Comparative Genotyping of Staphylococcus aureus Strains Isolated from Skin Lesions, Nasal Cavities, and Feces of Children with Atopic Dermatitis

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Background: The lesion of skin of the majority atopic dermatitis patients is chronically colonized by bacteria belonging to the species Staphylococcus aureus. Topical antibacterial and anti-inflammatory therapy treatment are often ineffective due to fast recolonization by S. aureus and exacerbation of allergic process.

Aims: Our aim was to determine a frequency of S. aureus colonization in skin lesions, mucous membranes of the nasal cavity and intestine of children with atopic dermatitis, to compare the genotypes of Staphylococcus aureus strains isolated from different biotopes of atopic dermatitis patients, and to clarify whether the intestinal and nasal cavities microbiota may act as a source of S. aureus recolonization of skin lesions.

Materials and methods: Bacteriological examination of fecal samples, skin, and nasal swabs was conducted in 38 atopic dermatitis patients. The pure bacterial cultures of S. aureus were identified using API Staph (Biomerieux, France) and Vitek 2 MS (Biomerieux, France). Isolates of S. aureus were subjected to genotyping by analysis of rRNA internal 16S-23S rRNA spacer regions and high resolution melting analysis (HMR) of polymorphic spa X-regions.

Results: 99% S. aureus strains were successfully identified using MALDI-TOF mass-spectrometry. S. aureus cultures were isolated from all biotopes in 31,6% of children, from skin and nasal cavities — in 42% of cases, from skin and feces — in 2,6% of cases, only from skin — in 10,5%, from nasal cavities and feces — in 2,6%, and only from nasal cavities — in 2,6% of cases. In 8% of children, S. aureus was not detected in any of the biotopes. Genotyping of the isolates enabled the detection of 17 different genotypes. A match between the genotypes of skin and nasal strains, and skin and fecal strains was observed in 88% and 61% of the cases respectively.

Conclusions: The observed a high-frequency matching genotypes suggests the possibility of migration of S. aureus strains inside biotopes in humans and the absence of specialization to colonization of any of the niches.

About the authors

A. P. Pikina

Russian National Research Medical University

Author for correspondence.
ORCID iD: 0000-0001-7232-3288
Moscow Russian Federation

