Article Category:
Research Article

A Multicenter Experience of Inducible Clindamycin Resistance in Staphylococcus aureus Infection among 800 Egyptian Patients with or without Diabetes Mellitus

Housam Ahmad Helmy Department of Hepatology and Gastroenterology, National Liver Institute, Menoufia University, Menoufia, Egypt;

Search for other papers by Housam Ahmad Helmy in
Current site
Google Scholar
PubMed Close
,
Mohamed Rashed AbdElhamed Department of Clinical Pathology, Faculty of Medicine, Al-Azhar University, Cairo, Egypt;

Search for other papers by Mohamed Rashed AbdElhamed in
Current site
Google Scholar
PubMed Close
,
Mohamed I. Youssef Department of Internal Medicine, Faculty of Medicine, Al-Azhar University, Cairo, Egypt;

Search for other papers by Mohamed I. Youssef in
Current site
Google Scholar
PubMed Close
,
Houssam M. F. El Zamek Department of Clinical Pathology, Faculty of Medicine, Al-Azhar University, Cairo, Egypt;

Search for other papers by Houssam M. F. El Zamek in
Current site
Google Scholar
PubMed Close
,
Ahmed Kamal Department of Hepatology and Gastroenterology, National Liver Institute, Menoufia University, Menoufia, Egypt;

Search for other papers by Ahmed Kamal in
Current site
Google Scholar
PubMed Close
,
Ahmed Abdelfattah Department of Hepatology and Gastroenterology, National Liver Institute, Menoufia University, Menoufia, Egypt;

Search for other papers by Ahmed Abdelfattah in
Current site
Google Scholar
PubMed Close
,
Hossam Shabana Department of Internal Medicine, Faculty of Medicine, Al-Azhar University, Cairo, Egypt;

Search for other papers by Hossam Shabana in
Current site
Google Scholar
PubMed Close
,
Ahmed Abuamer Department of Hepatology and Gastroenterology, National Liver Institute, Menoufia University, Menoufia, Egypt;

Search for other papers by Ahmed Abuamer in
Current site
Google Scholar
PubMed Close
,
Galal Abdelhameed Aboufarrag Departments of Hepatology, Gastroenterology, and Infectious Diseases, Al-Azhar University, Cairo, Egypt;

Search for other papers by Galal Abdelhameed Aboufarrag in
Current site
Google Scholar
PubMed Close
,
Amr Aly Elshormilisy Department of Internal Medicine, Faculty of Medicine, Helwan University, Cairo, Egypt;

Search for other papers by Amr Aly Elshormilisy in
Current site
Google Scholar
PubMed Close
,
Doaa Elwazzan Department of Tropical Medicine, Faculty of Medicine, Alexandria University, Alexandria, Egypt;

Search for other papers by Doaa Elwazzan in
Current site
Google Scholar
PubMed Close
,
Sara A. Saied Department of Clinical Pathology, National Liver Institute, Menoufia University, Menoufia, Egypt;

Search for other papers by Sara A. Saied in
Current site
Google Scholar
PubMed Close
,
Ashraf Yousif Elfert Department of Clinical Biochemistry, National Liver Institute, Menoufia University, Menoufia, Egypt;

Search for other papers by Ashraf Yousif Elfert in
Current site
Google Scholar
PubMed Close
,
Shimaa Y. Kamel Department of Tropical Medicine, Faculty of Medicine, Ain Shams University, Cairo, Egypt;

Search for other papers by Shimaa Y. Kamel in
Current site
Google Scholar
PubMed Close
,
Amal El Sharnoby Department of Clinical Pathology, National Liver Institute, Menoufia University, Menoufia, Egypt;

Search for other papers by Amal El Sharnoby in
Current site
Google Scholar
PubMed Close
,
Hendawy Abdel-moety Zedan Department of Internal Medicine, Faculty of Medicine, Al-Azhar University, Cairo, Egypt;

Search for other papers by Hendawy Abdel-moety Zedan in
Current site
Google Scholar
PubMed Close
,
Basant Mostafa Gabr Department of Microbiology and Immunology, Faculty of Medicine, Tanta University, Tanta, Egypt;

Search for other papers by Basant Mostafa Gabr in
Current site
Google Scholar
PubMed Close
,
Farag Khalil Department of Internal Medicine, Faculty of Medicine, Al-Azhar University, Cairo, Egypt;

Search for other papers by Farag Khalil in
Current site
Google Scholar
PubMed Close
,
Ismail Mohamed Elmancy Department of Internal Medicine, Faculty of Medicine, Al-Azhar University, Cairo, Egypt;

