and blood cultures from 123 injured persons (26), and fungi accounted for 7.6% of clinical isolates obtained from 42 patients with crush syndrome (27). Similarly, after a 1970 tornado in Texas, United States, fungi were identified in 8 (6.5%) of 124 wound isolates from 24 hospitalized patients (Fusarium, unspecified yeast, Rhodotorula, Aspergillus, Hormodendrum [now Cladosporium], and Cephalosporium), and in 4 (10.5%) of 38 wound isolates from 23 ambulatory patients (28). In each of these reports, multiple organisms were isolated from many of the patients, and the fungi recovered may not necessarily have been agents of infection.

Respiratory Fungal Infections after Disasters

Airborne

Inhalation is a common route for fungal infections. Fungi are known to cause respiratory infections ranging from asymptomatic to life-threatening, depending on the pathogen and host characteristics. Coccidioides spp. are dimorphic fungi that grow in semiarid soil and are endemic to the southwestern United States, northern Mexico, and parts of South America. Two instances of disaster-associated coccidioidomycosis have been described.

An outbreak of coccidioidomycosis after the January 1994 earthquake in Northridge, California, United States, was 1 of few known examples of any infectious disease outbreak directly related to a geophysical disaster (3). Coccidioides spores were presumably aerosolized as a consequence of the earthquake, its aftershocks, and associated landslides and were dispersed by the resulting widespread dust clouds (16). In Ventura County, California, 203 outbreak-associated coccidioidomycosis cases were identified, and investigators found that dust exposure was substantially associated with acute illness (16). Fungal infection may not have been considered in the initial diagnoses in this outbreak; 93% of case-patients received [greater than or equal to] 1 antibacterial drug before coccidioidomycosis was diagnosed (16).

Another coccidioidomycosis outbreak occurred after a severe dust storm in the southern San Joaquin Valley of California in December 1977 (18). The storm originated near Bakersfield, an area to which coccidioidomycosis is highly endemic, and covered nearly 90,000 [km.sup.2], an area larger than the state of Maine (18). In Sacramento County, an area to which the disease was not previously considered to be endemic, 115 cases of coccidioidomycosis were attributed to the dust storm, including 16 cases of disseminated disease (18). Eighteen additional cases were identified at a US Navy air station in Kings County (19), and other California counties affected by the storm saw more coccidioidomycosis cases than usual; for example, Kern County recorded 134 cases during January and February 1978, compared with 17 cases during those months in the previous year (29).

Near-drowning

Drowning and near-drowning are common during and after disaster-related flooding (1). Aspiration of contaminated or debris-laden water can lead to sinus and pulmonary infections; aspiration pneumonia is often referred to as "tsunami lung" in post-tsunami settings (16,24). Tsunami lung can be caused by bacteria, fungi, or both. Pseudallescheria boydii (asexual form, Scedosporium apiospermum) is hypothesized to be the most common fungal pathogen associated with near-drowning, although this finding has not been studied specifically in the context of disasters (30). Information about post-disaster Scedosporium lung infection is limited to a small number of case reports; these reports also document the organism's propensity to progress to central nervous system infection, even in immunocompetent hosts (6,11). Other fungal pathogens, such as Aspergillus, have also been implicated as agents of tsunami lung; after the 2011 Great East Japan Earthquake and subsequent tsunami, a previously healthy near-drowning victim who later died was found to have pneumonia caused by Aspergillus fumigatus and evidence of multiorgan disseminated aspergillosis upon autopsy (5). The report describes delays in specimen transportation and receipt of culture results caused by the aftermath of the earthquake, which led to a delay in diagnosis and treatment (5).

Evidence of tsunami lung also was also apparent after the December 2004 earthquake and tsunami in the Indian Ocean, which killed >200,000 persons (3). In Sri Lanka, acute respiratory issues attributed to post-aspiration pneumonitis and polymicrobial pneumonia that were not related to communicable illnesses were the most frequent medical problems after this disaster (31). In Banda Aceh, Indonesia, several patients with necrotizing pneumonia, who did not respond to broad-spectrum antibacterial drugs, probably had polymicrobial infections that may have included fungal organisms (24). However, limited diagnostic capacity for fungi may have affected the ability to identify the potential role of fungi in these infections. A report from Germany demonstrated that among a cohort of 17 tourists injured during the tsunami, all had clinical and radiologic evidence of aspiration pneumonitis and pneumonia; Candida albicans and A. fumigatus were isolated from the respiratory tract of several patients, although it is unclear whether the isolation of these organisms represented true infection or colonization (15).

