Сравнительная характеристика особенностей микробиоты кишечника жителей Гвинейской Республики и России

Попова А.Ю.; Кафтырева Лидия Алексеевна; Сужаева Л.В.; Войтенкова Е.В.; Забровская А.В.; Егорова С.А.; Макарова М.А.; Матвеева З.Н.; Зуева Е.В.; Порин А.А.; Буаро М.Й.; Константинов О.К.; Арег А. Тотолян

Original articles

Оригинальные статьи

Russian Journal of Infection and Immunity = Infektsiya i immunitet 2017, vol. 7, no. 4, pp. 375-382

COMPARATIVE CHARACTERISTICS OF INTESTINE MICROBIOME OF REPUBLIC OF GUINEA AND RUSSIAN FEDERATION RESIDENTS

A.Yu. Popovaa, L.A. Kaftyreva\ L.V. Suzhaevab, E.V. Voitenkovab, A.V. Zabrovskaiab, S.A. Egorovab, M.A. Makarovab, Z.N. Matveevab, E.V. Zuevab, A.A. Porinb, M.Y. Boiroc, O.K. Konstantinov0, Areg A. Totolianb

a Federal Service for Surveillance on Consumer Rights Protection and Human Wellbeing, Moscow, Russian Federation b St. Petersburg Pasteur Institute, St. Petersburg, Russian Federation c Research Institute for Applied Biology of Guinea, Kindia, Republic of Guinea

Abstract. The gut microbiota of healthy people, living in different regions, may vary considerably. The article presents the results of comparative qualitative and quantitative study of the intestine aerobic and anaerobic microbiota of residents of the Republic of Guinea (46) and Russia (60). The content of microorganisms (Enterobacteriaceae, Enterococcus spp., Lactobacillus spp., Bifidobacterium spp., Staphylococcus spp., Candida spp., non-fermentative gram-negative bacteria and others) in 1.0 gram of faeces was determined by bacteriological methods. Generic and species identification was performed using Vitek 2 Compact (bioMerieux, France), tube biochemical tests and MALDI-TOF mass spectrometry (Bruker Daltonics, Germany). Pearson X2 criterion, p < 0.05 and Fisher's exact test (medstatistica.ru) were used to assess the differences in the compared groups. 95% confidence intervals were calculated by the method of Wilson. Microbiological disorders were characterized by a decrease in the number of obligate microorganisms, an increase in the number of facultative (opportunistic) microorganisms (above 106 CFU/g) and the emergence of their associations. Dysbiotic disorders were identified in both compared groups: in 100% patients from Republic of Guinea (95% CI:92.3-100) and in 86.7% patients from St. Petersburg (95% CI:75.8-93.1). Severe degree of microbiota disorders in the residents of the Republic of Guinea was revealed at 19.6% (95% CI:10.7—33.2), in group ofresidents of St. Petersburg in 9.6% (95% CI:4.2—20.6). In both groups the microbiota disorders ofthird degree were detected less frequently, compared with the microbiota disorders of second degree. The study has found no significant differences in the content of obligate bacteria (Bifidobacterium spp. and Lactobacillus spp.), however, significant differences in the species composition of the facultative part of the microbiota were revealed. The residents of the Republic of Guinea had "atypical" E. coli (lac-tosonegative and hemolytic) and non-fermenting gram-negative bacteria Comamonas kerstersii more frequently. Opportunistic microorganism associations have been found in 30.4% of the residents of the Republic of Guinea (95% CI:19.1—44.8) and 18.3% of residents of St. Petersburg (95% CI:10.6—29.9). Opportunistic microorganism associations from the residents of the Republic of Guinea always contained Staphylococcus aureus. It is necessary to conduct further research on a bigger population to access the differences in the compared groups in Staphylococcus aureus and Hafnia alvei.

Key words: intestine microbiome, Republic of Guinea, Enterobacteriaceae, Hafnia alvei, Comamonas kerstersii, Staphylococcus aureus, Escherichia ^li, Enterococcus spp.