Search for other papers by Ismail Mohamed Elmancy in
Current site
Google Scholar
PubMed Close
,
Hesham El-Sayed Lashin Department of Internal Medicine, Faculty of Medicine, Al-Azhar University, Cairo, Egypt;

Search for other papers by Hesham El-Sayed Lashin in
Current site
Google Scholar
PubMed Close
,
Hind S. AboShabaan Department of Clinical Pathology, National Liver Institute, Menoufia University, Menoufia, Egypt;

Search for other papers by Hind S. AboShabaan in
Current site
Google Scholar
PubMed Close
,
Yousef Nassar Department of Internal Medicine, Faculty of Medicine, Al-Azhar University, Cairo, Egypt;

Search for other papers by Yousef Nassar in
Current site
Google Scholar
PubMed Close
,
Safa Reyad Abd Elsalam Elfiky Department of Clinical Pharmacology, Faculty of Medicine, Menoufia University, Shebeen El-Kom, Egypt;

Search for other papers by Safa Reyad Abd Elsalam Elfiky in
Current site
Google Scholar
PubMed Close
,
Sally Waheed Elkhadry Department of Epidemiology and Preventive Medicine, National Liver Institute, Menoufia University, Shebeen El-Kom, Egypt;

Search for other papers by Sally Waheed Elkhadry in
Current site
Google Scholar
PubMed Close
,
Mohamed A. Sakr Department of Medical Microbiology and Immunology, Faculty of Medicine, Suez University, Suez, Egypt;

Search for other papers by Mohamed A. Sakr in
Current site
Google Scholar
PubMed Close
,
Ashraf M. Eid Department of Gastroenterology, Hepatology and Infectious Diseases, Shebin El-Kom Teaching Hospital, Shebin El-Kom, Egypt;

Search for other papers by Ashraf M. Eid in
Current site
Google Scholar
PubMed Close
,
Sobhy Elsayed Kotb Al Jalila Children’s Speciality Hospital, Dubai, United Arab Emirates;

Search for other papers by Sobhy Elsayed Kotb in
Current site
Google Scholar
PubMed Close
,
Marwa M. Omar Department of Clinical Pathology, Faculty of Medicine, Menoufia University, Menoufia, Egypt;

Search for other papers by Marwa M. Omar in
Current site
Google Scholar
PubMed Close
, and
Mohsen M. El-Khayat Department of Tropical Medicine, Faculty of Medicine, Menoufia University, Shebeen El-Kom, Egypt

Search for other papers by Mohsen M. El-Khayat in
Current site
Google Scholar
PubMed Close
DOI:
https://doi.org/10.4269/ajtmh.22-0492
Volume/Issue:
Volume 109: Issue 2
Page(s):
350–355
Restricted access
Get Permissions

ABSTRACT.

Staphylococcus aureus causes a wide range of illnesses, from skin infections and persistent bone infections to life-threatening septicemia and endocarditis. Methicillin-resistant S. aureus (MRSA) is one of the most common bacteria that cause nosocomial and community-acquired infections. Clindamycin is one of the most effective treatments for several bacterial infections. Despite this, these infections may develop inducible clindamycin resistance during treatment, leading to treatment failure. This study determined the incidence of inducible clindamycin resistance among S. aureus clinical isolates. A total of 800 S. aureus strains were identified from clinical samples collected from several university hospitals in Egypt. All isolates were examined for the presence of MRSA using cefoxitin (30 μg) and the Kirby Bauer disk diffusion technique. The induction phenotypes of all 800 S. aureus strains were evaluated using the disk approximation test (D test), as recommended by the Clinical and Laboratory Standard Institute. Of the 800 strains of S. aureus, 540 (67.5%) were identified as MRSA and 260 (32.5%) were classified as methicillin-sensitive S. aureus (MSSA). In MRSA infections, clindamycin constitutive and inducible resistance was more frequent than in MSSA infections (27.8% versus 11.5% and 38.9% versus 15.4%, respectively). Clindamycin-sensitive strains were more prevalent in MSSA (53.8%) than in MRSA (20.4%) infections. In conclusion, the frequency of constitutive and inducible clindamycin resistance in MRSA isolates emphasizes the need to use the D test in routine antimicrobial susceptibility testing to evaluate clindamycin susceptibility, as the inducible resistance phenotype can inhibit the action of clindamycin and thus affect treatment efficacy.