Soft Tissue Fungal Infections after Disasters

The risk for wound infections after a natural disaster is high when wounds are contaminated with water, soil, or debris (32). In addition, damage to the local health care infrastructure can compromise the ability to properly irrigate contaminated wounds with sterile solution or promptly treat injured persons with topical or systemic antimicrobial drugs (32). These factors can result in severe, often poly-microbial, infections of otherwise relatively minor injuries (32). Although most documented disaster-associated soft tissue infections are bacterial (typically gram-negative pathogens such as Aeromonas, Escherichia coli, and Klebsiella) (33), fungal wound infections can also occur, and they could be under-recognized because they can be clinically similar to bacterial infections, particularly during the early stages of infection.

Mucormycosis, caused by fungi that belong to the order Mucorales, is perhaps the most recognized example of post-disaster fungal soft tissue infection. Necrotizing fasciitis can result, and case-fatality rates of [approximately equal to] 30% are frequently described, although early diagnosis and treatment has been shown to lead to better outcomes (34). The first documented instance of disaster-associated mucormycosis occurred after the 1985 volcanic eruption in Armero, Colombia, which caused an estimated 23,000 deaths and [approximately equal to] 4,500 injuries (17). According to a report of 38 patients with necrotizing lesions who were hospitalized after the volcano, 8 patients had infections caused by the mucormycete Rhizopus arrhizus (oryzae) (17).

Similarly, a cluster of mucormycosis cases caused by Apophysomyces trapeziformis occurred among 13 persons who were severely injured in the May 22, 2011, tornado in Joplin, Missouri, United States (4). Penetrating trauma and an increased number of wounds were shown to be independent risk factors for mucormycosis. Whole-genome sequencing of A. trapeziformis isolates from case-patients' wounds (Figure) showed 4 nonidentical but closely related strains of A. trapeziformis. This finding, considered with case-patients' receipt of medical care at different hospitals, suggested that the infections were acquired from the natural environment as a result of exposure to organic matter and water, which are likely reservoirs for mucormycetes (4).

In addition to the 2 clusters described, several isolated cases of post-disaster soft tissue mucormycosis have been reported, notably among persons injured during the 2004 Indian Ocean tsunami (13-15). These reports illustrate some of the clinical challenges associated with soft tissue mucormycosis, caused by organisms that may initially appear indistinguishable from other types of wound infections but require aggressive treatment with intravenous antifungal medication and surgical debridement (13,14).

Other agents of fungal soft tissue infections in survivors injured during the 2004 Indian Ocean tsunami include Fusarium (which later caused systemic infection) in 1 tourist (15) and Cladophialophora bantiana in 2 other tourists (10). Subcutaneous C. bantiana infection has also been associated with a tornado-associated injury in which the patient was inoculated by a contaminated wood splinter but did not have symptoms until [approximately equal to] 16 years later (35). Soft tissue fungal infections have also been documented among persons who were not directly injured during a disaster but who sustained minor trauma while performing post-disaster tasks: in Texas after Hurricane Ike in 2008, chromoblastomycosis was diagnosed in 3 patients, all of whom had histories of cancer and all of whom described clearing brush and fallen trees near their homes after the storm (8).

Health Care-associated Fungal Infections after Disasters

Although respiratory and cutaneous infections are the most commonly described forms of fungal infection after natural disasters, other, more invasive fungal infections have also been observed. An outbreak of Aspergillus meningitis after the 2004 Indian Ocean tsunami was associated with the use of spinal anesthesia for cesarean section infant delivery for 6 previously healthy women in Sri Lanka (12). The first 5 case-patients were initially treated for bacterial meningitis, but the discovery of Aspergillus during the post-mortem examination of the index casepatient led to the use of amphotericin B and voriconazole in the surviving case-patients (12). Investigation of various medical supplies revealed that syringes from a central storage facility were contaminated with A. fumigatus, probably as a result of suboptimal storage conditions in a humid warehouse (12).