Инфекция и иммунитет 2017, Т. 7, № 4, с. 375-382

Адрес для переписки:

Кафтырева Лидия Алексеевна

197101, Россия, Санкт-Петербург, ул. Мира, 14,

ФБУН НИИ эпидемиологии и микробиологии имени Пастера.

Тел.: 8 (812) 232-48-83 (служебн.).

E-mail: kaflidia@mail.ru

Библиографическое описание:

Попова А.Ю., Кафтырева Л.А., Сужаева Л.В., Войтенкова Е.В., Забровская А.В., Егорова С.А., Макарова М.А., Матвеева З.Н., Зуева Е.В., Порин А.А., Буаро М.Й., Константинов О.К., Тотолян Арег А. Сравнительная характеристика особенностей микробиоты кишечника жителей Гвинейской Республики и России // Инфекция и иммунитет. 2017. Т. 7, № 4. С. 375-382. doi: 10.15789/2220-7619-2017-4-375-382

Contacts:

Lidiia A. Kaftyreva

197101, Russian Federation, St. Petersburg, Mira str., 14, St. Petersburg Pasteur Institute. Phone: +7 (812) 232-48-83 (office). E-mail: kaflidia@mail.ru

Citation:

Popova A.Yu., Kaftyreva L.A., Suzhaeva L.V., Voitenkova E.V., Zabrovskaia A.V., Egorova S.A., Makarova M.A., Matveeva Z.N., Zueva E.V., Porin A.A., Boiro M.Y., Konstantinov O.K., Totolian Areg A. Comparative characteristics of intestine microbiome of Republic of Guinea and Russian Federation residents // Russian Journal of Infection and Immunity = Infektsiya i immunitet, 2017, vol. 7, no. 4, pp. 375-382. doi: 10.15789/2220-7619-20174-375-382

DOI: http://dx.doi.org/10.15789/2220-7619-2017-4-375-382

СРАВНИТЕЛЬНАЯ ХАРАКТЕРИСТИКА ОСОБЕННОСТЕЙ МИКРОБИОТЫ КИШЕЧНИКА ЖИТЕЛЕЙ ГВИНЕЙСКОЙ РЕСПУБЛИКИ И РОССИИ

А.Ю. Попова1, Л.А. Кафтырева2, Л.В. Сужаева2, Е.В. Войтенкова2, А.В. Забровская2, С.А. Егорова2, М.А. Макарова2, З.Н. Матвеева2, Е.В. Зуева2, А.А. Порин2, М.Й. Буаро3, О.К. Константинов3, Арег А. Тотолян2

1 Федеральная служба по надзору в сфере защиты прав потребителей и благополучия человека, Москва, Россия

