Antimicrobial Resistance and Virulence of Staphylococcus spp. in patients from oncologic and non oncologic hospitals of Recife City/PE




Staphylococcus; Antibiotic resistance; Oncology; Virulence.


Staphylococcus spp. is one of the major infection-associated bacteria within health care, especially in intensive care units, and one of principal cause of complication in cancer patients. This study compared the antimicrobial susceptibility profile and frequency of resistance (mecA, blaZ, ermA and ermC) and virulence (icaA, icaD and hlg) genes in Staphylococcus spp. from patients of Oncology Hospital (OH) and University Hospital (UH). The type of the ccr complex was assessed by PCR among the mecA positive isolates from the UH. Higher percentage of susceptible isolates, except for oxacillin and cefoxitin was found among the UH isolates and 27,3% vancomycin-resistant isolates were identified through the screening spot; 41 isolates displayed the MLSBc phenotype and five the MSLBi phenotype, and one isolate from the OH displayed the constitutive phenotype ermC gene. The ccr types I and II were identified with a higher frequency of ccr type I. No statistically significant difference was found in the frequency of the genes between the two groups of patients or in the two hospitals. Regarding the virulence genes, there was statistically significant difference when comparing the two hospitals.


Aggarwal, S., Jena, S., Panda, S., Sharma, S., Dhawan, B., Nath, G. et al. (2019). Antibiotic susceptibility, virulence pattern, and typing of Staphylococcus aureus strains isolated from variety of infections in India. Frontiers in Microbiology, 10:2763. 10.3389/fmicb.2019.02763.

Andrade-Figueiredo, M. & Leal-Balbino, T.C. (2016). Clonal diversity and epidemiological characteristics of Staphylococcus aureus: high prevalence of oxacillin-susceptible mecA-positive Staphylococcus aureus (OS-MRSA) associated with clinical isolates in Brazil. BMC Microbiology, 16:115. 10.1186/s12866-016-0733-4.

Azmi, K., Qrei, W. & Abdeen, Z. (2019). Screening of genes encoding adhesion factors and biofilm production in methicillin resistant strains of Staphylococcus aureus isolated from Palestinian patients. BMC Genomics, 20:578. 10.1186/s12864-019-5929-1.

Barbieri, R., Pesce, M., Franchelli, S., Baldelli, I., De Maria, A., Marchese, A. (2015). Phenotypic and genotypic characterization of Staphylococci causing breast peri-implant infections in oncologic patients. BMC Microbiology, 15 (1), 26. 10.1186/s12866-015-0368-x.

Bezerra Neto, A. M., Rabelo, M. A., Lima, J. L. C., Loibman, S. O., Leal, N. C., Maciel, M. A. V. (2018). Occurrence of the vanA gene in Staphylococcus epidermidis from nasopharyngeal secretion of Health-Care Workers, Recife, Brazil. Revista da Sociedade Brasileira de Medicina Tropical, 51(3), 304-309. 10.1590/0037-8682-0159-2017.

Bride, L. L., Pereira, M. F., Barbosa, M. C., Silva, N. C., Klein, N. M., Nascimento, T. C., & Schuenck, R. P. (2019). Differences in resistance profiles and virulence genes among methicillin-resistant and methicillin-susceptible Staphylococcus aureus of different lineages at a public tertiary hospital. Revista da Sociedade Brasileira de Medicina Tropical, 52, e20190095. 10.1590/0037-8682-0095-2019

Burnham, C. A. D., Weber, C. J. & Dunne Jr, W. M. (2010). Novel screening agar for detection of vancomycin-nonsusceptible Staphylococcus aureus. Journal of Clinical Microbiology, 48(3), 949–951. 10.1128/JCM.02295-09.

Cagol, A. R., Castro Junior, C. G., Martins, M. C., Machado, A. L., Ribeiro, R. C., Gregianin, L. J., &Brunetto, A. L. (2209). Oral vs. intravenous empirical antimicrobial therapy in febrile neutropenic patients receiving childhood cancer chemotherapy. Jornal de Pediatria, 85(6), 531-535. 10.2223/JPED.1956.

CLSI (Clinical and Laboratory Standards Institute). (2014). Performance standards for antimicrobial susceptibility testing, twenty-fourth informational supplement, documentM100-S24.Wayne, PA, USA. 2014.