Author Notes

Address correspondence to Mohamed Rashed AbdElhamed, Department of Clinical Pathology, Faculty of Medicine, Al-Azhar University, Almokhayam Aldaaem St., Nasr City 11884, Cairo, Egypt. E-mail: mohamedrashedabdelhamed@gmail.com

Disclosure: The study was done after being approved by both the research ethics committee, Faculty of Medicine, Tanta University (approval number: 35858/9/22) and Institutional Review Board of the National Liver Institute (IRB number 00385/2022), Menoufia University.

Disclaimer: Informed written consent was obtained from all individual participants included in the study. The study was reviewed and approved by the ethical committee at the Faculty of Medicine, Tanta University (IRB no. 35858/9/22).

Authors’ addresses: Housam Ahmad Helmy, Ahmed Kamal, Ahmed Abdelfattah, and Ahmed Abuamer, Department of Hepatology and Gastroenterology, National Liver Institute, Menoufia University, Menoufia, Egypt, E-mails: housamhelmy316@gmail.com, a.kamal21076@gmail.com, ahmedabdelfattah299@outlook.com, and ahmedabuamer2001@hotmail.com. Mohamed Rashed AbdElhamed and Houssam M. F. El Zamek, Department of Clinical Pathology, Faculty of Medicine, Al-Azhar University, Cairo, Egypt, E-mails: mohamedrashedabdelhamed@gmail.com and dr_elzamek2008@yahoo.com. Mohamed I. Youssef, Hossam Shabana, Hendawy Abdel-moety Zedan, Farag Khalil, Ismail Mohamed Elmancy, Hesham El-Sayed Lashin, and Yousef Nassar, Department of Internal Medicine, Faculty of Medicine, Al-Azhar University, Cairo, Egypt, E-mails: drmohamed.youssef82@azhar.edu.eg, shabana109@azhar.edu.eg, hendawyzedan@yahoo.com, dr.farag7070@azhar.edu.eg, ielmancy@yahoo.com, heshamlashin1976@gmail.com, and yousefdoctor8@gmail.com. Galal Abdelhameed Aboufarrag, Departments of Hepatology, Gastroenterology, and Infectious Diseases, Al-Azhar University, Cairo, Egypt, E-mail: drgalal2009@yahoo.com. Amr Aly Elshormilisy, Department of Internal Medicine, Faculty of Medicine, Helwan University, Cairo, Egypt, E-mail: amraly74@yahoo.com. Doaa Elwazzan, Department of Tropical Medicine, Faculty of Medicine, Alexandria University, Alexandria, Egypt, E-mail: d.elwazzan@gmail.com. Sara A. Saied, Amal El Sharnoby, and Hind S. AboShabaan, Department of Clinical Pathology, National Liver Institute, Menoufia University, Menoufia, Egypt, E-mails: sarasaied@ymail.com, amalsharnoby000@gmail.com, and drhindsaad@liver.menofia.edu.eg. Ashraf Yousif Elfert, Department of Clinical Biochemistry, National Liver Institute, Menoufia University, Menoufia, Egypt, E-mail: ashrafelfert@outlook.com. Shimaa Y. Kamel, Department of Tropical Medicine, Faculty of Medicine, Ain Shams University, Cairo, Egypt, E-mail: shimaayoussif81@gmail.com. Basant Mostafa Gabr, Department of Microbiology and Immunology, Faculty of Medicine, Tanta University, Tanta, Egypt, E-mail: basant.mostafa@med.tanta.edu.eg. Safa Reyad Abd Elsalam Elfiky, Department of Clinical Pharmacology, Faculty of Medicine, Menoufia University, Shebeen El-Kom, Egypt, E-mail: safa.riad@med.menofia.edu.eg. Sally Waheed Elkhadry, Department of Epidemiology and Preventive Medicine, National Liver Institute, Menoufia University, Shebeen El-Kom, Egypt, E-mail: dr.salywaheed@gmail.com. Mohamed A. Sakr, Department of Medical Microbiology and Immunology, Faculty of Medicine, Suez University, Suez, Egypt, E-mail: msakr.md@gmail.com. Ashraf M. Eid, Department of Gastroenterology, Hepatology and Infectious Diseases, Shebin El-Kom Teaching Hospital, Shebin El-Kom, Egypt, E-mail: eid.ashraf74@yahoo.com. Sobhy Elsayed Kotb, Al Jalila Children’s Speciality Hospital, Dubai, United Arab Emirates, E-mail: sobhyelsayedkotb@gmail.com. Marwa M. Omar, Department of Clinical Pathology, Faculty of Medicine, Menoufia University, Menoufia, Egypt, E-mail: drmarwaomar2010@gmail.com. Mohsen M. El-Khayat, Department of Tropical Medicine, Faculty of Medicine, Menoufia University, Shebeen El-Kom, Egypt, E-mail: mohsenelkhayat@gmail.com.

