THE PREVALENCE OF SERIOUS AND CHRONIC FUNGAL DISEASES IN
THE RUSSIAN FEDERATION
Klimko N1, Kozlova Y1, Khostelidi S1, Shadrivova O1, Borzova Y1, Burygina E1,
Vasilieva N1 and Denning D2
1
I.Metchnikov North-Western State Medical University, St. Petersburg, Russia
The University of Manchester, UK in association with the LIFE program at www.LIFEworldwide.org
2
Abstract. The aim of this research is to estimate the prevalence of serious and chronic
fungal diseases in the Russian Federation. According to the model proposed by LIFE (Leading
International Fungal Education) community was determined the number of newly emerged
diseases (tinea capitis, invasive aspergillosis, invasive candidiasis, cryptococcal meningitis,
mucormycosis, Pneumocystis pneumonia) and chronic diseases (recurrent Candida vaginitis,
recurrent oral and oesophageal candidiasis, chronic pulmonary aspergillosis, allergic
bronchopulmonary aspergillosis, severe asthma with fungal sensitization) in 2011 (www.LIFEworldwide.org). The data was obtained from national studies and in the cases of their absence –
from international studies. The total number of patients with serious and chronic fungal diseases
was 2.7 million people in the Russian Federation in 2011. Most of these patients (2 207 093
persons) had superficial fungal infections: recurrent Candida vaginitis, recurrent oral and
oesophageal candidiasis, tinea capitis. 75 995 patients had invasive mycosis: invasive
candidiasis, invasive and chronic aspergillosis, cryptococcal meningitis, mucormycosis and
Pneumocystis pneumonia. The total number of patients with allergic bronchopulmonary
aspergillosis and severe asthma with fungal sensitization was 406 082.
Key words: fungal diseases, mycosis, Russian Federation
Introduction.
Over the past decades, fungal diseases have become a serious clinical problem. The
number of fungal diseases is progressively increasing worldwide but more epidemiologic studies
are required. The prevalence of different variants of fungal infections remains unstudied.
Exceptions are candidemia and cryptococcosis the incidence of which was analyzed in large
population studies. National study of patients with candidemia was conducted in Denmark from
2004 to 2009 [1]. The results of multicenter study of cryptococcosis was published by Hajjeh
RA, Conn LA, Stephens DS at al. in 1999.
1
For superficial mycosis is typical longtime relapsing course of disease. Invasive mycosis
have severe clinical manifestations and high mortality rate. Many fungal infections are
characterized by a rapid and aggressive course. Worldwide mortality from fungal infections is
comparable to mortality from tuberculosis or malaria and is 1 350 000 patients per year [2, 3].
Therefore, the LIFE (Leading international fungal education) organization has launched the
initiative to calculate the preliminary epidemiological parameters for fungal diseases in many
countries (www.LIFE-worldwide.org). In our research we used the calculation models proposed
by LIFE. The obtained data allows to estimate the prevalence of main chronic and severe fungal
diseases in the Russian Federation.
The aim of this research is to estimate the prevalence of serious and chronic fungal
diseases in the Russian Federation. Previously such evaluation was not performed.
Materials and Methods.
According to the LIFE methodology, calculation was performed using the data received
in 2011. The results of already published epidemiological studies of fungal infections in the
Russian Federation were analyzed. If the official data was absent, we determined the size of
specific groups with the risk of fungal infections development and then used published data of
mycosis frequency in these groups of patients for estimating the national prevalence of mycosis.
Statistics information about number and structure of Russian population was obtained from the
Federal State Statistics Service (http:www.gks.ru/).
The incidence of the scalp mycosis was assessed according to the data of the Ministry of
Health [4].
Number of patients with chronic recurrent vulvovaginal candidiasis was calculated
according to the international epidemiological studies data, which showed that this disease
occurred in 5% of women in the population [5].