2 ФБУН НИИ эпидемиологии и микробиологии имени Пастера, Санкт-Петербург, Россия

3 НИИ прикладной биологии Гвинеи, Киндия, Гвинейская Республика

Резюме. Известно, что микробиота кишечника у клинически здоровых людей, проживающих в разных регионах, может значительно различаться. Цель исследования — сравнительное изучение качественного и количественного состава аэробной и анаэробной микробиоты кишечника на случайной малой выборке проб испражнений жителей Гвинейской Республики (46 человек) и России (60 человек). Содержание микроорганизмов (Enterobacteriaceae, Enterococcus spp., Lactobacillus spp., Bifidobacterium spp., Staphylococcus spp., дрожжепо-добные грибы рода Candida, неферментирующие грамотрицательные бактерии и др.) в 1,0 грамме фекалий определяли бактериологическим методом. Родовую и видовую идентификацию проводили с использованием бактериологического анализатора Vitek 2 Compact (bioMerieux, Франция), рутинных биохимических тестов, а также MALDI-TOF масс-спектрометрии (Bruker Daltonics, Германия). Для оценки различий результатов в сравниваемых группах применяли критерий %2 Пирсона, p < 0,05 и точный критерий Фишера, вычисленные с использованием он-лайн калькулятора medstatistica.ru. 95% доверительные интервалы рассчитывали по методу Уилсона. Микробиологические нарушения характеризовались снижением количества облигат-ных, повышением количества факультативных (условно-патогенных) микроорганизмов (в количестве 106 и выше КОЕ/г.) и появлением их ассоциаций. Дисбиотические нарушения были выявлены в обеих сравниваемых группах: у 100% обследованных из Гвинейской Республики (95% ДИ:92,3—100) и у 86,7% обследованных из Санкт-Петербурга (95% ДИ:75,8—93,1). Выраженная степень нарушений микробиоциноза в группе жителей Гвинейской Республики встречалась в 19,6% (95% ДИ:10,7—33,2), в группе жителей Санкт-Петербурга в 9,6% (95% ДИ:4,2—20,6). Как у жителей Гвинейской Республики, так и у жителей Санкт-Петербурга нарушения третьей степени выявлялись реже, по сравнению с нарушениями второй степени. Исследование не выявило значимых различий в содержании облигатных бактерий (Bifidobacterium spp. и Lactobacillus spp.), однако, выявлены достоверные различия в видовом составе факультативной части микробиоты. У жителей Гвинейской Республики чаще обнаруживали «атипичные» Escherichia coli (гемолитические и лактозонегативные) и неферментирующие грамотрицательные бактерии Comamonas kerstersii. Ассоциации условно-патогенных микроорганизмов в разных по составу сочетаниях обнаружены в составе микробиоты у 30,4% обследованных жителей Гвинейской Республики (95% ДИ:19,1-44,8) и у 18,3% жителей Санкт-Петербурга (95% ДИ:10,6-29,9). Ассоциации микроорганизмов у жителей Гвинейской Республики всегда содержали Staphylococcus aureus. Выявлены отличия в сравниваемых группах в отношении Staphylococcus aureus и Hafnia alvei, однако необходимо проведение дальнейших исследований на большей выборке.

Ключевые слова: микробиота кишечника, Гвинейская Республика, Enterobacteriaceae, Hafnia alvei, Comamonas kerstersii, Staphylococcus aureus, Escherichia свli, Enterococcus spp.

Introduction

At present, the importance of bacteria for life, normal development and full functioning of the human body is beyond doubt. It has been proved by numerous studies of both Russian and foreign authors [2, 3, 10, 17, 19]. In the gastrointestinal tract (GIT) of a healthy person, as a result of a long joint evolution, a complex multicomponent ecological system that contains a large number of various types of bacteria and is called a "microbiome" was formed [2]. Its functional state, species composition, quantitative characteristics are influenced by various biotic and abiotic factors: climatic, ecological, social, etc. Being an open system, a microbiome, on the one hand, has a certain stability, and on the other hand it is capable of changing under the influence of the above factors [7, 12]. The adaptive possibilities of microbiome depend not only on external influences, but also are

closely related to the individual genetic characteristics of the macroorganism, the state of its immune system. At present, it has been shown that disruption of the well-functioning of intestinal microbiocenosis plays a leading role in the emergence and development of many pathological processes, both infectious and non-infectious [1, 9, 10, 23, 27].

The composition of the intestinal microbiome is formed from the first days of a newborn's life, varies depending on the age and nature of nutrition [1, 4]. As the development of age processes in humans, the composition of microorganism associations in the intestine changes (the content of Bifidobacterium spp., Lactobacillus spp., etc. decreases) [8].

Dysbiosis, the quantitative and qualitative disturbance of homeostasis of the intestinal microbiome, as already mentioned above, plays an important role in the pathogenesis of various diseases [13]. In this case, the dysbiotic states, depending on the degree

of disturbances in the composition of the microbiome, and the intensity and duration of the reasons that cause them, can either disappear due to the inclusion of compensatory mechanisms, or grow to a pathological stage requiring specific therapy.

