Advances in Infectious Diseases, 2012, 2, 76-81 Published Online September 2012 (
Mucormycosis: A Review on Environmental Fungal Spores
and Seasonal Variation of Human Disease
Rima I. El-Herte, Tania A. Baban, Souha S. Kanj*
Division of Infectious Diseases, Department of Internal Medicine, American University of Beirut Medical Center, Beirut, Lebanon.
Email: *
Received May 1st, 2012; revised June 3rd, 2012; accepted July 5th, 2012
Mucormycosis is on the rise especially among patients with immunosuppressive conditions. There seems to be more
cases seen at the end of summer and towards early autumn. Several studies have attempted to look at the seasonal varia-
tions of fungal pathogens in variou indoor and outdoor settings. Only two reports, both from the Middle East, have ad-
dressed the relationship of mucormycosis in human disease with climate conditions. In this paper we review, the rela-
tionship of indoor and outdoor fungal particulates to the weather conditions and the reported seasonal variation of hu-
man cases.
Keywords: Mucormycosis; Seasonal Variation; Fungal Air Particulate Concentration; Mucor; Rhizopus; Rhinocerebral
1. Introduction
Mucormycosis refers to infections caused by molds be-
longing to the order of Mucorales. Members of the fam-
ily Mucoraceae are the most common cause of mucor-
mycosis in humans. This includes the genera Absidia,
Mucor, Rhizomucor, and Rhizopus. Two additional patho-
genic families are the Cunninghamellaceae and the Sak-
senaceae. These are opportunistic fungi that are able to
cause acute, rapidly progressing fulminant infections in
compromised hosts. They can cause rhinocerebral, pul-
monary, gastrointestinal, cutaneous and disseminated in-
fections. Risk factors for such infections include diabetes,
ketoacidosis, lymphoma, leukemia, neutropenia, corti-
costeroid use, long term immunosuppressive therapy, de-
feroxamine therapy, and prior intake of fungal prophy-
laxis with voriconazole [1]. Such infections are fatal if no
adequate and rapid surgical and medical interventions are
initiated. Two reports suggested that the incidence of
mucormycosis increases in summer and early autumn
[2,3]. In this review, we present the available published
literature on the seasonal variation of the air concentration
of various spores of mucorale sp. and other fungi and the
seasonal variation of clinical mucormycosis.
2. Environment and Seasonality
Mucorales are thermotolerant. They are ubiquitous in na-
ture and widely found on organic substrates, including
bread, decaying fruits, vegetable matters, crop debris, soil,
compost piles, animal excreta, and on excavation and con-
struction sites. Sporangiospores are easily aerosolized, and
are readily dispersed throughout the environment making
inhalation the major mode of transmission. Published data
describing the levels of zygomycete sporangiospores in
outdoor and indoor air in relation to seasonal variation is
2.1. Outdoor Concentration and Seasonal
Most of the studies addressing variations of fungal spores
in the air in relation to the season have been done in
European countries. The earliest study that considered
metereological conditions and airborne particulate con-
centration of fungi was done in Athens and showed that
during autumn and winter the number of suspended mi-
crofungi was twice as high as in spring and summer [4];
Mucor species were cultured during the months of June
through December excluding September. This result sug-
gested a positive correlation with humidity and a nega-
tive correlation with temperature. In a Spanish study
done in 1980 over a two-year survey on the airborne
fungi in the atmosphere of Barcelona, Rhizopus, and Mu-
cor were the second most commonly isolated fungi after
Aureobasidium [5]. In another study by Herrero in Pa-
lencia in 1992, air cultures revealed that Mucor sp. were
the most common pathogens (25%) followed by Asper-
gillus sp. (23%) and Penicillium sp. (16%). Thirty two
percent of the fungal colonies grew in autumn, while
*Corresponding author.
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Mucormycosis: A Review on Environmental Fungal Spores and Seasonal Variation of Human Disease 77
28% during spring [6]. A study from Ankara, Turkey
failed to reveal mucoracae in air particulates but showed
a predominance of other fungi such as Cladosporium
(75.5%) followed by Alternaria (6.1%), Leptosphaeria
(2.2%) and others. The highest value of spore concentra-
tion was detected in July, and the lowest in January. This
was thought to be related to monthly mean temperatures,
wind velocity and humidity [7]. Soil and air samples
from seven different localities around a Turkish city were
sampled and revealed that the most isolated genus from
air samples was Alternaria (43.96%), followed by Clado-
sporium (25.52%) and Phoma (5.40%) [8]. Fusarium and
Penicillium occurred at very low concentrations in air
and no mucoracae were isolated. The highest airborne
spore concentration was found during autumn and the
lowest concentration during the summer. Aspergillus’ air
spore concentration was very low in all seasons during
the research period [8]. Another Turkish study meas-
uring the indoor and outdoor concentration of fungi in
Istanbul revealed that Cladosporium and Alternaria were
the most commonly recovered followed by Penicillium,
Aspergillus, Rhizopus, Aureobasidium, Mucor and Fusa-
rium at a lower concentration [9]. Oliveria et al. found
similar results in Porto, Portugal: Cladosporium being
the most common to recover (74.5%) throughout the year
followed by Alternaria, Aspergillus, Penicillium, Botry-
tis, Coprinus, Epicoccum, Fusarium, Ganoderma, Mucor ,
and Ustilago. The highest airborne spore concentrations
in Porto were observed during summer and late autumn
and the lowest during winter and were negatively corre-
lated with wind speed; while positively correlated with
temperature and relative humidity. Alternaria, Botrytis
and Ganoderma spore density peaked from summer to
autumn. Spore densities of Corynespora, Fusarium, Oid-
ium, Periconia and Rhizopus peaked in late spring [10].