Indoor Mold Exposures after Disasters

Disaster-induced water damage to structures can create moist environments that can promote indoor fungal growth, but the extent to which damp indoor spaces and mold growth affect human health remains somewhat ambiguous (36). A 2004 report by the Institute of Medicine found sufficient evidence of association between indoor mold exposure and upper respiratory tract symptoms, cough, and wheezing, and evidence of an association between indoor mold exposure and some noninfectious health conditions that included asthma symptoms in persons with asthma and hypersensitivity pneumonitis in some groups of people (36). Although the report found no association between indoor mold exposure and invasive infection in healthy persons, there was evidence to support a link between exposure to Aspergillus and aspergillosis in severely immunocompromised persons (36).

Few data clearly demonstrate that indoor mold exposures increase the risk for invasive infection in post-disaster settings. Flooding lasted for weeks after Hurricanes Katrina and Rita made landfall on the US Gulf Coast in August and September 2005, respectively, leading to visible mold growth in 46% of 112 inspected homes (37). Despite these high levels of indoor mold growth documented in some areas, 1 study showed no elevated risk for fungal infections among immunocompromised patients exposed to water-damaged buildings after Hurricane Katrina; 1 patient, 1.2% of the profoundly immunocompromised study population, had a mold infection (caused by a Cladosporium sp.), which resolved without antifungal treatment (9). Colonization in the absence of related clinical symptoms was observed in persons who returned to their water-damaged homes after Hurricanes Rita and Katrina: the mucormycete Syncephalastrum was detected in various clinical specimens from 8 persons whose self-reported exposures to mold ranged from none to heavy, but none had evidence of invasive infection (38).

After the 2011 Great East Japan Earthquake and subsequent tsunami, a medical relief team observed unexplained chronic cough among a group of previously healthy persons living in a temporary refuge (25). Fungal cultures of sputum samples from 6 persons yielded Aspergillus fumigatus, A. flavus, and basidiomycetous fungi; culture plates exposed inside the refuge showed a similar fungal profile, suggesting that the indoor environment may have played a role in the patients' infections (25). Although the authors of that report state that the patients' coughs resolved after treatment with the antifungal itraconazole, the extent to which an infectious process was responsible for the illnesses is unclear (25).

Disasters, Fungi, and Global Climate Change

Climate change could be affecting the ecology of pathogenic fungi in ways that are not yet fully understood; even minor or gradual changes in temperature, moisture, and wind patterns might affect fungal growth, distribution, and dispersal (20). For example, warmer average global temperatures may allow the geographic range of fungi typically restricted to tropical and subtropical environments, such as Cryptococcus gattii, to expand into areas that are currently more temperate (20). Global warming has also been hypothesized to select for fungi with tolerance to warmer temperatures (20). The relative scarcity of fungal diseases among mammals has been hypothesized to be associated with the inability of many fungal species to survive at temperatures >37[degrees]C; however, warmer ambient temperatures may enable nonpathogenic fungi to acquire the ability to infect warm-blooded hosts (20).

Huppert and Sparks suggest that global climate change is contributing to greater frequency and severity of extreme weather events and that current patterns of population growth, urbanization, and human activity create conditions that render many communities increasingly vulnerable to these hazards (39). Coupled with an increased risk for natural disasters, a larger or more geographically widespread ecologic burden of pathogenic fungi could lead to greater numbers of disaster-associated fungal infections through any of several mechanisms: inhalation of spores dispersed as a result of geophysical disruption, traumatic implantation of fungi into wounds contaminated with organic matter, or infection associated with suboptimal medical care where the local health care system has been damaged or destroyed. Altogether, a combination of factors including genetic and biological aspects of host-pathogen interactions; changing features of the physical environment; and social, political, or economic influences could lead to the emergence of new fungal pathogens or increased numbers of infections by known pathogens (40).

Conclusions

Disasters are complex events that can result in a wide range of health effects, although infectious disease outbreaks as an immediate consequence of disasters are uncommon. Health care providers should be aware of the possibility for cases or clusters of community-acquired or health care-associated fungal infections among disaster survivors because these infections often appear clinically similar to bacterial infections and can be associated with serious illness and death. These infections can occur in persons who do not have the typical immunocompromising risk factors for fungal infection but who have experienced near-drowning, trauma, or other unusual exposure to the environment, such as a dust storm. A fungal infection should be considered early if a patient has a persistent or progressive infection that is not responding to initial antibacterial treatment, particularly because rapid diagnosis and administration of appropriate antifungal therapy can improve patient outcomes. Prompt restoration of disaster-affected aspects of the local health care infrastructure may help facilitate earlier diagnosis and treatment and possibly reduce the risk for infection associated with the use of contaminated medical equipment or substandard care. Strategies to reduce disaster-associated fungal infections should be considered within the broader context of comprehensive and sustainable risk reduction methods to prevent disaster-related injury and illness.

