Аннотация
Представлена характеристика спектра и количества газовых сигнальных молекул, выделяемых стафилококками влагалища
у пациенток с досрочным преждевременным разрывом плодных оболочек (ПРПО) в сроке гестации 24,0-33 недель 6 дней в
зависимости от остаточного объёма околоплодных вод. Стафилококки, выделенные из влагалищной микробиоты представлены видами S. epidermidis, S. aureus, S. haemoliticus, S. xylosis. Спектр газовых сигнальных молекул, продуцируемых и
потребляемых стафилококками влагалища у пациенток с маловодием при досрочном ПРПО отличался в два раза меньшим
выделением азота (p=0,009), в 50 раз меньшим выделением сероводорода (р<0,001), при сравнении с аналогичными показателями у пациенток без маловодия, выделением оксида азота в группе с маловодием при его поглощении в группе с нормальным
остаточным объёмом околоплодных вод.
Annotation
The paper characterizes the spectrum and the amount of gas signaling molecules secreted by vaginal Staphylococci in patients upon
preterm premature rupture of membranes (PPROM) at 24.0–33.6 gestation weeks depending on the residual amount of the amniotic
fluid. The Staphylococci isolated from the vaginal microbiota were represented by S. epidermidis, S. aureus, S. haemoliticus, S. xylosis.
The spectrum of gas signaling molecules produced and consumed by the vaginal Staphylococci in patients with oligohydramnios upon
PPROM was characterized by two times less nitrogen excretion (p=0.009), by 50 times less hydrogen sulfide excretion (р<0.001),
compared to similar indicators in patients without oligohydramnios, as well as by nitrogen oxide excretion in the group with oligohydramnios upon its absorption in the group with the normal residual amount of the amniotic fluid.
Key words: microbiota; Staphylococci; preterm premature rupture of membranes (PPROM); oligohydramnios; gas
signaling molecules
Список литературы
ЛИТЕРАТУРА
1. Сухих Г.Т., Серов В.Н., Адамян Л.В. Филиппов О.С., Баев О.Р.,
Клименченко Н.И., и др. Преждевременные роды. Проблемы репродукции. 2015; 21 (прил. 6): 55-78.
2. Šket T., Železnik Ramuta T., Starčič Erjavec M., Erdani Kreft M.
The role of innate immune system in the human amniotic membrane
and human amniotic fluid in protection against intra-amniotic infections and inflammation. Front. Immunol. 2021; 12: 735324. DOI:
10.3389/fimmu.2021.735324.2021.
3. Moore T.R. The role of amniotic fluid assessment in evaluating fetal
well-being. Clin. Perinatol. 2011; 38 (1): 33-46. DOI: 10.1016/j.
clp.2010.12.005.
4. Боярский К.Ю., Кахиани Е.И. Микробиом репродуктивной системы человека. Проблемы репродукции. 2019; 25 (4): 34. DOI:
10.17116/repro201925041.
5. Buchta V. Vaginal microbiome. Ceska gynekol. 2018; 83(5): 371-9.
6. Mendling W. Vaginal Microbiota. Adv. Exp. Med. Biol. 2016; 902:
83-93. DOI: 10.1007/978-3-319-31248-4_6.
7. Зебзеева С.Ю., Стольникова И.И., Червинец Ю.В., Червинец
В.М. Характеристика вагинального микробиома пациенток с
привычным невынашиванием беременности. Вестник Национального медико-хирургического Центра им. Н.И. Пирогова.
2023; 18 (2): 74-8.
8. Kumar M., Murugesan S., Singh P., Saadaoui M., Elhag D.A., Terranegra A. Vaginal microbiota and cytokine levels predict preterm
delivery in Asian women. Front. Cell Infect. Microbiol. 2021; 4 (11):
639-65. DOI: 10.3389/fcimb.2021.639665.
