Antimicrobial susceptibility pattern of oral viridans group streptococci in children at risk of infective endocarditis
Antimicrobial susceptibility pattern of oral viridans group streptococci in children
Keywords:
Endocarditis; Dental Care for Children; Viridans Streptococci; Microbial Sensitivity Tests; Anti-Bacterial Agents
Abstract
Infective Endocarditis (IE) is an important clinical disease in children with a mortality rate of 11.6%. Prophylaxis with antibiotics is one of the most commonly used methods in children at risk of IE; therefore the evaluation of antibiotic resistance seems necessary in view of its increasing trend. This study aimed to determine the antibiotic susceptibility pattern of oral viridans group streptococci (VGS) isolated from the dental plaque of children at risk of IE.
Fifty one plaque samples were obtained from children aged 3 to 12 years old during April to July 2018. Samples were obtained with sterile swabs and were transferred to the laboratory in Brain Heart Infusion Broth (BHI). Samples were immediately cultivated on Columbia blood agar. After identifying VGS, antimicrobial susceptibility test (AST) was performed using Mueller-Hinton agar (MHA) with sheep’s blood and E-test strips for selected antibiotics. The minimum inhibitory concentration (MIC) was determined for each isolate and the results were reported as sensitive, intermediate and resistant.
Fifty one VGS bacteria were isolated from children with an average age of 7.3±2.5. The highest resistance was observed for azithromycin in 36 (70.6%) isolates and then cefazolin in 35 (68.6%) isolates. The highest susceptibility was observed for amoxicillin in 46 (90.2%) isolates.
Based on the findings of this study, amoxicillin is the most effective option for prophylaxis in children. Furthermore, cefazolin should be used with care because bacteria resistant to this antibiotic can be the carrier of resistance genes to the other bacteria.
References
1. Nemoto H, Nomura R, Ooshima T, Nakano K. Distribution of amoxicillin-resistant oral streptococci in dental plaque specimens obtained from Japanese children and adolescents at risk for infective endocarditis. J Cardiol. 2013; 62(5):296-300. https://doi.org/10.1016/j.jjcc.2013.05.008
2. Holland TL, Baddour LM, Bayer AS, Hoen B, Miro JM, Fowler VG Jr. Infective endocarditis. Nat Rev Dis Primers. 2016; 2:16059. https://doi.org/10.1038/nrdp.2016.59
3. Süzük S, Kaşkatepe B, Çetin M. Antimicrobial susceptibility against penicillin, ampicillin and vancomycin of viridans group Streptococcus in oral microbiota of patients at risk of infective endocarditis. Infez Med. 2016;24(3):190-3.
4. Goldsmith C, Hara Y, Sato T, Nakajima T, Nakanishi S, Mason C, et al. Comparison of antibiotic susceptibility in viridans group streptococci in low and high antibiotic‐prescribing General Practices. J Clin Pharm Ther. 2015; 40(2):204-7. https://doi.org/10.1111/jcpt.12245
5. Poveda-Roda R, Jiménez Y, Carbonell E, Gavaldá C, Margaix-Muñoz MM, Sarrión-Pérez G. Bacteremia originating in the oral cavity. A review. Med Oral Patol Oral Cir Bucal. 2008;13(6):E355-E362.
6. Kelchtermans J, Grossar L, Eyskens B, Cools B, Roggen M, Boshoff D, et al. Clinical Characteristics of Infective Endocarditis in Children. Pediatr Infect Dis J. 2019; 38(5):453-458. https://doi.org/10.1097/INF.0000000000002212
7. Dixon G, Christov G. Infective endocarditis in children: an update. Curr Opin Infect Dis. 2017; 30(3):257-267. https://doi.org/10.1097/QCO.0000000000000370
8. Seymour RA. Dentistry and the medically compromised patient. Surgeon. 2003; 1(4):207-14. https://doi.org/10.1016/s1479-666x(03)80019-7
9. Thornhill MH, Dayer M, Lockhart PB, Prendergast B. Antibiotic prophylaxis of infective endocarditis. Curr Infect Dis Rep. 2017; 19(2):9. https://doi.org/10.1007/s11908-017-0564-y
10. Abu-zineh R, Dar-Odeh N, Shehabi A. Macrolide resistance genes and virulence factors of common viridans Streptococci species colonizing oral cavities of patients in Jordan. Oral Health Dent Manag. 2015;14:337-41.