A lot of work has been devoted to the study of the microbiome of the intestine, both in children and in adults. Thanks to the research conducted within the framework of the Human Microbiome Project, the participants were able to compile a comprehensive understanding of the diversity of microorganisms inhabiting the biotopes of the human body. The results of genetic analysis showed that in the human body there are over 10 thousand species of various microorganisms, and the most colonized organ is the intestine: the number of bacteria varies from 10—103 cells in 1.0 gram in the small intestine to 1012 in the large intestine [5].

It is noted that the microbiome of the intestine in clinically healthy people living in different regions and countries can vary significantly. For example, the distinctive features of the microbiome of children living in Mongolia, whose diet was dominated by meat products, was an excessive amount of Clostridium spp. against a pronounced deficiency of Lactobacillus spp., Bifidobacterium spp. and other anaerobic non-spore-forming bacteria. In children who lived in Russia and were on a mixed diet, the intestinal microbiome also showed a deficiency of Bifidobacterium spp. and Lactobacillus spp. However, in general, the content of these microorganisms was significantly higher than that of children living in Mongolia. At the same time, various species of Enterobacteriaceae, Staphylococcus spp., yeast-like fungi of the Candida genus were present in abundant quantities in children living in Russia. One third of the children living in Switzerland had an increase in Enterobacteriaceae, and 16.7% had no Enterococcus spp. and in 50% had a reduced amount of Bifidobacterium spp. [7].

In a study of healthy residents of Vietnam and Russia, it was found that Vietnamese residents' fecal samples contained more Enterobacteriaceae and less Lactobacillus spp. than Russians, apart from the differences in the species belonging to Enterococcus spp. [6]. The residents of Uganda, Japan, India had a lower

number of bacteroides than those living in Europe and America [21]. The peculiarities of microbiome in the residents of the highland and lowland regions of China, various regions of India, Indonesia, Japan, Mongolia and Hong Kong have been revealed [16, 18, 24, 25, 27].

The aim of the study was to carry out a comparative study of the qualitative and quantitative composition of the aerobic and anaerobic microbiome of the intestine in a random batch of feces samples from the residents of the Republic of Guinea (Conakry) and Russia (St. Petersburg).

Materials and methods

Laboratory studies were conducted in the laboratory of enteric infections of the St. Petersburg Pasteur Institute. 106 samples of feces were obtained from 46 residents of the Republic of Guinea (Conakry) aged 24—64 and from 60 residents of St. Petersburg aged 19—63. The qualitative and quantitative composition of microbial communities of the intestine was determined in the autumn-winter periods (December 2015, October 2016). The persons were clinically healthy and did not have a history of somatic and infectious diseases of the digestive tract during the 12 months preceding the study. A survey of food characteristics showed that the diet of the surveyed group of residents of the Republic of Guinea included a large number of local vegetables, fruits, cereals and a limited number of meat and, especially, natural dairy products. The surveyed group of residents of St. Petersburg followed a typical diet for our country with sufficient consumption of meat, dairy and plant products.

The content of microorganisms (bacteria of the Enterobacteriaceae family, Enterococcus spp., Lactobacillus spp., Bifidobacterium spp., Staphylococcus spp., yeast-like fungi of the Candida genus, non-fermenting gram-negative bacteria, etc.) in 1.0 gram of feces was determined by the bacteriological method. Russian selective and differential-diagnostic nutrient media were used to isolate and identify bacteria, according to the current regulatory documents. Generic and species identification was carried out using a bacteriological analyzer Vitek 2 Compact, routine bio-

Table 1. The degree of microbiota disorders of the gastrointestinal tract in the residents of the Republic of Guinea and Saint Petersburg

Comparable groups Number of samples, in which abnormalities were detected Degree of severity of microbiota disorders

