Monitoring of distribution of antibiotic-resistant strains of microorganisms in patients with dysbiosis of the urogenital tract
AbstractCurrently, the problem of the development of resistance to drugs among microorganisms that colonize the urogenital system is becoming especially relevant due to broadly distributed dysbiotic conditions of the reproductive system of men and women. Therefore, there should be constant monitoring of the qualitative and quantitative composition of microbiota of the urogential tract and determination of the levels of antibiotic-resistance of strains of conditionally pathogenic microorganisms in the reproductive system of various layers of the population. We monitored 774,375 people of various age and sex – patients of the independent diagnostic laboratory INVITRO in the city Dnipro in 2017–2019. Among the examined people, 640,783 of the patients were diagnosed with the development of dysbiotic disorders, accounting for 82.7% of the total amount of the applications for medical help. According to the results of identification of the range of dysbiotic conditions of the urogenital system of patients of different ages and sexes, we determined the dominating role of facultative anaerobes in the development of dysbiotic impairments caused by colonizations by large numbers of conditionally-pathogenic microorganisms: in women, Gardnerella accounted for 86.1%, Staphylococcus – 63.2%, Streptococcus – 54.1%, Candida – 69.3%; in men, Streptococcus were found in 83.0%, Staphylococcus – 79.4%, Corynebacterium – 54.2% and Candida – 37.6% of the cases. Share of obligate anaerobes was also quite large: women were diagnosed with Prevotella in 59.7%, Peptostreptococcus in 53.2%, Fusobacterium in 45.4% of the cases cases; men were observed to have Peptostreptococcus 62.4%, Clostridium in 54.3%, Bacteroides in 32.5% of the cases. We determined high parameters of frequency of diagnosing antibiotic-resistant isolates of conditionally pathogenic microorganisms that circulate in the urogenital tract of patients with dysbiotic impairments, belonging to the following families: Mycoplasmataceae – 78.6%, Enterobacteriaceae – 56.0% and genera – Staphylococcus – 76.1%, Gardnerella – 24.3%, Corynebacterium – 21.2%. The research revealed increase in the frequency of detection of strains of urapathogenic bacteria resistant to the applied antibiotic preparations in 2018–2019 compared with the data of 2017: increases of 10.3% and 6.4% in representatives of family Mycoplasmataceae resistant to ciprofloxacin and ofloxacin respectively, 4.8% and 4.0% in Enterobacteriaceae resistant to chloramphenicol and ampicillin respectively, and 8.9% in the genus Staphylococcus resistant to vancomycin.
Abelson, B., Sun, D., Que, L., Nebel, R., Baker, D., Popiel, P., Amundsen, C., Chai, T., Close, C., DiSanto, M., Fraser, M., Kielb, S., Kuchel, G., Mueller, E., Palmer, M., Parker-Autry, C., Wolfe, A., & Damaser, M. (2018). Sex differences in lower urinary tract biology and physiology. Biology of Sex Differences, 9(1), 45.
Agar, A., Descalzi, B., Nally, M., Perez, D., & Christiansen, P. (2020). Urogenital dysbiosis: The importance of a complete immune/nutritional evaluation and the therapeutic intervention with probiotics, vitamins and minerals. World Allergy Organization Journal, 13(8), 100319.
Aragón, I., Herrera-Imbroda, B., Queipo-Ortuño, M., Castillo, E., Del Moral, J., Gómez-Millán, J., Yucel, G., & Lara, M. (2018). The Urinary tract microbiome in health and disease. European Urology Focus, 4(1), 128–138.
Bajic, P., Dornbier, R., Doshi, C., Wolfe, A., Farooq, A., & Bresler, L. (2019). Implications of the genitourinary microbiota in prostatic disease. Current Urology Reports, 20(7), 34.
Bitew, A., Abebaw, Y., Bekele, D., & Mihret, A. (2017). Prevalence of bacterial vaginosis and associated risk factors among women complaining of genital tract infection. International Journal of Microbiology, 2017, 4919404.