CME Questions

1. You are responding to provide medical care in a location that was devastated by an earthquake and subsequent tsunami 2 days ago. What should you consider regarding fungal infections in this situation?

A. Most fungi are human pathogens

B. Disasters pose a higher risk for fungal infections, but smaller activities such as excavations do not

C. Coccidioides spp. are endemic to the southwestern United States

D. Most cases of coccidioidomycosis are promptly identified and treated appropriately

2. You treat multiple individuals who had prolonged exposure to water and nearly drowned. Which of the following statements regarding waterborne fungal infections is most accurate?

A. "Tsunami lung" refers specifically to fungal infections

B. Pseudallescheria boydii is thought to be the most common fungal pathogen associated with near-drowning

C. After the 2004 Indian Ocean tsunami, most acute respiratory illness was the result of influenza, not fungal infections

D. Aspergillus spp. generally have no role in post-disaster infections

3. What should you consider regarding soft tissue infections after a natural disaster?

A. Most soft tissue infections after disasters are the result of fungi

B. Fungal soft tissue infections generally appear similar to bacterial infections at the initial presentation

C. Mucormycosis results in death in fewer than 3% of cases

D. Surgical debridement is usually contraindicated in cases of mucormycosis

4. Two weeks after the disaster, a number of patients are concerned about mold growing in their shelter. What can you tell them?

A. Indoor mold exposure can lead to cough and wheeze

B. Mold exposure frequently leads to infection, even among immunocompetent hosts

C. Hurricane Katrina was associated with high rates of mold infection among immunocompromised individuals

D. Molds generally result in invasive infection but not colonization

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DOI:http://dx.doi.org/10.3201/eid2003.131230

Release date: February 13, 2014; Expiration date: February 13, 2015

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(27.) Wang T, Li D, Xie Y, Kang M, Chen Z, Chen H, et al. The microbiological characteristics of patients with crush syndrome after the Wenchuan earthquake. Scand J Infect Dis. 2010;42:479-83. http://dx.doi.org/10.3109/00365541003671226

(28.) Gilbert DN, Sanford JP, Kutscher E, Sanders CV Jr, Luby JP, Barnett JA. Microbiologic study of wound infections in tornado casualties. Arch Environ Health. 1973;26:125-30. http://dx.doi.org/10.1080/00039896.1973.10666239

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(32.) Ivers LC, Ryan ET. Infectious diseases of severe weather-related and flood-related natural disasters. Curr Opin Infect Dis. 2006;19:408-14. http://dx.doi.org/10.1097/01qco.0000244044. 85393.9e

(33.) Hiransuthikul N, Tantisiriwat W, Lertutsahakul K, Vibhagool A, Boonma P. Skin and soft-tissue infections among tsunami survivors in southern Thailand. Clin Infect Dis. 2005;41:e93-6. http://dx.doi.org/10.1086/497372

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Learning Objectives

Upon completion of this activity, participants will be able to:

* Analyze the risk for fungal infections after natural disasters, including coccidioidomycosis

* Distinguish features of water-related fungal infections after natural disasters

* Assess the prevalence and microbiological characteristics of soft tissue fungal infections after natural disasters

* Evaluate the health risks associated with exposure to mold after natural disasters.

CME Editor

Jean Michaels Jones, Technical Writer/Editor, Emerging Infectious Diseases. Disclosure: Jean Michaels Jones has disclosed no relevant financial relationships.

CME Author

Charles P. Vega, MD, Health Sciences Clinical Professor; Residency Director, Department of Family Medicine, University of California, Irvine. Disclosure: Charles P. Vega, MD, has disclosed no relevant financial relationships.

Authors

Disclosures: Kaitlin Benedict, MPH, and Benjamin J. Park, MD, have disclosed no relevant financial relationships.

Author affiliation: Centers for Disease Control and Prevention, Atlanta, Georgia, USA

Ms Benedict is an epidemiologist in the Mycotic Diseases Branch, Centers for Disease Control and Prevention. Her interests include the epidemiology of fungal infections and health communications.