Coutinho, V. L. S, Paiva, R. M., Reiter, K. C., de-Paris, F., Barth, A. L., & Machado, A. B. (2010). Distribution of erm genes and low prevalence of inducible resistance to clindamycin among staphylococci isolates. The Brazilian Journal of Infectious Diseases, 14(6), 564-568. 10.1016/S1413-8670(10)70113-6

Elboshra, M. M. E., Hamedelnil, Y. F., Moglad, E. H., & Altayb, H. N. (2020). Prevalence and characterization of virulence genes among methicillin resistant Staphylococcus aureus isolated from Sudanese patients in Khartoum state. New Microbe and New Infect. 38, 100784.

Figueiredo, A. M. S., Ferreira, F. A., Beltrame, C. O., & Côrtes, M. F. (2017). The role of biofilms in persistent infections and factors involved in ica-independent biofilm development and gene regulation in Staphylococcus aureus. Critical Reviews in Microbiology, 43(5), 602-620. 10.1080/1040841X.2017.1282941.

Fontelles, M. J., Simões, M. G., Farias, S. H., & Fontelles, R. G. S. (2009). Scientific research methodology: guidelines for elaboration of a research protocol. Revista Paraense de Medicina, 23(3).

Jenkins, A., Diep, B. A., Mai, T. T., Vo, N. H., Warrener, P., Suzich, J., Stover, C. K., & Sellman, B. R. (2015). Differential Expression and Roles of Staphylococcus aureus Virulence Determinants during Colonization and Disease. mBio. 6(1), e02272-14. 10.1128/mBio.02272-14

Jiang, A.M., Shi, X., Liu, N., Gao, H., Ren, M. D., Zheng, X. Q. et al. (2020). Nosocomial infections due to multidrugresistant bacteria in cancer patients: a sixyear retrospective study of an oncology Center in Western China. BMC Infectious Diseases. 20, 452. 10.1186/s12879-020-05181-6.

Jones, R. N., Guzman-Blanco, M., Gales, A. C., Gallegos, B., Castro, A. L., Martino, M. D., Vega, S., Zurita, J., Cepparulo, M., & Castanheira, M. (2013). Susceptibility rates in Latin American nations: report from a regional resistance surveillance program (2011). The Brazilian Journal of Infectious Diseases, 17(6), 672–681. 10.1016/j.bjid.2013.07.002.

Juyal, D., Shamanth, A. S., Pal, S., Sharma, M. K., Prakash, R., & Sharma, N. (2013). The prevalence of inducible clindamycin resistance among Staphylococci in a tertiary care hospital – A study from the Garhwal Hills of Uttarakhand, India. Journal of Clinical & Diagnostic Research, 7(1), 61-65. 10.7860/JCDR/2012/4877.2671.

Kang, C. I., Song, J. H., Chung, D. R., Peck, K. R., Yeom, J. S., Son, J. S., & Wi, Y. M. (2012). Bloodstream infections in adult patients with cancer: clinical features and pathogenic significance of Staphylococcus aureus bacteremia. Supportive Care in Cancer, 20(10), 2371–2378. 10.1007/s00520-011-1353-z.

Kondo, Y., Ito, T., Ma, X. X., Watanabe, S., Kreiswirth, B. N., Etienne, J., & Hiramatsu, K. (2007). Combination of multiplex PCRs for staphylococcal cassette chromosome mec type assignment: rapid identification system for mec, ccr, and major differences in junkyard regions. Antimicrobial Agents and Chemoterapy, 51(1), 264-274. 10.1128/AAC.00165-06.

Kord, M., Ardebili, A., Jamalan, M., Jahanbakhsh, R., Behnampour, N., & Ghaemi, E. A. (2018). Evaluation of biofilm formation and presence of Ica genes in Staphylococcus epidermidis clinical isolates. Osong Public Health and Research Perspectives, 9(4), 160−166. 10.24171/j.phrp.2018.9.4.04.

Kumar, S., Bandyopadhyay, M., Bhattacharya, K., Bandyopadhyay, M.K., Banerjee, P., Pal, N., Mondal, S., & Ghosh, T. (2012). Inducible clindamycin resistance in Staphylococcus isolates from a tertiary care hospital in eastern India. Annals of Tropical Medicine and Public Health, 5(5), 468-470. doi:10.4103/1755-6783.105134.