11. Chitra N, Mangayarkarasi V, Balakrishnan D, Smiline Girija AS. Resistance Patterns of Viridans Group of Streptococci isolated in transient bacteremia after third molar surgery. Int J Curr Microbiol App Sci. 2015;4(6):78-85.
12. Parks T, Barrett L, Jones N. Invasive streptococcal disease: a review for clinicians. Br Med Bull. 2015; 115(1):77-89. https://doi.org/10.1093/bmb/ldv027
13. Prakash D, Ramesh K, Gopinath N, SS SK, Varuvelil GJ. Antibacterial efficacy of Syzygium aromaticum extracts on multi-drug resistant Streptococcus mutans isolated from dental plaque samples. J Biochem Technol. 2014;3(5):155-7.
14. Rotimi V, Salako N, Mokaddas E, Philip L, Rajan P. High frequency of isolation of antibiotic-resistant oral Viridans streptococci from children in Kuwait. J Chemother. 2005; 17(5):493-501. https://doi.org/10.1179/joc.2005.17.5.493
15. Chun S, Huh HJ, Lee NY. Species-specific difference in antimicrobial susceptibility among viridans group streptococci. Ann Lab Med. 2015; 35(2):205-11. https://doi.org/10.3343/alm.2015.35.2.205
16. Park S-C, Park Y, Hahm K-S. The role of antimicrobial peptides in preventing multidrug-resistant bacterial infections and biofilm formation. Int J Mol Sci. 2011;12(9):5971-92. https://doi.org/10.3390/ijms12095971
17. Garg P, Ko DT, Bray Jenkyn KM, Li L, Shariff SZ. Infective Endocarditis Hospitalizations and Antibiotic Prophylaxis Rates Before and After the 2007 American Heart Association Guidelines Revision. Circulation. 2019; 140(3):170-180. https://doi.org/10.1161/CIRCULATIONAHA.118.037657
18. Shafiee F, Moghadamnia AA, Shahandeh Z, Sadighian F, Khodadadi E. Evaluation of the antibacterial effects of aqueous and ethanolic leaf extracts of Aloysia Citriodora (Lemon verbena) on Streptococcus mutans and Streptococcus sobrinus. Electron Physician. 2016;8(12):3363. https://doi.org/10.19082/3363
19. Carroll KC BJ, Morse S. Jawetz, Melnick& Adelbergs medical microbiology. 17 ed. Caroll KC HJ, editor. Toronto: McGraw-Hill; 2016.
20. Gloria-Garza MA, Gomez-Flores R, De La Garza-Ramos MA, Quintanilla-Licea R, Tamez-Guerra R, Tamez-Guerra P, et al. In vitro antimicrobial activity of Ruta chalepensis methanol extracts against the cariogenic Streptococcus mutans. Afr J Microbiol Res. 2013;7(46):5234-7.
21. Basak S, Singh P, Rajurkar M. Multidrug resistant and extensively drug resistant bacteria: A study. J Pathog. 2016;2016:4065603. https://doi.org/10.1155/2016/4065603
22. Liu S, Zheng Y, Wu X, Xu B, Liu X, Feng G, et al. Early target attainment of azithromycin therapy in children with lower respiratory tract infections. J Antimicrob Chemother. 2018; 73(10):2846-2850. https://doi.org/10.1093/jac/dky273
23. Saffar MJ. Acute Lower Respiratory Tract Infections Including Pneumonia; Clinical Approach to Diagnosis and Treatment: A Narrative Review. J Clin Exc. 2014;3(1):29-45.