1 2 3

Residents of St. Petersburg 52 abs. 17 30 5

% 32.7 57.7 9.6

95%CI 21.5-46.2 44.2-70.1 4.2-20.6

Residents of Guinea 46 abs. 9 28 9

% 19.6 60.8 19.6

95%CI 10.7-33.2 46.5-73.6 10.7-33.2

The value of x2 (df = 1) 2.158 0.102 1.973

Level of significance (P) > 0.05 > 0.05 > 0.05

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chemical tests, and MALDI-TOF mass spectrometry. For MALDI-TOF mass spectrometry, the bacterial cells from isolated colonies grown on differential diagnostic solid media for 18—24 hours of incubation were applied in a thin layer on the MALDI target wells, followed by lamination of 1 pl of the matrix, which is a saturated solution of a-cyano-4-hydroxycinnamic acid (Bruker Daltonics, Germany) in an aqueous solution of 50% acetonitrile and 2.5% trifluoroacetic acid (Sigma-Aldrich). Spectra of the samples were obtained in the linear positive mode of operation of the MALDI-TOF mass spectrometer "Microflex LRF" (Bruker Daltonics, Germany) using the "FlexCon-trol" 3.3 software (Bruker Daltonics, Germany). Prior to measurement, the instrument was calibrated using a bacterial test standard (Bruker Daltonics, Germany). The spectral profiles of the samples were the sum of ions obtained from 240 laser flares at different locations in each MALDI target well, performed automatically in the mass/charge range (m/c) from 2000 to 20 000 Da. Identification of the microorganisms was carried out using the "MALDI Biotyper RTC" software (Bruker Daltonics, Germany) by comparing the mass spectra of each test sample with the reference spectra data from the taxonomic base and calculating the coincidence coefficients represented as scores.

The degrees of microbiological disturbances were assessed according to the Industry Standard OST No. 91500.11.004-2003 "Protocol of patient management. Dysbacteriosis of the Intestine", Federal Clinical Recommendations "Determination of Dysbiotic Changes in the Gastrointestinal Tract by Markers of the Intestinal Content", 2015. In order to evaluate the differences in the results in the compared groups, the x2 Pearson criterion, p < 0.05 and Fisher's exact test, calculated using the on-line calculator medsta-tistica.ru, were used. 95% confidence intervals were calculated using the Wilson method.

Findings

According to OST No. 91500.11.004-2003 and FCG (Federal clinical guidelines) of 2015, the degree of microbiological disturbances is characterized by a decrease in the number of obligatory ones, an increase in the number of facultative (opportunistic pathogens) microorganisms (OPM) and the appearance of their associations. Using these criteria, dysbiotic disorders were detected in both compared groups: 100% (95% CI: 92.3-100) surveyed from the Republic of Guinea and 86.7% (95% CI: 75.8-93.1) surveyed from St. Petersburg (Table 1).

Minor deviations from the norm (the first degree of microbiological disorders) occurred in the group of St. Petersburg residents in 32.7% (95% CI: 21.546.2), in the group of residents of the Republic of Guinea in 19.6% (95% CI: 10.7-33.2). The changes revealed were characterized by a decrease in the amount of Bifidobacterium spp. (up to 108—107 CFU/g), Lactobacillus spp. (up to 106 CFU/g), "typical" Escherichia coli (up to 106 CFU/g).

Microbiota disorders corresponding to the second degree occurred in 60.8% (95% CI: 46.5-73.6) in the group of surveyed residents of the Republic of Guinea and in 57.7% (95% CI: 44.2-70.1 ) of the surveyed residents of St. Petersburg. Deviations from the norm were characterized by a decrease in the content of Bifidobacterium spp. (up to 107 CFU/g) and Lactobacillus spp. (up to 105 CFU/g), an imbalance in the quantitative and qualitative composition of Escherichia coli (the presence of "atypical" strains with hemolytic activity and not able to ferment lactose), as well as the appearance in the microbiome of OPM and their associations in an amount exceeding 105 CFU/g.