Leclercq R. (2002). Mechanisms of resistance to macrolides and lincosamides: nature of the resistance elements and their clinical implications. Clinical Infectious Diseases, 34(4), 482- 492. 10.1086/324626.

Lim, K. T., Hanifah, Y. A., Yusof, M. Y. M., & Thong, K. L. (2012). Characterisation of the virulence factors and genetic types of methicillin susceptible Staphylococcus aureus from patients and healthy individuals. Indian Journal of Microbiology, 52(4), 593–600. 10.1007/s12088-012-0286-7.

Lima, D. F., Brazão, N. B., Folescu, T. W., Neves, F. P., Ferreira, A. G., Santos, E. A., Marques, E. A., & Leão, R. S. (2014). Panton-Valentine leukocidin (PVL) gene carriage among Staphylococcus aureus strains with SCCmec types I, III, IV,and V recovered from cystic fibrosis pediatric patients in Brazil. Diagnostic Microbiology and Infectious Disease, 78(1), 59–62. 10.1016/j.diagmicrobio.2013.10.004.

Lina, G., Quaglia, A., Reverdy, M. E., Leclercq, R., Vandenesch, F., & Etienne, J. (1999a). Distribution of genes encoding resistance to macrolides, lincosamides, and streptogramins among Staphylococci. Antimicrobial Agents and Chemoterapy, 43(5), 1062–1066. 10.1128/aac.43.5.1062.

Lina, G., Piémont, Y., Godail-Gamot, F., Bes, M., Peter, M. O., Gauduchon, V., Vandenesch, F., & Etienne, J. (1999b). Involvement of Panton-Valentine Leukocidin- producing Staphylococcus aureus in primary skin infections and pneumonia. Clinical Infectious Diseases. 29(5), 1128-1132. 10.1086/313461.

Milheiriço, C., Portelinha, A., Krippahl, L., de Lencastre, H., & Oliveira, D. C. (2011). Evidence for a purifying selection acting on the betalactamase lócus in epidemic clones of methicillin-resistant Staphylococcus aureus. BMC Microbiology, 11(1), 76. 10.1186/1471-2180-11-76.

Montassier, E., Batar, E., Gastinne, T., Potel, G., & de La Cochetière, M. F. (2013). Recent changes in bacteremia in patients with cancer: a systematic review of epidemiology and antibiotic resistance. European Journal of Clinical Microbiology & Infectious Diseases, 32 (7), 841–50. 10.1007/s10096-013-1819-7.

Muldrew, K. L., Tang, Y. W., Li, H., & Stratton, C. W. (2008). Clonal Dissemination of Staphylococcus epidermidis in an Oncology Ward. Journal of Clinical Microbiology, 46(10), 3391–3396. 10.1128/JCM.00115-08.

Oliveira, A. A. F., Pinheiro Jr, J. W., Mota, R. A., Cunha, M. L., Lopes, C. A., & Rocha, N. S. (2011). Phenotype characterization of Staphylococcus species strains isolated from buffalo (Bubalus bubalis) milk. Journal of Veterinary Diagnostic Investigation, 23(6), 1208-1211. 10.1177/1040638711428946.

Oliveira, W. L. M., Ferreira, E. L., Mangueira, E. V. C., Vilela, M. A., Almeida, A. M. P., & Leal, N. C. (2014). Coagulase-Negative Staphylococci from hospital-associated infections harboring virulence genes. Jacobs Journal of Microbiology and Pathology, 1(2), 013.

Oliveira, W. L. M., Mangueira, E. V. C., Vilela, M. A., Júnior, S. P., Leal, N. C., & Almeida, A. M. P. (2015). Diversity of Sccmec types in methicillin resistant Staphylococcus spp. causing hospital-associated infections. Jacobs Journal of Microbiology and Pathology, 2(3), 020.

Panesso, D., Planet, P. J., Diaz, L., Hugonnet, J. E., Tran, T. T., Narechania, A. et al. (2015). Methicillin-Susceptible, Vancomycin-Resistant Staphylococcus aureus, Brazil. Emerging Infectious Diseases, 21(10): 1844-1848. 10.3201/eid2110.141914.

Prabhash, K., Medhekar, A., Ghadyalpatil, N., Noronha, V., Biswas, S., Kurkure, P., Nair, R., & Kelkar, R. (2010). Blood stream infections in cancer patients: a single center experience of isolates and sensitivity pattern. Indian Journal of Cancer, 47 (2), 184–188. 10.4103/0019-509X.63019.