Copyright:
© American Society of Tropical Medicine and Hygiene 2023
Received:
01 Aug 2022
|
Accepted:
27 Feb 2023
|
Published Online:
03 Jul 2023
Cover The American Journal of Tropical Medicine and Hygiene
The American Journal of Tropical Medicine and Hygiene
Print ISSN:
0002-9637
Online ISSN:
1476-1645
  • 1.

    Vivek JS, Rajesh GN, Mukesh S, Manpreet K, Misra RN, Matnani GB, Ujagare MT, Saikat B, Ajay K, 2011. The prevalence of inducible clindamycin resistance among community and hospital-associated Staphylococcus aureus isolates in a tertiary care hospital in India. Biomed Res 22: 465–469.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 2.

    Deotale V, Mendiratta DK, Raut U, Narang P, 2010. Inducible clindamycin resistance in Staphylococcus aureus isolated from clinical samples. Indian J Med Microbiol 28: 124–126.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 3.

    Fiebelkorn KR, Crawford SA, Mcelmeel ML, Jorgensen JH, 2003. Practical disk diffusion method for detection of inducible clindamycin resistance in Staphylococcus aureus and coagulase-negative staphylococci. J Clin Microbiol 41: 4740–4744.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 4.

    Kader AA, Kumar A, Krishna A, 2005. Induction of clindamycin resistance in erythromycin-resistant, clindamycin susceptible and methicillin-resistant clinical staphylococcal isolates. Saudi Med J 26: 1914–1917.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 5.

    Prabhu K, Rao S, Rao V, 2011. Inducible clindamycin resistance in Staphylococcus aureus isolated from clinical samples. J Lab Physicians 3: 25–27.

  • 6.

    Vandana KE, Singh J, Chiranjay M, Bairy I, 2009. Inducible clindamycin resistance in Staphylococcus aureus: reason for treatment failure. J Glob Infect Dis 1: 76–77.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 7.

    Patel M, Waites KB, Moser SA, Cloud GA, Hoesley CJ, 2006. Prevalence of inducible clindamycin resistance among community- and hospital-associated Staphylococcus aureus isolates. J Clin Microbiol 44: 2481–2484.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 8.

    CLSI , 2019. CLSI Performance Standards for Antimicrobial Susceptibility Testing, 29th edition. Wayne, PA: Clinical and Laboratory Standard Institute.

  • 9.

    American Diabetes Association , 2019. Standard of medical care in diabetes 2019. Diabetes Care 42 (Suppl 1):S4–S6.

  • 10.

    Collee JG, Mackie TJ, McCartney JE, 1996. Mackie and McCartney Practical Medical Microbiology, 14th edition. New York, NY: Churchill Livingstone.

  • 11.

    Winn W, Allen S, Janda W, Koneman E, Procop G, Schreckenberger P, Woods G, 2006. Koneman’s Color Atlas and Textbook of Diagnostic Microbiology, 6th Edition. New York, NY: Lippincott Williams and Wilkins.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 12.

    Ryan KJ, Ryan KJ & Ray CG Sherris Medical Microbiology, 4th edition. New York, NY: McGraw Hill, 21–71.

  • 13.

    Deepak KG, Anita P, Bhaskar Th, Kalpana C, Sonat J, 2019. Occurrence of inducible clindamycin resistance in clinical isolates of Staphylococcus aureus in a tertiary care hospital. Int J Health Sci Res 9: 71–77.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 14.

    Adhikari RP, Shrestha S, Barakoti A, Amatya R, 2017. Inducible clindamycin and methicillin resistant Staphylococcus aureus in a tertiary care hospital, Kathmandu, Nepal. BMC Infect Dis 17: 483.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 15.

    Lyall KS, Gupta V, Chhina D, 2013. Inducible clindamycin resistance among clinical isolates of Staphylococcus aureus. J Mahatma Gandhi Inst Med Sci 18: 112–115.

  • 16.

    Bradely JR, 2005. Newer anti staphylococcal agents. Curr Opin Pediatr 17: 71–77.

  • 17.

    Kishk RM, Anani MM, Nemr NA, Soliman NM & Fouad MM. 2020. Inducible clindamycin resistance in clinical isolates of Staphylococcus aureus in Suez Canal University Hospital, Ismailia, Egypt. J Infect Dev Ctries 14: 1281–1287.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 18.