The number of patients with HIV/AIDS in the Russian Federation was evaluated
according to the data of the Ministry of Health [6]. Different literature sources (Smith E, Orholm
M. in 1990; Matee M.I., Scheutz F., Moshy J. in 2000) showed that oropharyngeal candidiasis
was detected in 90% and esophageal candidiasis in 20% of HIV-infected patients.
According to the results of our previous studies, the incidence of candidemia and Candida
peritonitis was 0.37 per 1000 persons hospitalized to in-patient department [7]. The total number
of in-patients in hospitals for the year was obtained from the report about hospital-acquired
infections of Federal Service on Consumers’ Rights Protection and Human Well-being
Surveillance [8].
2
The prevalence of hematological diseases was evaluated according to the data of the
Ministry of Health [9]. In patients with hematological diseases the risk of invasive aspergillosis
(IA) development was calculated according to the data of the National Register of Patients with
Invasive Aspergillosis created in St. Petersburg [10]. The information about number of organs
and tissue transplantations made in 2011 was obtained from Russian Transplantation Society
data [11]. Among patients who underwent hematopoietic stem cell transplantation (HSCT) the
incidence of invasive mycosis was evaluated according to our earlier study results [12]. The total
number of patients with IA was calculated according to the formula proposed by Denning D.W.:
10% of patients with acute myeloid leucosis + 0.5% of patients after kidney
transplantation + 4% of patients after lung transplantation + 6% of patients after heart
transplantation + 4% of patients underwent liver transplantation + 1.3% of patients admitted to
hospital with chronic obstructive pulmonary disease = total number of patients with IA.
The incidence of mucormycosis in the general population was calculated using the data of
the National Register created in St. Petersburg and the data of the Ministry of Health of the
Russian Federation on acute myeloid leucosis prevalence [9].
The overall morbidity of tuberculosis was evaluated according to the information of the
Ministry of Health [13]. The calculation of possible cases number of chronic pulmonary
aspergillosis (CPA) was performed according to the formula proposed by Denning D.W. et al.
[14]:
The annual number of cases of tuberculosis of lungs with the presence of cavities (≈ 12%
of the total number)  the risk of CPA development (22%) + the number of emerged cases of
tuberculosis without cavities (≈ 88% of the total incidence)  risk of CPA in this patients (2%) =
possible cases of CPA.
The number of patients with asthma was obtained from the data of the Russian
Respiratory Society [15]. The estimated number of patients with allergic bronchopulmonary
aspergillosis (ABPA) was calculated by another formula proposed by Denning D.W. et al. [16]:
2.5% of patients with asthma + 155 of adult patients with cystic fibrosis = estimated
patients with ABPA.
To assess patients with severe asthma with fungal sensitization was considered that 10%
of patients with asthma have severe course of disease and 33% of them have fungal sensitization
[17].
The information about cystic fibrosis (CF) incidence was obtained from the Russian
Register of Patients with Cystic Fibrosis [18]. According to the data of Medical Genetic
Research Center of Russian Academy of Science among patients with CF 21% were adults [19].
3
The results of research performed in St.Petersburg was used to calculate the incidence of
cryptococcal meningitis. In 2011 cryptococcal meningitis occurred in 0.44 % of patients with
HIV [20]. The number of Pneumocystis pneumonia cases was calculated on the base of the LIFE
data according to which Pneumocystis pneumonia develops in 60% of HIV-infected patients
who receive antiretroviral therapy.
Results and Discussion.
In 2011 the population of the Russian Federation was 142.9 million, 85% of which were
adults and 15% were children younger than 14 years. Among adults 54% were women. In table 1
is showed the prevalence of different fungal diseases and its incidence per 100 000 inhabitants.