24. Malhotra-Kumar S, Lammens C, Coenen S, Van Herck K, Goossens H. Effect of azithromycin and clarithromycin therapy on pharyngeal carriage of macrolide-resistant streptococci in healthy volunteers: a randomised, double-blind, placebo-controlled study. Lancet. 2007; 369(9560):482-90. https://doi.org/10.1016/S0140-6736(07)60235-9
25. Dhotre S, Jahagirdar V, Suryawanshi N, Davane M, Patil R, Nagoba B. Assessment of periodontitis and its role in viridans streptococcal bacteremia and infective endocarditis. Indian Heart J. 2018; 70(2):225-232. https://doi.org/10.1016/j.ihj.2017.06.019
26. Borji A, Naghavi A, Borji H. An investigation on drug resistance of viridance group streptococci isolated from 3-12 years healthy individuals. Zahedan. J Res Med Sci. 2010;12(4):28-32.
27. Fani M, Kohanteb J, Dayaghi M. Inhibitory activity of garlic (Allium sativum) extract on multidrug-resistant Streptococcus mutans. J Indian Soc Pedod Prev Dent. 2007; 25(4):164-8. https://doi.org/10.4103/0970-4388.37011
28. Geethu M, Prabhu N, Jasmine M. Antimicrobial susceptibility trends among viridan streptococci isolates from cases of endocarditis from 2007-2009. Ann Biol Res. 2010;1(1):130-3.
29. Groppo FC, Castro FM, Pacheco AB, Motta RH, Ramacciato JC, Florio FM, et al. Antimicrobial resistance of Staphylococcus aureus and oral streptococci strains from high-risk endocarditis patients. Gen Dent. 2005; 53(6):410-3.
30. Karikalan S, Mohankumar A. Studies on ampicillin resistant plasmid of Streptococcus mutans isolated from dental caries patients. Biosc Biotech Res Comm. 2016;9(1):151-6. http://dx.doi.org/10.21786/bbrc/9.1/23
31. Aslam B, Wang W, Arshad MI, Khurshid M, Muzammil S, Rasool MH, et al. Antibiotic resistance: a rundown of a global crisis. Infect Drug Resist. 2018; 11:1645-1658. http://dx.doi.org/10.2147/IDR.S173867
32. Chunduri NS, Madasu K, Goteki VR, Karpe T, Reddy H. Evaluation of bacterial spectrum of orofacial infections and their antibiotic susceptibility. Ann Maxillofac Surg. 2012; 2(1):46-50. http://dx.doi.org/10.4103/2231-0746.95318
33. William B, Rwenyonyi CM, Swedberg G, Kironde F. Cotrimoxazole prophylaxis specifically selects for cotrimoxazole resistance in Streptococcus mutans and Streptococcus sobrinus with varied polymorphisms in the target genes folA and folP. Int J Microbiol. 2012;2012:916129. https://doi.org/10.1155/2012/916129
34. Hussain Z, Curtain C, Mirkazemi C, Gadd K, Peterson GM, Zaidi STR. Prophylactic Cefazolin Dosing and Surgical Site Infections: Does the Dose Matter in Obese Patients? Obes Surg. 2019; 29(1):159-165. https://doi.org/10.1007/s11695-018-3497-0
35. Kim MK, Chuang S-K, August M. Antibiotic resistance in severe orofacial infections. J Oral Maxillofac Surg. 2017; 75(5):962-968. https://doi.org/10.1016/j.joms.2016.10.039
36. Ang JY, Asmar BI. Multidrug-resistant viridans streptococcus (MDRVS) osteomyelitis of the mandible successfully treated with moxifloxacin. South Med J. 2008; 101(5):539-40. https://doi.org/10.1097/SMJ.0b013e3181684ee3
37. Dhotre S, Dharne M, Potdar S, Suklikar J, Suryawanshi N, Nagoba B. Viridians Group Streptococci in Patients Undergoing Tooth Extraction. Eur J Gen Med. 2015;12(3):227-33. https://doi.org/10.15197/ejgm.01406