Results were similar in studies done from Northeast
America where Cladosporium sp. was also dominant in
both indoor and outdoor air in summer, with not much
isolated mucoracae [11]. In another study done in the
USA in 2002, the median outdoor fungal concentrations
varied according to seasons and were highest in the fall
and summer and lowest in the spring and winter. Mostly
they were Cladosporium, Penicillium, Aspergillus; how-
ever, there was no available data concerning Mucor and
Rhizopus sp. [12]. The seasonal variation of fungal pro-
pagules in a fruit market environment in Nagpur, India
showed that Aspergillus was the most frequent and pre-
dominant genus detected, peaking in summer, followed
by Cladosporium, Penicillium and Alternaria peaking
during December-January [13]. Fungi related to animals
have also been studied. Rodents from a Czech study
showed that they harbor various species of Aspergillus,
Mucor and Penicilliu m ; R. oryzae represented 10% of the
fungi [14]. Studies on the fungal biota of the fur of dogs
in Spain yielded Alternaria, Aspergillus, Cladosporiurn,
Chrysosporium, Penicillium and Scopulariopsis. Mucor
(27.3%) peaked in autumn and Rhizopus (14.5%) in
summer [15]. Another study looking into the dermatomy-
cosis of the dogs revealed that Mucor sp. formed 1.5% of
the causative agents mostly in warm and humid climates
[16]. In an Indian study, fungi involved in skin infections
in poultry included Aspergillus, Pencillium, Alternaria,
Rhizopus, Chry sospor ium, Mucor , Scopulariopsis among
others and the soil tested in the vicinity revealed Chry-
sosporium, Alternaria, Aspergillus, Paecilomyces, Peni-
cillium, Mucor, and Rhizopus among various other gen-
era [17].
2.2. Indoor Concentration and Seasonal
The spore density of different fungi was measured in
different districts of Istanbul and the results showed that
Penicillium and Aspergillus were the most abundant fol-
lowed by Rhizopus, Mucor and Fusari um; Rhizopus was
found at a lower density outdoors than in indoor air [9].
In the US, the indoor fungal concentrations were founde
to be highest in the fall and summer and lowest in the
spring and winter. The most commonly recovered fungi
were Cladosporium, Penicillium, the nonsporulating fungi
and Aspergil lus. Mucor and Rhizopus sp. were detected
mostly in winter and summer [12]. Also indoor mycobiota
varied with the niche. Wooden and paper materials had
the highest median concentrations of fungi whereas min-
eral insulation, ceramic products, and paints and glues
had the lowest. The wooden materials harbored Penicil-
lium and yeasts, as well as Cladosporium and Stachybotrys.
Ceramic products, paints and glues seemed to favor
Acremonium and Aspergillus versicolor [18].
2.3. Seasonal Variation of Human Disease
Roden et al. analyzed 929 cases of mucormycosis with-
out shedding light on its seasonal variation [19]. Possible
seasonal variation of mucormycosis has been addressed
in 2 studies, both from the Middle East. Al-Ajam et al.
reported a series of 16 cases of invasive rhinocerebral,
cutaneous and pulmonary mucormycosis. He showed that
the onset of symptoms clustered at the end of a dry pe-
riod, which consistently extended from late May to Oc-
tober; i.e. early summer to end of autumn in 12 out of 16
patients with a statistically significant seasonal variation
(p = 0.007) which coincided with increasing rain levels
[2]. However, data is lacking on the mycobiota species
and their concentration in Beirut or any other cities in
Lebanon. A similar study from Israel analyzing 36 cases
of rhinocerebral mucomycosis showed that most of the
cases occurred between August and December with a
peak incidence in September. In this country, the weather
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Mucormycosis: A Review on Environmental Fungal Spores and Seasonal Variation of Human Disease
Copyright © 2012 SciRes. AID
is hot and humid from May till September. Rhizopus
oryzae was the most commonly isolated organism [3].