Quiles, M. G., Menezes, L. C., Bauab, K. C., Gumplv, E. K., Rocchetti, T. T., Palomo, F. S., Carlesse, F., & Pignatari, A. C. C. (2015). Diagnosis of bacteremia in pediatric oncologic patients by in-house real-time PCR. BMC Infectious Diseases, 15, 283. 10.1186/s12879-015-1033-6.

Rabelo, M. A., Bezerra Neto, A. M., Loibman, S. O., Lima, J. L. C., Ferreira, E. L., Leal, N. C., & Maciel, M. A. V. (2014). The occurrence and dissemination of methicillin and vancomycin-resistant Staphylococcus in samples from patients and health professionals of a university hospital in Recife, State of Pernambuco, Brazil. Revista da Sociedade Brasileira de Medicina Tropical, 47(4), 437-446. 10.1590/0037-8682-0071-2014.

Rabelo, M. A., Bezerra Neto, A. M., Silva, E. C. B. F., Oliveira, W. L. M., Melo, F. L., Lopes, A. C. S., Leal, N. C., & Maciel, M. A. V. (2013). Phenotypic methods for determination of methicillin resistance in Staphylococcus spp. from health care workers. Jornal Brasileiro de Patologia e Medicina Laboratorial, 49(2), 91-96. 10.1590/S1676-24442013000200003.

Rossi, F., Diaz, L., Wollam, A., Panesso, D., Zhou, Y., Rincon, S. et al. (2014). Transferable Vancomycin Resistance in a Community-Associated MRSA Lineage. The New England Journal of Medicine, 370(16), 1524-1531. 10.1056/NEJMoa1303359.

Saderi, H., Emadi, B. & Owlia, P. (2011). Phenotypic and genotypic study of macrolide, lincosamide and streptogramin B (MLSB) resistance in clinical isolates of Staphylococcus aureus in Tehran, Iran. Medical Science Monitor, 17 (2), 48-53. 10.12659/MSM.881386.

Sangappa, M. & Thiagarajan, P. (2012). Methicillin resistant Staphylococcus aureus: resistance genes and their regulation. International Journal of Pharmacy and Pharmaceutical Sciences, 4(1):658-667.

Sedaghat, H., Esfahani, B. N., Mobasherizadeh, S., Jazi, A. S., Halaji, M., Sadeghi, P., Emaneini, M., & Havaei, A. S. (2017). Phenotypic and genotypic characterization of macrolide resistance among Staphylococcus aureus isolates in Isfahan, Iran. Iranian Journal of Microbiology, 9(5), 264-270.

Silveira, A., Cunha, G. R., Caierão, J., Cordova, C. M., & d'Azevedo, P. A. (2015). MRSA from Santa Catarina State, Southern Brazil: intriguing epidemiological differences compared to other Brazilian regions. The Brazilian Journal of Infectious Diseases, 19(4), 384–389. 10.1016/j.bjid.2015.04.009

Spaan, A. N., Vrieling, M., Wallet, P., Badiou, C., Reyes-Robles, T., Ohneck, E. A. et al. (2014). The staphylococcal toxins γhaemolysin AB and CB differentially target phagocytes by employing specific chemokine receptors. Nature Communications, 5, 5438. 10.1038/ncomms6438.

Vasudevan, P., Nair, M. K. M., Annamalai, T., & Venkitanarayanan, K. S. (2003). Phenotypic and genotypic characterization of bovine mastitis isolates of Staphylococcus aureus for biofilm formation. Veterinary Microbiology. 92, 179-185. 10.1016/S0378-1135(02)00360-7.




How to Cite

RABELO, M. A.; SILVA, S. T. da; PEREIRA, J. N. da P.; SILVA, N. R. S. da; ROCHA, V. H. de A.; ARAÚJO, P. S. R.; ALMEIDA, A. M. P. de; LEAL, N. C.; MACIEL, M. A. V. Antimicrobial Resistance and Virulence of Staphylococcus spp. in patients from oncologic and non oncologic hospitals of Recife City/PE. Research, Society and Development, [S. l.], v. 10, n. 10, p. e323101018951, 2021. DOI: 10.33448/rsd-v10i10.18951. Disponível em: Acesso em: 5 dec. 2021.



Health Sciences