Boboia, A., Florea, L. S., Turcu-Stiolica, A., Tăerel, A. E., Rais, C., Revnic, C., Florea, A., Vedeanu, N. S., Nastasă, C., & Oniga, O. (2020). Decision analysis of antibiotic use. Farmacia, 68(4), 757–765.
Bondarenko, G., Dzhoraeva, S., Kondakova, A., Shcherbakova, I., Sobol, N., & Ivantsova, H. (2017). Main agents of opportunistic infections of genitourinary tracts and their antibiotic resistance. Eureka: Health Sciences, 1(3), 18–25.
Boujemaa, S., Mlik, B., Allaya, A. B., Mardassi, H., & Mardassi, B. B. A. (2020). Spread of multidrug resistance among Ureaplasma serovars, Tunisia. Antimicrobial Resistance and Infection Control, 9, 19.
Burnham, C. A. D., Leeds, J., Nordmann, P., O’Grady, J., & Patel, J. (2017). Diagnosing antimicrobial resistance. Nature Reviews Microbiology, 15, 697–703.
Ceccarani, C., Foschi, C., Parolin, C., D’Antuono, A., Gaspari, V., Consolandi, C., Laghi, L., Camboni, T., Vitali, B., Severgnini, M., & Marangoni, A. (2019). Diversity of vaginal microbiome and metabolome during genital infections. Scientific Reports, 9(1), 14095.
CLSI (2018). Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically. 11th ed. CLSI standart M07. Clinical and Laboratory Standarts Institute, Wayne.
Conway, R., Cook, S., & Soni, S. (2019). Antibiotic treatment of Mycoplasma genitalium infection. The Pharmaceutical Journal, 303, 7928.
Drago, F., Ciccarese, G., Rebora, A., Cordara, V., & Parodi, A. (2020). Common bacterial urogenital infections: A study on their aetiology and prevalence in a sexually transmitted infections centre. Journal of the European Academy of Dermatology and Venerology, 34(10), e630–e632.
Graspeuntner, S., Loeper, N., Künzel, S., Baines, J. F., & Rupp, J. (2018). Selection of validated hypervariable regions is crucial in 16S-based microbiota studies of the female genital tract. Scientific Reports, 8(1), 9678.
Ho, H., Tan, M., Chen, M., Tan, T., Koo, S., Koong, A., Ng, L., Hu, P., Tan, K., Moey, P., Koh, E., Wong, C., Lye, D., & Tan, N. (2019). Interaction between antibiotic resistance, resistance genes and treatment response for urinary tract infections in primary care. Journal of Clinical Microbiology, 57(9), e00143–19.
Kamińska, D., & Gajecka, M. (2017). Is the role of human female reproductive tract microbiota underestimated? Beneficial Microbes, 8(3), 327–343.
Karou, S., Djigma, F., Sagna, T., Nadembega, C., Zeba, M., Kabre, A., Anani, K., Ouermi, D., Gnoula, C., Pietra, V., Pignatelli, S., & Simpore, J. (2012). Antimicrobial resistance of abnormal vaginal discharges microorganisms in Ouagadougou, Burkina Faso. Asian Pacific Journal of Tropical Biomedicine, 2(4), 294–297.
Knight, G. M., Davies, N. G., Colijn, C., Coll, F., Donker, T., Gifford, D. R., Glover, R. E., Jit, M., Klemm, E., Lehtinen, S., Lindsay, J. A., Lipsitch, M., Llewelyn, M. J., Mateus, A., Robotham, J. V., Sharland, M., Stekel, D., Yakob, L., & Atkins, K. E. (2019). Mathematical modelling for antibiotic resistance control policy: Do we know enough? BMC Infectious Diseases, 19(1), 1011.
Koedooder, R., Mackens, S., Budding, A., Fares, D., Blockeel, C., Laven, J., & Schoenmakers, S. (2019). Identification and evaluation of the microbiome in the female and male reproductive tracts. Human Reproduction Update, 25(3), 298–325.
Kudinova, A. G., Soina, V. S., Maksakova, S. A., & Petrova, M. A. (2019). Basic antibiotic resistance of bacteria isolated from different biotopes. Microbiology, 88(6), 739–746.