9. Saraf V.S., Sheikh S.A, Ahmad A., Gillevet P.M., Bokhari H., Javed
S. et.al. Vaginal microbiome: normalcy vs dysbiosis. Arch. Microbiol.
2021; 203 (7): 3793-3802. DOI: 10.1007/s00203-021-02414-3.
10. Whidbey C., Vornhagen J., Gendrin C., Boldenow E., Samson J.M.,
Doering K. et. al. A streptococcal lipid toxin induces membrane
permeabilization and pyroptosis leading to fetal injury. EMBO Mol.
Med. 2015; 7 (4): 488-95. DOI: 10.15252/emmm.201404883.
11. Singh N., Pattnaik L., Panda S. R., Jena P., Panda J. Fetomaternal
outcomes in women affected with preterm premature rupture of membranes: an observational study from a tertiary care center in Eastern
India. Cureus. 2022; 14 (5): e25533. DOI: 10.7759/cureus.25533.
12. Velemínský M., Tosner J. Relationship of vaginal microflora to
PROM, pPROM and the risk of early-onset neonatal sepsis. Neur. Endocrinol. Lett. 2008; 29 (2): 205-21.
13. Кунгурцева Е.А., Джиоев Ю.П., Попкова С.М., Лещенко О.Я., Загвозкина А.В. Патогенный потенциал и взаимовлияние микрофлоры слизистых оболочек открытых полостей различных биотопов у женщин как важные факторы их репродуктивного здоровья. Acta Biomedica Scientifica. 2014; 100 (6): 63-7.
14. Sparvoli L.G., Cortez R.V., Daher S., Padilha M., Sun S.Y., Nakamura M.U. Women’s multisite microbial modulation during pregnancy. Microb. Pathog. 2020; 147: 104230. DOI: 10.1016/j.micpath.2020.104230.
15. Gonçalves B., Fernandes L., Henriques M., Silva S. Environmental
pH modulates biofilm formation and matrix composition in Candida
albicans and Candida glabrata. Biofouling. 2020; 36 (5): 621-30.
DOI: 10.1080/08927014.2020.1793963.
16. Mukherjee S., Bassler B.L. Bacterial quorum sensing in complex and
dynamically changing environments. Nat. Rev. Microbiol. 2019; 17
(6): 371-82. DOI: 10.1038/s41579-019-0186-5.
17. Червинец В.М., Червинец Ю.В., Беляева Е.А., Петрова О.А., Ганина Е.Б. Метаболическая активность высокоантагонистических
штаммов лактобацилл здорового человека. Журнал микробиологии, эпидемиологии и иммунобиологии. 2018; 4: 11-7.
18. Rengarajan A., Mauro A., Boeldt D. S. Maternal disease and gasotransmitters. Nitric. Oxide. 2020; 1 (96): 1-12. DOI: 10.1016/j.
niox.2020.01.001.
19. Yeruva T., Lee C. H. Regulation of Vaginal Microbiome by Nitric
Oxide. Curr. Pharm. Biotechnol. 2019; 20 (1): 17-31. DOI: 10.2174
/1389201020666190207092850.
20. Guerra D.D., Hurt K.J. Gasotransmitters in pregnancy: from
conception to uterine involution. Biol. Reprod. 2019; 101 (1): 4-25.
DOI: 10.1093/biolre/ioz038.
21. Rengarajan A., Mauro A. K., Boeldt D.S. Maternal disease and
gasotransmitters. Nitric. Oxide. 2020; 1 (96): 1-12. DOI: 10.1016/j.
niox.2020.01.001.
22. Ncib K., Bahia W., Leban N. Microbial diversity and pathogenic
properties of microbiota associated with aerobic vaginitis in women
with recurrent pregnancy loss. Diagnostics (Basel). 2022; 12 (10):
24-44. DOI: 10.3390/diagnostics12102444.
23. Досова С.Ю. Роль вагинального микробиома в патогенезе привычного невынашивания беременности. Тверской медицинский
журнал. 2020; (2): 8-10.