Infection with mucorales has also been reported to o-
ccur as a consequence of natural disasters such as vol-
canic eruptions [20] and tsunami [21,22]. In some reports,
the victims had multiple sites of necrotizing fasciitis due
to R. arrhizus, Apophysomyces elegans and others. Analy-
sis of the volcanic mud flow revealed Rhizopus arrhizus,
Mucor sp., Trichoderma sp., Penicillium sp., Fusarium sp.,
Aspergillus niger, Paecylomyces sp. and Candida sp.
Table 1 summarizes the various studies done correlat-
ing fungi, air particulate concentration with season and
3. Discussion
The various published reports show that Mucor and
Rhizopus sp. are not among the most commonly isolated
fungi from outdoors environment with highest outdoor
concentrations in spring and summer [13,15], whereas
indoor concentration of these fungi was highest during
winter and spring [13]. Other studies have failed to detect
any mucorales by PCR from indoor and outdoor air sam-
ples [23]. Hence a clear conclusion cannot be reached.
Sesonal variation of human mucormycosis seems to be
plausible. The 2 studies from the Middle East showed
that most cases of mucormycosis occurred in late sum-
mer, fall and early winter. In Lebanon, the cases clus-
tered between August and December when the weather
ranges from hot and dry to wet and cool. In Israel, the
weather is very similar to Lebanon and cases also had a
similar distribution according to the months of the year
(Figure 1). In both studies there was no attempt to iden-
tify the source of infection but infection was attributed to
airborne transmission from air conditioners. Two patients
of the latter study had infection with R. oryzae, which
was also cultured from the doctor’s office. This sug-
gested that improving the ventilation systems may de-
creases the incidence. Also no unusual precipitations or
temperature data were recorded from the Israeli study. It
is probable that infestation can build up in earlier months
and manifest in August and September. However, in both
studies there is no data about the fungal particulate air
concentration to correlate them to this type of fungal in-
fection. Other publications about invasive mucormycosis
infection did not mention any information about the sea-
son when these patients were diagnosed [19]. There re-
main many unanswered questions that need to be ad-
dressed in future studies. Particularly investigating whe-
ther the organisms have a true seasonal variation in out-
door and indoor settings and whether this correlates to
human diseases. Since both studies addressing seasonal
variations of human disease have been done in the Mid-
dle East in countries with similar weather and humidity
conditions, the results cannot be extrapolated to other
regions and countries. It will be of interest to study this
in various centers worldwide where there are increasing
numbers of immunosuppressed patients at risk for mu-
cormycosis such as oncology and transplant patients.
Knowledge about seasonal variation of this deadly fungal
infection might have important implications. Physicians
will have a lower threshold to consider such infections in
their immunocompromised hosts, better attention to air
filters in transplant units during peak seasons, and possi-
ble prophylaxis in outbreak situations, especially with the
availability of potent oral agents such as posaconazole
are to be considered [24]. Since mucormycosis is fatal in
most cases when therapy is delayed, more efforts should
be done by the medical community caring for immuno-
compromised patients to better understand its epidemic-
ology. The availability of advanced culture and molecu-
Figure 1. Distribution of mucormycosis cases versus month of year in Israel and Lebanon (with permission from author [2]).
Mucormycosis: A Review on Environmental Fungal Spores and Seasonal Variation of Human Disease 79
Table 1. The table shows each author’s publication, country, year time during which the highest concentration of fungi was
recovered, the fungi recovered and associated meteorological factors. High humidity, rain, low temperatures showed positive
correlation with increasing air particulates concentration; not all studies showed correlation with wind velocity.
Author/Country Year Time Molds Species Factors
Outdoor Bartzokas/Greece Autumn & Winter Aspergillus
Low Temperature and
Increase Humidity
Calvo et al./Spain Aureobasidium
Herrero/Spain Autumn & Spring Mucor
Ceter et al./Turkey July Cladosporium
Wind Speed
Asan et al./Turkey Autumn Alternaria
Çolakoğlu/Turkey Cladosporium
Mucor Fusarium
Oliveria et al./Portugal Summer & Late Autumn Cladosporium
Temperature Humidity
Ren et al./ Summer Cladosporium
Shelton et al./USA Summer & Autumn Cladosporium
Kakde et al./India December-January/Summer Aspergillus
Stejskal et al./Czech Aspergillu,
R. oryzae
Cabafies et al./Spain Summer & Autumn Alternaria,
Jand et al. Mucor Warmth and Humidity
Saidi et al./India Chrysosporium
Penicillius Mucor
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Mucormycosis: A Review on Environmental Fungal Spores and Seasonal Variation of Human Disease
Copyright © 2012 SciRes. AID
Indoor Çolakoğlu/Turkey Penicillium
Rhizopus, Mucor
Shelton et al. Fall & Summer
Winter & Summer Cladosporium,
Rhizopus sp.
Human Disease Al-Ajam et al./Lebanon May-October/Summer-Autumn Rain
Shpitzer et al./Israel August-December/Summer-Winter
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