The third degree of microbiota disorders in the group of residents of the Republic of Guinea was found in 19.6% (95% CI: 10.7-33.2), in the St. Petersburg group in 9.6% (95% CI: 4.2-20.6).

The disorders were characterized by a pronounced decrease in the number of obligate bacteria (Bifidobacterium spp. — less than 107 CFU/g, Lactobacillus spp. — less than 105 CFU/g), an increase in the content of OPM and their associations in an amount of 106 CFU/g and higher. When comparing the prevalence of each of the three degrees of microbiota disorders between the population of the Republic of Guinea and the population of St. Petersburg, no differences were found, however, statistically significant differences in the distribution of the proportion of micro-biota disorders of various degrees were found within each population. Second degree disorders prevailed in the residents of the Republic of Guinea, the differences between the prevalence of disorders of the first and third degrees were not identified. In St. Petersburg residents, the prevalence of microbiota disorders of the third degree is significantly lower than the first and second degree, however, there is no difference between the prevalence of disorders of the first and second degree. At the same time, both in the residents of the Republic of Guinea and in St. Petersburg resi-

dents, the proportion of disorders of the third degree is significantly lower than the second degree.

Associations of OPM in different combinations were found in microbiome in 30.4% of the surveyed residents of the Republic of Guinea (95% CI: 19.144.8) and 18.3% of St. Petersburg residents (95% CI: 10.6-29.9). At the same time, OPM associations in the surveyed residents of the Republic of Guinea always contained Staphylococcus aureus.

Table 2 represents data on the number of samples corresponding to norm for the content of obligatory and facultative microorganisms, significant for determining the severity of dysbiotic conditions. In the compared groups, the proportion of samples corresponding to norm by the number of Bifidobacterium spp., Lactobacillus spp. and "typical" Escherichia coli, did not differ statistically significantly.

Statistically significant differences were detected in the number of samples corresponding to the norm for the content of Enterococcus spp.: in St. Petersburg residents — 81.6% (95% CI: 70.1-89.4), in the Republic of Guinea residents — 56.5% (95% CI: 42.2-69.8). Species composition of Enterococcus spp. was identical in both groups. Proportions of E. faecium and E. fae-calis were practically the same and amounted to 38.7% and 32.3%, respectively in the group of residents of St. Petersburg and 38.9% and 33.3% in the group of residents of the Republic of Guinea. In both groups there were isolated findings of other species (E. avium, E. durans, E. galinarum, E. hirae, E. casseliflavus).

Analysis of the content of facultative microorganisms revealed statistically significant differences in relation to some bacteria. In the group of surveyed residents of the Republic of Guinea, samples with "atypical" (hemolytic and lactose-negative) Escherichia coli exceeding the norm were more common: 43.5% (95% CI: 30.2-57.8) compared to 16.7% (95% CI: 9.3-28.0) in the group of residents of St. Petersburg. The nonfer-mentative gram-negative bacteria Comamonas kerster-

Table 3. The frequency of opportunistic pathogens detection in the feces of the residents of the Republic of Guinea and Saint Petersburg

Number of samples containing opportunistic pathogens

Comparable groups of residents: Total samples Klebsiella spp. Citrobacter spp. Enterobacter spp. Proteus spp. H. alvei Comamonas kerstersii S. aureus Candida spp.

abs. 12 3 5 0 1 1 10 9

St. Petersburg 60 % 20.0 5.0 8.3 0 1.7 1.7 16.7 15.0

95% CI 11.8-31.8 1.7-13.7 3.6-18.1 0.0-6.0 0.3-8.9 0.3-8.9 9.3-28.0 8.1-26.1

The Republic of Guinea abs. 12 4 4 1 6 8 16 7

46 % 26.1 8.7 8.7 2.2 13.0 17.4 34.8 15.2

95% CI 15.6-40.3 3.4-20.3 3.4-20.3 0.4-11.3 6.1-25.7 9.1-30.7 22.7-49.2 7.6-28.2

Fisher's exact test 0.48992 0.46430 1.00 0.43396 0.04111 0.0096 0.04096 1.00

sii were detected in 17.4% (95% CI: 9.1-30.7) of residents from the Guinean Republic and 1.7% (95% CI: 0.3-8.9) of residents from St. Petersburg (Table 3).