38. Cahill TJ, Harrison JL, Jewell P, Onakpoya I, Chambers JB, Dayer M, et al. Antibiotic prophylaxis for infective endocarditis: a systematic review and meta-analysis. Heart. 2017; 103(12):937-944. https://doi.org/10.1136/heartjnl-2015-309102
39. Vogkou CT, Vlachogiannis NI, Palaiodimos L, Kousoulis AA. The causative agents in infective endocarditis: a systematic review comprising 33,214 cases. Eur J Clin Microbiol Infect Dis. 2016; 35(8):1227-45. https://doi.org/10.1007/s10096-016-2660-6
40. Błochowiak KJ. Dental treatment and recommended management in patients at risk of infective endocarditis. Kardiochir Torakochirurgia Pol. 2019; 16(1):37-41. https://doi.org/10.5114/kitp.2019.83944
2. Holland TL, Baddour LM, Bayer AS, Hoen B, Miro JM, Fowler VG Jr. Infective endocarditis. Nat Rev Dis Primers. 2016; 2:16059. https://doi.org/10.1038/nrdp.2016.59
3. Süzük S, Kaşkatepe B, Çetin M. Antimicrobial susceptibility against penicillin, ampicillin and vancomycin of viridans group Streptococcus in oral microbiota of patients at risk of infective endocarditis. Infez Med. 2016;24(3):190-3.
4. Goldsmith C, Hara Y, Sato T, Nakajima T, Nakanishi S, Mason C, et al. Comparison of antibiotic susceptibility in viridans group streptococci in low and high antibiotic‐prescribing General Practices. J Clin Pharm Ther. 2015; 40(2):204-7. https://doi.org/10.1111/jcpt.12245
5. Poveda-Roda R, Jiménez Y, Carbonell E, Gavaldá C, Margaix-Muñoz MM, Sarrión-Pérez G. Bacteremia originating in the oral cavity. A review. Med Oral Patol Oral Cir Bucal. 2008;13(6):E355-E362.
6. Kelchtermans J, Grossar L, Eyskens B, Cools B, Roggen M, Boshoff D, et al. Clinical Characteristics of Infective Endocarditis in Children. Pediatr Infect Dis J. 2019; 38(5):453-458. https://doi.org/10.1097/INF.0000000000002212
7. Dixon G, Christov G. Infective endocarditis in children: an update. Curr Opin Infect Dis. 2017; 30(3):257-267. https://doi.org/10.1097/QCO.0000000000000370
8. Seymour RA. Dentistry and the medically compromised patient. Surgeon. 2003; 1(4):207-14. https://doi.org/10.1016/s1479-666x(03)80019-7
9. Thornhill MH, Dayer M, Lockhart PB, Prendergast B. Antibiotic prophylaxis of infective endocarditis. Curr Infect Dis Rep. 2017; 19(2):9. https://doi.org/10.1007/s11908-017-0564-y
10. Abu-zineh R, Dar-Odeh N, Shehabi A. Macrolide resistance genes and virulence factors of common viridans Streptococci species colonizing oral cavities of patients in Jordan. Oral Health Dent Manag. 2015;14:337-41.
11. Chitra N, Mangayarkarasi V, Balakrishnan D, Smiline Girija AS. Resistance Patterns of Viridans Group of Streptococci isolated in transient bacteremia after third molar surgery. Int J Curr Microbiol App Sci. 2015;4(6):78-85.
12. Parks T, Barrett L, Jones N. Invasive streptococcal disease: a review for clinicians. Br Med Bull. 2015; 115(1):77-89. https://doi.org/10.1093/bmb/ldv027
13. Prakash D, Ramesh K, Gopinath N, SS SK, Varuvelil GJ. Antibacterial efficacy of Syzygium aromaticum extracts on multi-drug resistant Streptococcus mutans isolated from dental plaque samples. J Biochem Technol. 2014;3(5):155-7.