24. Sutton E.F, Gemmel M., Powers R.W. Nitric oxide signaling in pregnancy and preeclampsia. Nitric. Oxide. 2020; 95 (1): 55-62. DOI:
10.1016/j.niox.2019.11.006.
25. Banerji R., Kanojiya P., Saroj S.D. Role of interspecies bacterial communication in the virulence of pathogenic bacteria. Crit. Rev. Microbiol. 2020; 46 (2): 136-46. DOI: 10.1080/1040841X.2020.1735991.
26. Lev-Sagie A., De Seta F., Verstraelen H., Ventolini G., LonneeHoffmann R., Vieira-Baptista P. et. al. The vaginal microbiome: II.
Vaginal dysbiotic conditions. J. Low Genit. Tract. Dis. 2022; 26 (1):
79-84. DOI: 10.1097/LGT.0000000000000644.
27. Ganguly A., Ofman G., Vitiello P.F. Hydrogen sulfide-clues from
evolution and implication for neonatal respiratory diseases. Children
(Basel). 2021; 8 (3): 213. DOI: 10.3390/children8030213.
28. Helms C., Kim-Shapiro D.B. Hemoglobin-mediated nitric oxide
signaling. Free Radic. Biol. Med. 2013; 61: 464–72.
29. Curieses Andrés C.M, Pérez de la Lastra J.M. Chemistry of hydrogen
sulfide-pathological and physiological functions in mammalian cells.
Cells. 2023; 12 (23): 2684. DOI: 10.3390/cells12232684.
30. Menon R., Boldogh I., Hawkins H.K., Woodson M., Polettini
J., Syed T.A. et.al. Histological evidence of oxidative stress and
premature senescence in preterm premature rupture of the human
fetal membranes recapitulated in vitro. Am. J. Pathol. 2014; 184 (6):
1740–51. DOI: 10.1016/j.ajpath.2014.02.011.
31. Yuan B., Ohyama K., Takeichi M., Toyoda H. Direct contribution of
inducible nitric oxide synthase expression to apoptosis induction in
primary smooth chorion trophoblast cells of human fetal membrane
tissues. Int. J. Biochem. Cell Biol. 2009; 41 (5): 1062–9. DOI:
10.1016/j.biocel.2008.09.031.
32. Polettini J., Richardson L.S., Menon R. Oxidative stress induces
senescence and sterile inflammation in murine amniotic cavity.
Placenta. 2018; 63: 26–31. DOI: 10.1016/j.placenta.2018.01.009.
33. Dutta E.H., Behnia F., Boldogh I. Oxidative stress damage-associated
molecular signaling pathways differentiate spontaneous preterm birth
and preterm premature rupture of the membranes. Mol. Hum. Reprod.
2016; 22 (2): 143-57. DOI: 10.1093/molehr/gav074.
REFERENCES
1. Sukhikh G.Т., Serov V.N., Аdamyan L.V., Filippov О.S., Baev O.R.,
Klimenchenko N.I. Preterm labor. Problemy reproduktsii. 2015; 21
(Suppl.6): 55-78. (in Russian)
2. Šket T., Železnik Ramuta T., Starčič Erjavec M., Erdani Kreft M. The
Role of innate immune system in the human amniotic membrane and
human amniotic fluid in protection against intra-amniotic infections
and inflammation. Front. Immunol. 2021; 12: 735324. DOI: 10.3389/
fimmu.2021.735324.2021.
3. Moore T.R. The role of amniotic fluid assessment in evaluating fetal
well-being. Clin. Perinatol. 2011; 38 (1): 33-46. DOI: 10.1016/j.
clp.2010.12.005.