There were no statistically significant differences in the prevalence of facultative opportunistic pathogenic Enterobacteria among residents of St. Petersburg and the Republic of Guinea: Klebsiella spp. — 20.0% (95% CI: 11.8-31.8) and 26.1% (95% CI: 15.6-40.3), Citro-bacter spp. — 5.0% (95% CI: 1.7-13.7) and 8.7% (95% CI: 3.4-20.3), Enterobacter spp. — 8.3% (95% CI: 3.6-18.1) and 8.7% (95% CI: 3.4-20.3), Proteus spp. — 0% (95% CI: 0.0-6.0) and 2.2% (95% CI: 0.4-11.3), Clostridium spp. — 25.0% (95% CI: 15.8-37.2) and 19.6% (95% CI: 10.7-33.2), Candida spp. — 15.0% (95% CI: 8.1-26.1) and 15.2% (95% CI: 7.6-28.2), respectively.

It was found that Staphylococcus aureus and Hafnia alvei were more common in the group of residents of the Republic of Guinea, but when the results were projected for the population, the differences were statistically insignificant: Staphylococcus aureus 34.8% (95% CI: 22.7-49.2) and 16.7% (95% CI: 9.3-28.0); Hafnia alvei — 13.0% (95% CI: 6.1-25.7) and 1.7% (95% CI: 0.3-8.9).

Discussion

The human society is constantly confronted with various new problems, despite progress in many areas of medical science and health. One of such problems at present is the violation of the microbial balance of the gastrointestinal tract, leading to the dysbiotic states of the human body. Analysis of the microbiome of the gastrointestinal tract in healthy people living in different regions of the world, presented in the works of many researchers, have shown significant variations in its quantitative and qualitative composition [11, 14, 15, 16, 17, 18, 20, 24, 25, 26, 27].

The results of our pilot project showed that in compared groups of practically healthy people in St. Petersburg, who had a relatively balanced diet with a predominance of animal proteins, and residents of the Republic of Guinea, who had a predominant prevalence of vegetables and cereals in the diet, significant differences in the content of obligate bacteria (Bifi-dobacterium spp. and Lactobacillus spp.), responsible for colonization resistance (one of the most important factors of the anti-infection protection system), have not been identified. According to our data, the prevalence of microbiota disorders of varying severity was noted with equal frequency among residents of the

Список литературы/References

Republic of Guinea and among residents of St. Petersburg. Moreover, within each population, statistically significant differences in the distribution of the proportion of microbiota disorders of various degrees were found. Both in the residents of the Republic of Guinea and the residents of St. Petersburg, the proportion of disorders of the third degree was detected less frequently, compared with the proportion of disorders of the second degree.

Reliable differences in the species composition of the facultative part of the microbiome are revealed. "Atypical" Escherichia coli (hemolytic and lactose-negative) and non-fermenting gram-negative bacteria Comamonas kerstersii are more often found in the residents of the Republic of Guinea.