Kulchavenya, E. (2020). The best rules for antimicrobial stewardship in urogenital tract infections. Current Opinion in Urology, 30(6), 838–844.
Lee, K., Song, H., & Kim, Y. (2020). The microbiome in urological diseases. Investigative and Clinical Urology, 61(4), 338–348.
Lewis, F., Bernstein, K., & Aral, S. (2017). Vaginal microbiome and its relationship to behavior, sexual health, and sexually transmitted diseases. Obstetrics and Gynecology, 129(4), 643–654.
Li, J., Chiu, P., & Ng, C. (2019). The impact of microbiome in urological diseases: A systematic review. International Urology and Nephrology, 51(10), 1677–1697.
Li, W., & Ma, Z. (2019). Diversity scaling of human vaginal microbial communities. Zoological Research, 40(6), 587–594.
Li, X., Chen, Y., Gao, W., Ye, H., Shen, Z., Wen, Z., & Wei, J. (2017). A 6-year study of complicated urinary tract infections in Southern China: Prevalence, antibiotic resistance, clinical and economic outcomes. Therapeutics and Сlinical Risk Management, 13, 1479–1487.
Machowska, A., & Lundborg, C. S. (2019). Drivers of irrational use of antibiotics in Europe. International Journal of Environmental Research and Public Health, 16(1), 27.
MacIntyre, D., Sykes, L., & Bennett, P. (2017). The human female urogenital microbiome: Complexity in normality. Emerging Topics in Life Sciences, 1(4), 363–372.
Magistro, G., & Stief, C. (2019). The urinary tract microbiome: The answer to all our open questions? European Urology Focus, 5(1), 36–38.
Martin, D., & Marrazzo, J. (2016). The vaginal microbiome: Current understanding and future directions. Journal of Infectious Diseases, 214(1), 36–41.
Mediati, D. G., Wu, S., Wu, W., & Tree, J. J. (2021). Networks of resistance: Small RNA control of antibiotic resistance. Trends in Genetics, 37(1), 35–45.
Muhleisen, A., & Herbst-Kralovetz, M. (2016). Menopause and the vaginal microbiome. Maturitas, 91, 42–50.
Neugent, M., Hulyalkar, N., Nguyen, V., Zimmern, P., & De Nisco, N. (2020). Advances in understanding the human urinary microbiome and its potential role in urinary tract. American Society for Microbiology, 11(2), e00218–20.
Ortega Martell, J. (2020). Immunology of urinary tract infections. GMS Infectious Diseases, 8(21), 1–6.
Oztekin, C., Kaya-Sezginer, E., Yilmaz-Oral, D., & Gur, S. (2018). Male urogenital disorders and metabolic syndrome: Possible links, characteristics and potential treatment strategies. Current Pharmaceutical Design, 24(9), 1019–1033.
Palchykov, V. A., Zazharskyi, V. V., Brygadyrenko, V. V., Davydenko, P. O., Kulishenko, O. M., Borovik, I. V., Chumak, V., Kryvaya, A., & Boyko, O. O. (2019). Bactericidal, protistocidal, nematodicidal properties and chemical composition of ethanol extract of Punica granatum peel. Biosystems Diversity, 27(3), 300–306.
Patwardhan, V., Kumar, D., Goel, V., & Singh, S. (2017). Changing prevalence and antibiotic drug resistance pattern of pathogens seen in community-acquired pediatric urinary tract infections at a tertiary care hospital of North India. Journal of Laboratory Physicians, 9(4), 264–268.
Rigo, G. V., & Tasca, T. (2020). Vaginitis: Review on drug resistance. Current Drug Targets, 21(16), 1672–1686.
Saad, D., Gameel, S., Ahmed, S., Basha, E., Osman, M., & Khalil, E. (2020). Etiological agents of urinary tract infection and 7 years trend of antibiotic resistance of bacterial uropathogens in Sudan. The Open Microbiology Journal, 14, 312–320.