    Majhi S, Dash M, Mohapatra D, Mohapatra A, Chayani N, 2016. Nirupama Chayani: Detection of inducible and constitutive clindamycin resistance among Staphylococcus aureus isolates in a tertiary care hospital, Eastern India. Avicenna J Med 6: 75–80.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 19.

    Mazloumi MJ, Akbari R, Yousefi SJM, Letters B, 2021. Detection of inducible clindamycin resistance genes (ermA, ermB, and ermC) in Staphylococcus aureus and Staphylococcus epidermidis. Microbiol Biotechnol Lett 49: 449–457.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 20.

    Toleti S, Bobbillapati JR, Kollipaka SR, Myneni RB, 2015. Detection of inducible clindamycin resistance and susceptibilities to other antimicrobial agents in clinical isolates of Staphylococcus aureus. Int J Res Med Sci 3: 612–616.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 21.

    Jarajreh D, Aqel A, Alzoubi H, Al-Zereini W, 2017. Prevalence of inducible clindamycin resistance in methicillin-resistant Staphylococcus aureus: the first study in Jordan. J Infect Dev Ctries 11: 350–354.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 22.

    Singh T, Deshmukh AB, Chitnis V, Bajpai T, 2016. Inducible clindamycin resistance among the clinical isolates of Staphylococcus aureus in a tertiary care hospital. Int J Health Allied Sci 5: 111–114.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 23.

    Mokta K, Verma S, Chauhan D, Ganju SA, Singh D, Kanga A, Kumari A, Mehta V, 2015. Inducible clindamycin resistance among clinical isolates of Staphylococcus aureus from sub Himalayan region of India. J Clin Diagn Res 9: DC20–DC23.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 24.

    Mansouri S, Sadeghi J, 2014. Inducible clindamycin resistance in methicillin-resistant and -susceptible Staphylococcus aureus isolated from south east of Iran. Jundishapur J Microbiol 7: e11868.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 25.

    Bansal VP, Gadekar KS, Mulay MV, Mishra JK, 2019. Incidence of inducible clindamycin resistance in clinical isolates of staphylococci and their antibiotic sensitivity pattern. Int J Adv Res (Indore) 7: 1066–1073.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 26.

    Regha IR, Harichandran D, Sulekha B, 2016. Inducible clindamycin resistance among clinical isolates of Staphylococcus aureus in a tertiary care centre, Kerala, India. Curr Microbiol App Sci 5: 929–934.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 27.

    Steward CD, Raney PM, Morrell AK, Williams PP, McDougal LK, Jevitt L, McGowan JE Jr. , Tenover FC, 2005. Testing for induction of clindamycin resistance in erythromycin-resistant isolates of Staphylococcus aureus. J Clin Microbiol 43: 1716–1721.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 28.

    Azap OK, Arslan H, Timurkaynak F, Yapar G, Oruc E, Gagir U, 2005. Incidence of inducible clindamycin resistance in erythromycin-resistant isolates of Staphylococcus aureus. J Clin Microbiol 43: 1716–1721.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 29.

    Bottega A, Rodrigues Md A, Carvalho FA, Wagner TF, Leal IA, Santos SO, Rampelotto RF, Hörner R, 2014. Evaluation of constitutive and inducible resistance to clindamycin in clinical samples of Staphylococcus aureus from a tertiary hospital. Rev Soc Bras Med Trop 47: 589–592.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 30.

    Kawahito S, Kitahata H, Oshita S, 2009. Problems associated with glucose toxicity: role of hyperglycemia-induced oxidative stress. World J Gastroenterol 15: 4137–4142.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 31.

    Basu S, Ramchuran Panray T, Bali Singh T, Gulati AK, Shukla VK, 2009. A prospective, descriptive study to identify the microbiological profile of chronic wounds in outpatients. Ostomy Wound Manage 55: 14–20.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 32.

    Njunda AL, Assob NJC, Nsagha SD, Nde FP, Kamga FHL, Nkume AF, Kwenti TE, 2012. Uropathogens from diabetic patients with asymptomatic bacteriuria and urinary tract infections. Sci J Microbiol 1: 141–146.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 33.

    Rawat V, Singhai M, Kumar A, Jha PK, Goyal R, 2012. Bacteriological and resistance profile in isolates from patients with diabetes. N Am J Med Sci 4: 563–568.

Past two years Past Year Past 30 Days
Abstract Views 1602 934 56
Full Text Views 202 157 0
PDF Downloads 53 27 0
 
 
 
 
Affiliate Membership Banner
 
 
Research for Health Information Banner
 
 
CLOCKSS
 
 
 
Society Publishers Coalition Banner
Save