A. N. Shkoporov

Russian National Research Medical University


E. V. Kulagina

Engelhardt Institute of Molecular Biology, Russian Academy of Sciences

ORCID iD: 0000-0002-5381-1785

E. V. Khokhlova

Russian National Research Medical University


A. V. Chaplin

Russian National Research Medical University

ORCID iD: 0000-0003-1377-7153

N. N. Volodin

D. Rogachev Federal Research Center of Pediatric Hematology, Oncology and Immunology


L. I. Kafarskaya

Russian National Research Medical University


N. G. Korotkiy

Russian National Research Medical University


B. A. Efimov

Russian National Research Medical University



  1. Семенов В.Ю., Руголь Л.В., Матвеев Э.Н. Повозрастные показатели нуждаемости детского населения в специализированной стационарной медицинской помощи на примере Московской области // Социальные аспекты здоровья населения. ― 2010. ― T.16. ― №4 ― C. 10. [Semenov VYu, Rugol LV, Matveev EN. Age-related indicators of children population’s needs in the specialized stationary medical care by an example of the Moscow region. Sotsial’nye aspekty zdorov’ya naseleniya. 2010;16(4):10. (In Russ).]
  2. Bieber T. Atopic dermatitis. Ann Dermatol. 2010;22(2):125–137. doi: 10.5021/ad.2010.22.2.125.
  3. Leung DY. New insights into atopic dermatitis: role of skin barrier and immune dysregulation. Allergol Int. 2013;62(2):151−161. doi: 10.2332/allergolint.13-RAI-0564.
  4. Ефимов Б.А., Короткий Н.Г., Постникова Е.А. и др. Изучение качественного состава стафилококков кожи у больных атопическим дерматитом // Стерилизация и госпитальные инфекции. ― 2007. ― T.3. ― №5 ― C. 17–20. [Efimov BA, Korotkii NG, Postnikova EA, et al. Izuchenie kachestvennogo sostava stafilokokkov kozhi u bol’nykh atopicheskim dermatitom. Sterilizatsiya i gospital’nye infektsii. 2007;3(5):17−20. (In Russ).]
  5. Mempel M. Staphylococcus aureus and atopic eczema. In: Ring JPB, Przybilla B, Ruzicka T, editors. Handbook of atopic eczema. Berlin: Springer Science & Business; 2006. p. 406–409.
  6. Park HY, Kim CR, Huh IS, et al. Staphylococcus aureus colonization in acute and chronic skin lesions of patients with atopic dermatitis. Ann Dermatol. 2013;25(4):410–416. doi: 10.5021/ad.2013.25.4.410.
  7. Gilani SJ, Gonzalez M, Hussain I, et al. Staphylococcus aureus recolonization in atopic dermatitis: beyond the skin. Clin Exp Dermatol. 2005;30(1):10–13. doi: 10.1111/j.1365-2230.2004.01679.x.
  8. Elias PM, Schmuth M. Abnormal skin barrier in the etiopathogenesis of atopic dermatitis. Curr Allergy Asthma Rep. 2009;9(4):265–272. doi: 10.1007/s11882-009-0037-y.
  9. Arisawa T, Arisawa S, Yokoi T, et al. Endoscopic and histological features of the large intestine in patients with atopic dermatitis. J Clin Biochem Nutr. 2007;40(1):24–30. doi: 10.3164/jcbn.40.24.
  10. Stephens AJ, Inman-Bamber J, Giffard PM, Huygens F. Highresolution melting analysis of the spa repeat region of Staphylococcus aureus. Clin Chem. 2008;54(2):432–436. doi: 10.1373/clinchem.2007.093658.
  11. Gürtler V, Barrie HD, Mayall BC. Use of denaturing gradient gel electrophoresis to detect mutation in VS2 of the 16S-23S rDNA spacer amplified from Staphylococcus aureus isolates. Electrophoresis. 2001;22(10):1920−1924. doi: 10.1002/1522-2683(200106)22:10<1920::aid-elps1920>;2-0.
  12. Saruta K, Matsunaga T, Kono M, et al. Rapid identification and typing of Staphylococcus aureus by nested PCR amplified ribosomal DNA spacer region. FEMS Microbiol Lett. 1997;146(2):271–278. doi: 10.1016/s0378-1097(96)00487-9.
  13. Nomura F. Proteome-based bacterial identification using matrixassisted laser desorption ionization-time of flight mass spectrometry (MALDI-TOF MS): A revolutionary shift in clinical diagnostic microbiology. Biochim Biophys Acta. 2015;1854(6):528–537. doi: 10.1016/j.bbapap.2014.10.022.
  14. Zhu W, Sieradzki K, Albrecht V, et al. Evaluation of the Biotyper MALDI-TOF MS system for identification of Staphylococcus species. J Microbiol Methods. 2015;117:14–17. doi: 10.1016/j.mimet.2015.07.014.
  15. Good P. Permutation tests: a practical guide to resampling methods for testing hypotheses. Springer series in statistics. New York: Springer Science & Business Media; 2013. 228 p.
  16. Kim BS, Park JY, Song CH, et al. Clarifying the transmission route of Staphylococcus aureus colonizing the skin in early childhood atopic dermatitis. Ann Allergy Asthma Immunol. 2012;109(6):448–453. doi: 10.1016/j.anai.2012.09.015.
  17. Bonness S, Szekat C, Novak N, Bierbaum G. Pulsed-field gel electrophoresis of Staphylococcus aureus isolates from atopic patients revealing presence of similar strains in isolates from children and their parents. J Clin Microbiol. 2008;46(2):456–461. doi: 10.1128/JCM.01734-07.



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