Schuppe, H., Pilatz, A., Hossain, H., Diemer, T., Wagenlehner, F., & Weidner, W. (2017). Urogenital infection as a risk factor for male infertility. Deutsches Arzteblatt International, 114(19), 339–346.
Shaskolskiy, B., Dementieva, E., Leinsoo, A., Runina, A., Vorobyev, D., Plakhova, X., Kubanov, A., Deryabin, D., & Gryadunov, D. (2016). Drug resistance mechanisms in bacteria causing sexually transmitted diseases and associated with vaginosis. Frontiers in Microbiology, 7, 747.
Shoskes, D., Altemus, J., Polackwich, A., Tucky, B., Wang, H., & Eng, C. (2016). The urinary microbiome differs significantly between patients with chronic prostatitis/chronic pelvic pain syndrome and controls as well as between patients with different clinical phenotypes. Urology, 92, 26–32.
Sirichoat, A., Lulitanond, A., Kanlaya, R., Tavichakorntrakool, R., Chanawong, A., Wongthong, S., & Thongboonkerd, V. (2016). Phenotypic characteristics and comparative proteomics of Staphylococcus aureus strains with different vancomycin-resistance levels. Diagnostic Microbiology and Infectious Disease, 86(4), 340–344.
Solís-Martínez, R., Vázquez-Castillo, T., Celis, S., & Hernández-Callejas, L. (2006). Susceptibilidad de Mycoplasma hominis y Ureaplasma urealyticum ante diferentes antibióticos. Revista Medica de la Universidad Veracruzana, 6(2), 11–17.
Song, S., Acharya, K., Zhu, J., Deveney, C., Walther-Antonio, M., Tetel, M., & Chia, N. (2020). Daily vaginal microbiota fluctuations associated with natural hormonal cycle, contraceptives, diet and exercise. MSphere, 5(4), e00593–20.
Stout, M., Wylie, T., Gula, H., Miller, A., & Wylie, K. (2020). The microbiome of the human female reproductive tract. Current Opinion in Physiology, 13, 87–93.
Tang, J. (2017). Microbiome in the urinary system – a review. AIMS Microbiology, 3(2), 143–154.
Tran, K., & Rybak, M. (2018). Beta-lactams combinations with vancomycin provide synergy against VSSA, hVISA, and VISA. Antimicrobial Agents and Chemotherapy, 62(6), e00157.
Valentine-King, M., & Brown, M. (2017). Antibacterial resistance in Ureaplasma species and Mycoplasma hominis isolates from urine cultures in college-aged females. Antimicrobial Agents and Chemotherapy, 61(10), e01104-17.
Wagenlehner, F. (2020). Urogenital infections. World Journal of Urology, 38(1), 1–2.
Xu, J., Bian, G., Zheng, M., Lu, G., Chan, W., Li, W., & Du, Y. (2020). Fertility factors affect the vaginal microbiome in women of reproductive age. American Journal of Reproductive Immunology, 83(4), e13220.
Zazharskyi, V. V., Davydenko, P. О., Kulishenko, O. М., Borovik, I. V., & Brygadyrenko, V. V. (2019). Antimicrobial activity of 50 plant extracts. Biosystems Diversity, 27(2), 163–169.
Zazharskyi, V. V., Davydenko, P. О., Kulishenko, O. М., Borovik, I. V., Zazharska, N. M., & Brygadyrenko, V. V. (2020). Antibacterial and fungicidal activities of ethanol extracts of 38 species of plants. Biosystems Diversity, 28(3), 281–289.
Zheng, W., Zhang, W., Cui, D., Nie, Z., Ding, B., Cheng, J., & Mei, C. (2021). Examination of Ureaplasma urealyticum and Mycoplasma hominis in 4082 Chinese patients. Brazilian Journal of Medical and Biological Research, 54(2), e10099.
Copyright (c) 2021 Regulatory Mechanisms in Biosystems
This work is licensed under a Creative Commons Attribution 4.0 International License.
Authors retain copyright and grant the journal right of first publication with the work simultaneously licensed under a Creative Commons «Attribution» 4.0 License that allows others to share the work with an acknowledgement of the work's authorship and initial publication in this journal.