Dr Park is a medical officer in the Mycotic Diseases Branch, Centers for Disease Control and Prevention, and leader of the branch epidemiology team. His research interests include the prevention and epidemiology of fungal infections.

Address for correspondence: Benjamin J. Park, Centers for Disease Control and Prevention,1600 Clifton Rd NE, Mailstop C09, Atlanta, GA 30033, USA; email: bip5@cdc.gov

Table: Disaster-associated fungal infections *

                                                        No.
Disaster                   Reference       Location    cases

Tornado, 2011           Neblett Fanfair       USA       13
                          et al. (4)

Great East Japan           Kawakami          Japan       1
Earthquake and            et al. (5)
Tsunami, 2011              Nakamura          Japan       1
                          et al. (6)
                       Igusa et al. (7)      Japan       1

Hurricane Ike,         Riddel et al. (8)      USA        3
2008

Hurricane Katrina,      Rao et al. (9)        USA        1
2005

Indian Ocean            Petrini et al.     Thailand      2
Tsunami, 2004                (10)
                        Garzoni et al.     Thailand      2
                             (11)
                           Gunaratne       Colombo,      6
                          et al. (12)      Sri Lanka
                        Andresen et al.    Sri Lanka     1
                             (13)
                           Snell and       Thailand      1
                         Tavakoli (14)
                        Maegele et al.     Southeast     1
                             (15)            Asia        1

Earthquake, 1994       Schneider et al.       USA       203
                             (16)

Volcano, 1985            Patino et al.     Colombia      8
                             (17)

Dust storm             Flynn et al. (18)      USA       115
originating near
Bakersfield,            Williams et al.       USA       18
California, 1977             (19)

Disaster                  Fungal organism         Type of infection

Tornado, 2011              Apophysomyces             Soft tissue
                           trapeziformis

Great East Japan       Aspergillus fumigatus    Pulmonary, multi-organ
Earthquake and                                      dissemination
Tsunami, 2011              Scedosporium             Lung and brain
                            apiospermum               abscesses

                           Pathogen not             Sinusitis and
                       identified ([dagger])          meningitis

Hurricane Ike,          Unspecified agent of         Soft tissue
2008                    chromoblastomycosis

Hurricane Katrina,        Cladosporium sp.            Pulmonary
2005

Indian Ocean             Cladophialophora            Soft tissue
Tsunami, 2004                 bantiana
                                                 Spondylodiscitis, 1;
                           Scedosporium            brain abscess,1
                            apiospermum               Meningitis

                            A. fumigatus

                       Apophysomyces elegans         Soft tissue

                             A. elegans              Soft tissue

                            Fusarium sp.         Soft tissue, sepsis
                             Mucor sp.               Soft tissue

Earthquake, 1994        Coccidioides immitis     Pulmonary; 6 (3.7%)
                                                     disseminated

Volcano, 1985            Rhizopus arrhizus           Soft tissue

Dust storm                   C. immitis          Pulmonary; 16 (14%)
originating near                                     disseminated
Bakersfield,                 C. immitis           Pulmonary; 4 (22%)
California, 1977                                     disseminated

Disaster                  Outcome

Tornado, 2011          38% all-cause
                         mortality

Great East Japan           Death
Earthquake and
Tsunami, 2011              Death

                           Death

Hurricane Ike,            Recovery
2008

Hurricane Katrina,        Resolved
2005                      without
                         treatment

Indian Ocean              Recovery
Tsunami, 2004
                          Recovery

                       50% all-cause
                         mortality
                       Not specified

                          Recovery

                           Death
                       Not specified

Earthquake, 1994       1.5% all-cause
                         mortality

Volcano, 1985          80% all-cause
                         mortality

Dust storm              7% all-cause
originating near         mortality
Bakersfield,           5.5% all-cause
California, 1977         mortality

* As documented in reports with sufficient detail about the
number of persons affected, pathogen, and body site. Reports
describing cases of post-disaster fungal colonization without
infection are not included in the table. Number of cases and
percentages are provided when data were available.

([dagger]) Fungai infection diagnosed on the basis of cerebrospinal
fluid profile (decreased glucose, high mononuclear cell
count, + [beta]-D  glucan test result).
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Title Annotation:SYNOPSIS
Author:Benedict, Kaitlin; Park, Benjamin J.
Publication:Emerging Infectious Diseases
Article Type:Author abstract
Date:Mar 1, 2014
Words:5381
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