14. Rotimi V, Salako N, Mokaddas E, Philip L, Rajan P. High frequency of isolation of antibiotic-resistant oral Viridans streptococci from children in Kuwait. J Chemother. 2005; 17(5):493-501. https://doi.org/10.1179/joc.2005.17.5.493
15. Chun S, Huh HJ, Lee NY. Species-specific difference in antimicrobial susceptibility among viridans group streptococci. Ann Lab Med. 2015; 35(2):205-11. https://doi.org/10.3343/alm.2015.35.2.205
16. Park S-C, Park Y, Hahm K-S. The role of antimicrobial peptides in preventing multidrug-resistant bacterial infections and biofilm formation. Int J Mol Sci. 2011;12(9):5971-92. https://doi.org/10.3390/ijms12095971
17. Garg P, Ko DT, Bray Jenkyn KM, Li L, Shariff SZ. Infective Endocarditis Hospitalizations and Antibiotic Prophylaxis Rates Before and After the 2007 American Heart Association Guidelines Revision. Circulation. 2019; 140(3):170-180. https://doi.org/10.1161/CIRCULATIONAHA.118.037657
18. Shafiee F, Moghadamnia AA, Shahandeh Z, Sadighian F, Khodadadi E. Evaluation of the antibacterial effects of aqueous and ethanolic leaf extracts of Aloysia Citriodora (Lemon verbena) on Streptococcus mutans and Streptococcus sobrinus. Electron Physician. 2016;8(12):3363. https://doi.org/10.19082/3363
19. Carroll KC BJ, Morse S. Jawetz, Melnick& Adelbergs medical microbiology. 17 ed. Caroll KC HJ, editor. Toronto: McGraw-Hill; 2016.
20. Gloria-Garza MA, Gomez-Flores R, De La Garza-Ramos MA, Quintanilla-Licea R, Tamez-Guerra R, Tamez-Guerra P, et al. In vitro antimicrobial activity of Ruta chalepensis methanol extracts against the cariogenic Streptococcus mutans. Afr J Microbiol Res. 2013;7(46):5234-7.
21. Basak S, Singh P, Rajurkar M. Multidrug resistant and extensively drug resistant bacteria: A study. J Pathog. 2016;2016:4065603. https://doi.org/10.1155/2016/4065603
22. Liu S, Zheng Y, Wu X, Xu B, Liu X, Feng G, et al. Early target attainment of azithromycin therapy in children with lower respiratory tract infections. J Antimicrob Chemother. 2018; 73(10):2846-2850. https://doi.org/10.1093/jac/dky273
23. Saffar MJ. Acute Lower Respiratory Tract Infections Including Pneumonia; Clinical Approach to Diagnosis and Treatment: A Narrative Review. J Clin Exc. 2014;3(1):29-45.
24. Malhotra-Kumar S, Lammens C, Coenen S, Van Herck K, Goossens H. Effect of azithromycin and clarithromycin therapy on pharyngeal carriage of macrolide-resistant streptococci in healthy volunteers: a randomised, double-blind, placebo-controlled study. Lancet. 2007; 369(9560):482-90. https://doi.org/10.1016/S0140-6736(07)60235-9
25. Dhotre S, Jahagirdar V, Suryawanshi N, Davane M, Patil R, Nagoba B. Assessment of periodontitis and its role in viridans streptococcal bacteremia and infective endocarditis. Indian Heart J. 2018; 70(2):225-232. https://doi.org/10.1016/j.ihj.2017.06.019
26. Borji A, Naghavi A, Borji H. An investigation on drug resistance of viridance group streptococci isolated from 3-12 years healthy individuals. Zahedan. J Res Med Sci. 2010;12(4):28-32.