Fungal diseases of the scalp
According to the data obtained from the Ministry of Health of the Russian Federation the
total number of patients with tinea capitis (caused by Microsporum canis or Trihophyton spp.)
was 60 366 persons, 47 092 of which were children. The prevalence of tinea capitis caused by
Microsporum canis was 40.8 per 100 000 persons and 213.1 per 100 000 children. Tinea capitis
caused by Trihophyton spp. was less frequent – 1.8 per 100 000 persons and 6.9 per 100 000
children. These results exceeded the average levels in Europe. For example, in Greece the overall
incidence of tinea capitis was 6.06 per 100 000 people [21], in Denmark – 3.3 per 100 000 [22].
According to the data of LIFE experts the highest incidence of these superficial mycosis was in
Vietnam – 457 per 100 000 people [23].
Mucosal candidiasis
Chronic recurrent vulvovaginal candidiasis is characterized by frequent relapses (at least
4 per year) and is the most common recurrent fungal disease in Russia. According to our
estimations 2 072 679 Russian women suffer from chronic recurrent vulvovaginal candidiasis
which is 2 900 per 100 000 people. The similar data was obtained in Europe (in Hungary – 2193
per 100 000)[24] and in other countries (in Iraq – 2664 per 100 000)[25]. In Ukraine the
prevalence of recurrent vulvovaginal candidiasis is higher – 3 923 per 100 000 people [26].
In 2011 in Russia the number of patients with first diagnosed HIV infection was 67 317
(47.1 per 100 000 people) [9]. Hence, the number of HIV-infected patients with oropharyngeal
candidiasis amounted 60 585 persons (42.4 per 100 000 people). The estimated number of HIVinfected patients with Candida esophagitis was 13 463 persons (9.42 per 100 000). International
epidemiological observations also are focused on the study of Candida esophagitis only in the
group of HIV-infected patients. According to the data of LIFE experts the frequency of this
4
fungal disease in Hungary was 1.56 per 100 000 people, in the UK and Denmark – 0.1 per
100 000 [22, 27, 24]. Currently, the determination of esophageal candidiasis incidence in patients
without HIV infection is a subject of one of our researches.
Invasive candidiasis
In 2011, 32 million patients were treated in the inpatient departments of the Russian
Federation. The total number of patients with invasive candidiasis was 11 840 per year. Thus, the
frequency of invasive candidiasis in the population was estimated 8.29 per 100 000 people.
These values corresponds to the average levels in Europe. In European countries this parameter
varies from 5.0 to 11.4 per 100 000 people. However, the international studies showed that 50%
of patients in the ICU with candidemia had Candida peritonitis [28]. According to the results of
our research candidemia was noted more often (82%) than Candida peritonitis (18.4%) [7].
Pulmonary aspergillosis
It is known that hematologic diseases are one of the major risk factor for invasive
aspergillosis (IA) development. According to our register, 88% of patients with IA have
hematologic diseases 30% of which is acute myeloid leucosis (AML). This data correlates with
the results of European studies. The incidence of AML in patients with IA in Italy is 36% [29],
in France – 35% [30]. According to the European average values, the risk of IA in these patients
is 10%. Thus, in Russia every year there are 160 new cases of IA in patients with AML.
According to the formula proposed by Denning D.W. the same number of IA cases develops in
patients with other hematologic malignancies.
Annually about 200 hematopoietic stem cell transplantations are carried out in the
Russian Federation [11]. According to the results of the studies made in St. Petersburg, the
incidence of invasive mycosis in HSTC recipients was 19.1% and in recipients of allogeneic
HSCT – 23.2% [12]. 82.3% of these mycoses were caused by fungi of the genus Aspergillus spp.
Thus, in Russia the incidence of invasive aspergillosis in HSCT recipients varied from 16 to
20%. For calculation was used the rate 20%, so in these patients there were 40 cases of IA.