We obtained differences in the compared groups for Staphylococcus aureus and Hafnia alvei (Fisher's exact test of 0.04096 and 0.04111, respectively), however, when projecting the results to population, the differences were statistically insignificant, further research on a larger population is necessary. It should be noted that these bacteria belong to the OPM and sanitary indicator microorganisms. Under certain conditions, any OPM can cause human diseases, especially in people with weakened immunity (purulent-septic infections, food poisoning, etc.) On the other hand, the presence of these bacteria in the digestive tract may reflect the characteristics of the macroorganism's habitat. This is confirmed by the example of our data on the content of Comamonas kerstersii in the digestive tract in a group of surveyed residents of the Republic of Guinea. For these microorganisms, the ecological niche is the environment: according to the literature sources, strains of Comamonas spp. were often identified in the study of samples of swampy soil and water environment, washings from fruit and vegetables, plankton, termites gut, etc. Comamonas kerstersii is often present in micro-bial communities associated with natural biocenoses and biodegradation processes [28]. More frequent findings of Comamonas kerstersii and "atypical" Escherichia coli characterize the microbiome of the gastrointestinal tract of the residents of the Republic of Guinea. It can be assumed that this is due to the humid tropical climate, low socio-economic level, and also the predominance of local vegetables and fruits in the diet.

Acknowledgements

The authors are grateful to Marina Sofronova for her advice in writing the article.

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Авторы:

Попова А.Ю., д.м.н., профессор, Главный государственный санитарный врач Российской Федерации, руководитель Федеральной службы по надзору в сфере защиты прав потребителей и благополучия человека (Роспотребнадзор), Москва, Россия;

Кафтырева Л.А., д.м.н., профессор, зав. лабораторией кишечных инфекций ФБУН НИИ эпидемиологии и микробиологии имени Пастера, Санкт-Петербург, Россия; Сужаева Л.В., младший научный сотрудник лаборатории кишечных инфекций ФБУН НИИ эпидемиологии и микробиологии имени Пастера, Санкт-Петербург, Россия; Войтенкова Е.В., к.м.н., старший научный сотрудник лаборатории кишечных инфекций ФБУН НИИ эпидемиологии и микробиологии имени Пастера, Санкт-Петербург, Россия; Забровская А.В., к.в.н., старший научный сотрудник лаборатории кишечных инфекций ФБУН НИИ эпидемиологии и микробиологии имени Пастера, Санкт-Петербург, Россия; Егорова С.А., к.м.н., старший научный сотрудник лаборатории кишечных инфекций ФБУН НИИ эпидемиологии и микробиологии имени Пастера, Санкт-Петербург, Россия; Макарова М.А., к.м.н., старший научный сотрудник лаборатории кишечных инфекций ФБУН НИИ эпидемиологии и микробиологии имени Пастера, Санкт-Петербург, Россия; Матвеева З.Н., к.м.н., ведущий научный сотрудник лаборатории кишечных инфекций ФБУН НИИ эпидемиологии и микробиологии имени Пастера, Санкт-Петербург, Россия; Зуева Е.В., к.б.н., старший научный сотрудник лаборатории молекулярной иммунологии ФБУН НИИ эпидемиологии и микробиологии имени Пастера, Санкт-Петербург, Россия; Порин А.А., к.м.н., научный сотрудник лаборатории кишечных инфекций ФБУН НИИ эпидемиологии и микробиологии им. Пастера, Санкт-Петербург, Россия; Буаро М.И., к.б.н., профессор, генеральный директор Института Пастера Гвинеи, г. Киндия, Гвинейская Республика; Константинов О.К., к.б.н., научный сотрудник Института Пастера Гвинеи, г. Киндия, Гвинейская Республика; Тотолян Арег А., академик РАН, д.м.н., профессор, зав. лабораторией молекулярной иммунологии, директор ФБУН НИИ эпидемиологии и микробиологии имени Пастера, Санкт-Петербург, Россия.

Поступила в редакцию 31.08.2017 Принята к печати 20.09.2017

Authors:

Popova A.Yu., PhD, MD (Medicine), Professor, Chief State Sanitary

Physician of the Russian Federation, Head of Federal Service

for Surveillance on Consumer Rights Protection and Human

Wellbeing (Rospotrebnadzor), Moscow, Russian Federation;

Kaftyreva L.A., PhD, MD (Medicine), Professor, Head of the

Laboratory of Enteric Infections, St. Petersburg Pasteur Institute,