4. Boyarskiy K.Y., Кakhiani Е.I. Мicrobiome of human reproductive
system. Problemy reproduktsii. 2019; 25 (4): 34. DOI: 10.17116/
repro201925041. (in Russian)
5. Buchta V. Vaginal microbiome. Ceska gynekol. 2018; 83 (5): 371-9.
6. Mendling W. Vaginal Microbiota. Adv. Exp. Med. Biol. 2016; 902:
83-93. DOI: 10.1007/978-3-319-31248-4_6.
7. Zebzeeva S.Yu., Stol`nikova I.I., Chervinets Yu.V., Chervinets V.M.
Characteristics of the vaginal microbiome of patients with habitual
miscarriage. Vestnik Natsional`nogo mediko-khirurgicheskogo tsentra imeni N.I. Pirogova. 2023; 18 (2):74-8. (in Russian)
8. Kumar M., Murugesan S., Singh P., Saadaoui M., Elhag D.A., Terranegra A. Vaginal microbiota and cytokine levels predict preterm
delivery in Asian women. Front. Cell Infect. Microbiol. 2021; 4 (11):
639-65. DOI: 10.3389/fcimb.2021.639665.
9. Saraf V.S., Sheikh S.A., Ahmad A., Gillevet P.M., Bokhari H., Javed
S. et.al. Vaginal microbiome: normalcy vs dysbiosis. Arch. Microbiol.
2021; 203 (7): 3793-3802. DOI: 10.1007/s00203-021-02414-3.
10. Whidbey C., Vornhagen J., Gendrin C., Boldenow E., Samson J.M.,
Doering K. et. al. A streptococcal lipid toxin induces membrane permeabilization and pyroptosis leading to fetal injury. EMBO Mol. Med.
2015; 7 (4) 488-95. DOI: 10.15252/emmm.201404883.
11. Singh N., Pattnaik L., Panda S.R., Jena P., Panda J. Fetomaternal outcomes in women affected with preterm premature rupture of membranes: an observational study from a certiary care center in Eastern
India. Cureus. 2022; 14 (5): e25533. DOI: 10.7759/cureus.25533.
12. Velemínský M., Tosner J. Relationship of vaginal microflora to
PROM, pPROM and the risk of early-onset neonatal sepsis. Neur. Endocrinol. Lett. 2008; 29 (2): 205-21.
13. Kungurtseva E.A., Dzhioev Y.P., Popkova S.M., Leschenko О.Yacroflora of mucous membranes of open cavities of different biotopes
in women as important factors of their reproductive health. Acta Biomedica Scientifica. 2014; 100 (6): 63-7. (in Russian)
14. Sparvoli L.G., Cortez R.V., Daher S. Padilha M., Sun S.Y., Nakamura M.U. Women’s multisite microbial modulation during pregnancy. Microb. Pathog. 2020; 147: 104230. DOI: 10.1016/j.micpath.2020.104230.
15. Gonçalves B., Fernandes L., Henriques M., Silva S. Environmental
pH modulates biofilm formation and matrix composition in Candida
albicans and Candida glabrata. Biofouling. 2020; 36 (5): 621-30.
DOI: 10.1080/08927014.2020.1793963.
16. Mukherjee S., Bassler B.L. Bacterial quorum sensing in complex and
dynamically changing environments. Nat. Rev. Microbiol. 2019; 17
(6): 371-82. DOI: 10.1038/s41579-019-0186-5.
17. Chervinets V.M., Chervinets Yu.V., Belyaeva Е.А., Petrova O.A.,
Ganina E.B. Metabolic activity of high-antagonistic strains of lactobacilli isolated from healthy people. Zhurnal mikrobiologii, epidemiologii i immunobiologii. 2018; 4: 11-7. (in Russian)
18. Rengarajan A., Mauro A., Boeldt D. S. Maternal disease and gasotransmitters. Nitric Oxide. 2020; 1 (96): 1-12. DOI: 10.1016/j.
niox.2020.01.001.