Organ and tissue transplantation and the related glucocorticoid therapy are also the risk
factors for IA. Most often IA develops in lung transplant recipients. The results of international
studies show that the incidence of IA after organ transplantations varies from 0.3 to 14% [31,
32]. According to the data of the Federal Scientific Center of Transplantation and Artificial
Organs named after Academician V.I. Shumakov in Russia in 2011 was performed 975 kidney
transplantations, 204 liver transplantations and 106 heart transplantations [33]. For determining
the risk of IA we used the European average values which believed to be 0.5% of patients after
kidney transplantation, 4% - after lung transplantation, 6% - after heart transplantation, 4% 5
after liver transplantation. It amounted in total 19 cases of IA in 2011. Summing up all the
parameters, 385 cases of invasive aspergillosis had occured in hematological patients and
recipients of solid organs transplants.
In the Russian Federation in 2011 was hospitalized 219 322 in-patients with chronic
obstructive pulmonary disease (COPD). According to Denning D.W. the risk of IA development
in these patients was 1.3%. Thus IA had occurred in 2853 with COPD. Using the above
mentioned formula was calculated the total number of newly emerged IA in the Russian
Federation which amounted 3238 patients (2.27 cases per 100 000 people). According to the data
of LIFE experts the similar results of IA prevalence were obtained in European countries (in
Greece – 3.27 per 100 000, in Hungary – 1.54 per 100 000) as well as in Iraq (2.62 per 100 000)
[21, 24, 25].
Chronic pulmonary aspergillosis (CPA) occurs in patients with chronic pulmonary
diseases (tuberculosis, sarcoidosis, chronic obstructive pulmonary disease, cystic fibrosis).
Overall incidence of tuberculosis in Russia in 2011 was 104 320 cases (68.1 per 100 000), which
included 94 297 cases of pulmonary tuberculosis (66.0 per 100 000). Fibrous-cavernous lung
tuberculosis was diagnosed in 1901 patients (1.33 per 100 000 population). Among the resident
population of Russia 10.3% of patients with tuberculosis were HIV-positive. The incidence rate
of tuberculosis in association with HIV infection in 2009 was 4.4 per 100 000 population, in
2011 – 5.6 per 100 000. The possible cases of chronic pulmonary aspergillosis were calculated in
accordance of the formula proposed by Denning D.W. et al. During 5-year period 13 078 cases
of CPA on the background of tuberculosis have occurred according this calculation. The total
number of patients with CPA was 52 311 (126 per 100 000 population). This data was consistent
with the results in Ukraine where the frequency of CPA was 109 per 100 000 population. In
other countries this parameter was much lower: in the UK – 8.1/100 000, in Greece –
3.48/100000, in Denmark – 3.05/100 000 [27, 21, 22].
Mucormycosis.
According to the data of the register of patients with mucormycosis in St. Petersburg in
2011, was calculated the incidence of mucormycosis in patients with acute myeloid leucosis
(AML) which was 3.6%. In 2011 in the Russian Federation overall was registered 1599 patients
with AML. In accordance to our calculations, in 58 hematologic patients the disease was
complicated by mucormycosis. On the basis of our study results, AML was a risk factor for
mucormycosis only in 25% of cases. Thus, the total number of patients with mucormycosis was
232 people (0.16/100 000). The calculated incidence of mucormycosis in Russian Federation
6
corresponded to the values in European countries. The frequency of mucormycosis in Greece
was 0.12/100 000, in Hungary – 0.1/100 000 population [21, 24].
Allergic bronchopulmonary disease
Epidemiological prevalence of asthma in Russia, as in other countries, far exceeds the
official medical statistics data. The experts of the Russian Respiratory Society estimated that the
number of patients with asthma in the Russian Federation is about 7 million people. Using the
formula proposed by Denning D.W. et al [16, 17] was calculated the estimated number of
patients with allergic bronchopulmonary disease (ABPA), which was 175 082 patients, and
number of patients with severe asthma and fungal sensitization (SAFS), which was 231 000
people. The total number of patients with ABPA and SAFS was 406 082 people. The incidence
of ABPA and SAFS in the Russian Federation corresponded the parameters in Denmark (ABPA
– 125/100 000; SAFS – 163/100 000). According to the data of LIFE experts the highest
frequency of ABPA was in UK (287/100 000) and the lowest was in Iraq (16/100 000) [22, 27.