27. Fani M, Kohanteb J, Dayaghi M. Inhibitory activity of garlic (Allium sativum) extract on multidrug-resistant Streptococcus mutans. J Indian Soc Pedod Prev Dent. 2007; 25(4):164-8. https://doi.org/10.4103/0970-4388.37011
28. Geethu M, Prabhu N, Jasmine M. Antimicrobial susceptibility trends among viridan streptococci isolates from cases of endocarditis from 2007-2009. Ann Biol Res. 2010;1(1):130-3.
29. Groppo FC, Castro FM, Pacheco AB, Motta RH, Ramacciato JC, Florio FM, et al. Antimicrobial resistance of Staphylococcus aureus and oral streptococci strains from high-risk endocarditis patients. Gen Dent. 2005; 53(6):410-3.
30. Karikalan S, Mohankumar A. Studies on ampicillin resistant plasmid of Streptococcus mutans isolated from dental caries patients. Biosc Biotech Res Comm. 2016;9(1):151-6. http://dx.doi.org/10.21786/bbrc/9.1/23
31. Aslam B, Wang W, Arshad MI, Khurshid M, Muzammil S, Rasool MH, et al. Antibiotic resistance: a rundown of a global crisis. Infect Drug Resist. 2018; 11:1645-1658. http://dx.doi.org/10.2147/IDR.S173867
32. Chunduri NS, Madasu K, Goteki VR, Karpe T, Reddy H. Evaluation of bacterial spectrum of orofacial infections and their antibiotic susceptibility. Ann Maxillofac Surg. 2012; 2(1):46-50. http://dx.doi.org/10.4103/2231-0746.95318
33. William B, Rwenyonyi CM, Swedberg G, Kironde F. Cotrimoxazole prophylaxis specifically selects for cotrimoxazole resistance in Streptococcus mutans and Streptococcus sobrinus with varied polymorphisms in the target genes folA and folP. Int J Microbiol. 2012;2012:916129. https://doi.org/10.1155/2012/916129
34. Hussain Z, Curtain C, Mirkazemi C, Gadd K, Peterson GM, Zaidi STR. Prophylactic Cefazolin Dosing and Surgical Site Infections: Does the Dose Matter in Obese Patients? Obes Surg. 2019; 29(1):159-165. https://doi.org/10.1007/s11695-018-3497-0
35. Kim MK, Chuang S-K, August M. Antibiotic resistance in severe orofacial infections. J Oral Maxillofac Surg. 2017; 75(5):962-968. https://doi.org/10.1016/j.joms.2016.10.039
36. Ang JY, Asmar BI. Multidrug-resistant viridans streptococcus (MDRVS) osteomyelitis of the mandible successfully treated with moxifloxacin. South Med J. 2008; 101(5):539-40. https://doi.org/10.1097/SMJ.0b013e3181684ee3
37. Dhotre S, Dharne M, Potdar S, Suklikar J, Suryawanshi N, Nagoba B. Viridians Group Streptococci in Patients Undergoing Tooth Extraction. Eur J Gen Med. 2015;12(3):227-33. https://doi.org/10.15197/ejgm.01406
38. Cahill TJ, Harrison JL, Jewell P, Onakpoya I, Chambers JB, Dayer M, et al. Antibiotic prophylaxis for infective endocarditis: a systematic review and meta-analysis. Heart. 2017; 103(12):937-944. https://doi.org/10.1136/heartjnl-2015-309102
39. Vogkou CT, Vlachogiannis NI, Palaiodimos L, Kousoulis AA. The causative agents in infective endocarditis: a systematic review comprising 33,214 cases. Eur J Clin Microbiol Infect Dis. 2016; 35(8):1227-45. https://doi.org/10.1007/s10096-016-2660-6
40. Błochowiak KJ. Dental treatment and recommended management in patients at risk of infective endocarditis. Kardiochir Torakochirurgia Pol. 2019; 16(1):37-41. https://doi.org/10.5114/kitp.2019.83944
Published
2025/12/21
Section
Originalni rad / Original article