19. Yeruva T., Lee C.H. Regulation of Vaginal Microbiome by Nitric Oxide. Curr. Pharm. Biotechnol. 2019; 20 (1): 17-31. DOI: 10.2174/1
389201020666190207092850.
20. Guerra D.D., Hurt K.J. Gasotransmitters in pregnancy: from conception to uterine involution. Biol. Reprod. 2019; 101 (1): 4-25. DOI:
10.1093/biolre/ioz038.
21. Rengarajan A., Mauro A. K., Boeldt D.S. Maternal disease and gasotransmitters. Nitric Oxide. 2020; 1 (96): 1-12. DOI: 10.1016/j.
niox.2020.01.001.
22. Ncib K., Bahia W., Leban N. Microbial diversity and pathogenic
properties of microbiota associated with aerobic vaginitis in women
with recurrent pregnancy loss. Diagnostics (Basel). 2022; 12 (10): 24-
44. DOI: 10.3390/diagnostics12102444.
23. Dosova S.Y. The role of vaginal microbiome in the pathogenesis of
habitual miscarriage. Tverskoy meditsinskiy zhurnal. 2020; 2: 8-10.
(in Russian)
24. Sutton E.F., Gemmel M., Powers R.W. Nitric oxide signaling in pregnancy and preeclampsia. Nitric. Oxide. 2020; 95 (1): 55-62. DOI:
10.1016/j.niox.2019.11.006.
25. Banerji R., Kanojiya P., Saroj S.D. Role of interspecies bacterial communication in the virulence of pathogenic bacteria. Crit. Rev. Microbiol. 2020;46 (2): 136-46. DOI: 10.1080/1040841X.2020.1735991.
26. Lev-Sagie A., De Seta F., Verstraelen H., Ventolini G., Lonnee-Hoffmann R., Vieira-Baptista P. et. al. The vaginal microbiome: II. Vaginal
dysbiotic conditions. J. Low Genit. Tract. Dis. 2022; 26 (1):79-84.
DOI: 10.1097/LGT.0000000000000644.
27. Ganguly A., Ofman G, Vitiello P.F. Hydrogen sulfide-clues from evolution and implication for neonatal respiratory diseases. Children (Basel). 2021; 8 (3): 213. DOI: 10.3390/children8030213.
28. Helms C., Kim-Shapiro D.B. Hemoglobin-mediated nitric oxide signaling. Free Radic. Biol. Med. 2013; (61):464–72.
29. Curieses Andrés C M, Pérez de la Lastra J.M., Chemistry of hydrogen
sulfide-pathological and physiological functions in mammalian cells.
Cells. 2023; 12(23): 2684. DOI: 10.3390/cells12232684.
30. Menon R., Boldogh I., Hawkins H.K., Woodson M., Polettini J., Syed
T.A. et.al. Histological evidence of oxidative stress and premature senescence in preterm premature rupture of the human fetal membranes
recapitulated in vitro. Am. J. Pathol. 2014; 184(6): 1740-51. DOI:
10.1016/j.ajpath.2014.02.011.
31. Yuan B., Ohyama K., Takeichi M., Toyoda H. Direct contribution
of inducible nitric oxide synthase expression to apoptosis induction
in primary smooth chorion trophoblast cells of human fetal membrane tissues. Int. J. Biochem. Cell Biol. 2009; 41(5): 1062-9. DOI:
10.1016/j.biocel.2008.09.031.
32. Polettini J., Richardson L.S, Menon R. Oxidative stress induces senescence and sterile inflammation in murine amniotic cavity. Placenta. 2018; 63: 26-31. DOI: 10.1016/j.placenta.2018.01.009.
33. Dutta E.H., Behnia F., Boldogh I. Oxidative stress damage-associated
molecular signaling pathways differentiate spontaneous preterm birth
and preterm premature rupture of the membranes. Mol. Hum. Reprod.
2016; 22(2): 143-57. DOI: 10.1093/molehr/gav074.