25].
Pneumocystis pneumonia and cryptococcal meningitis.
Pneumocystis pneumonia (PCP) and cryptococcal meningitis are among the major
opportunistic infections in patients with HIV. In the Russian Federation the incidence of PCP
was 5.65 cases per 100 000 people or 8078 cases per year. High incidence of PCP also was
marked in Ukraine – 13.5/100 000 [26]. In other countries this parameter was lower: in the UK –
0.94/100000, in Greece – 0.52/100 000, in Hungary – 0.05/100 000 people [27, 21, 24].
The overall incidence of cryptococcal meningoencephalitis in the Russian Federation was
296 cases per year (0.21/100 000), which corresponded to the data in Ukraine (0.22/100 000)
[26]. In the UK the frequency of cryptococcal meningoencephalitis was 0.16 per 100 000
population [27]. In other European countries the incidence of this opportunistic infection was
lower. For example, in Greece were detected less than five cases per year, in Denmark – two
cases per year [21, 22].
In Russia the high incidence of Pneumocystis pneumonia and cryptococcal meningitis
was certainly related to a large number of HIV patients in the country. Despite the antiretroviral
therapy, the number of patients detected in the later stages of the disease with severe secondary
lesions continues to grow.
Our study showed that mycoses are common diseases in Russian Federation. However, in
our work, we haven’t evaluated all fungal diseases because we wanted to save a single model of
7
the LIFE research and to have opportunity to compare the results with those of other countries.
For example, in this study we haven’t included mycosis of the smooth skin, mycosis of the feet
and hands, onychomycosis, chronic candidiasis of the skin and mucous, and some others.
We compile and constantly update the register of patients with severe invasive fungal
diseases but we don’t have our own data of the chronic fungal diseases prevalence. In this work
we used the results of international researches. Therefore, one of the main tasks in the study of
fungal diseases in the Russian Federation is registration not only the newly diagnosed cases of
invasive fungal infections but also chronic fungal infections (ABPA, SAFS, CPA, chronic
recurrent vulvovaginal candidiasis).
Further study of the mycosis epidemiology is especially important because the results of
it are the basis for preventive measures and treatment optimization of fungal diseases throughout
the world.
Conclusions.
1. Mycosis are common diseases in the Russian Federation. In 2011, according to the
estimation, there were 2.7 million patients with severe and chronic fungal disease.
2. Chronic superficial mycoses (recurrent vulvovaginal candidiasis, recurrent oral and
esophageal candidiasis, tenia capitis) had occurred in 2 207 093 people.
3. Invasive fungal diseases (invasive candidiasis, invasive and chronic aspergillosis,
cryptococcal meningitis, mucormycosis, Pneumocystis pneumonia) had occurred in
75 995 patients.
4. The total number of patients with ABPA and SAFS was 406 082.
5. In the Russian Federation is required registration of severe and chronic fungal diseases as
well as conducting further epidemiological studies of mycoses.
Table 1.
Fungal Diseases in Russian Federation
Fungal Diseases
Newly emerged
diseases
Invasive aspergillosis
Invasive candidiasis:
Cryptococcal meningitis
Mucormycosis
Pneumocystis pneumonia
Tinea capitis (caused by
Microsporum canis)
Tinea capitis (caused by
Trihophyton spp.)
Rate/100K
2,27
Total Burden
0,21
0,16
5,65
40,8
3238
11 840
296
232
8 078
57 871
1,8
2 495
84 050
Chronic recurrent Candida
8
Chronic diseases vulvovaginitis
Recurrent oral candidiasis
Recurrent oesophageal
candidiasis
Chronic pulmonary aspergillosis
Allergic bronchopulmonary
aspergillosis
Asthma with fungal
sensitization
2900
42,4
9,42
2 072 679
60 585
13 463
126,19
122,52
52 311
175 082
161,65
231 000
2 605 120
Total burden estimated
2 689 170
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