Inducible Clindamycin Resistant Staphylococcus aureus in Iran: A Systematic Review and Meta-Analysis
-
Ahmadreza Zarifian
,
Yasin Setayesh
,
Emran Askari
,
Aminreza Amini
,
Mohammad Rahbar
,
Mahboubeh Naderinasab
Abstract
Introduction: Staphylococcus aureus is a prominent human pathogen. One of the drugs used inthe treatment of staphylococcal infections (particularly infections of skin and soft tissue), is
clindamycin. Resistance to clindamycin includes two types: inducible and constitutive. Routine
laboratory methods of antibiotic susceptibility testing cannot detect the inducible type and Dtest is required for its detection. The purpose of this systematic review was to determine the
relative prevalence of this type of resistance in Iran.
Methods: Search terms "inducible clindamycin resistant", "D-test", "Staphylococcus aureus"
and "Iran" were used to find relevant articles in PubMed, Google Scholar and two Persian
search engines. Also, the abstracts of the recent national microbiology congresses were checked.
All studies used D-test to find iMLSB (inducible macrolide, lincosamide and streptograminB
resistance) phenotype among clinical isolates (not nasal swabs) of S. aureus, were included. In
order to perform meta-analysis, we used “comprehensive meta-analysis” software (ver. 2).
Results: In total, 9 articles and 8 abstracts related to the topic of the study were found. Random
effects meta-analyses showed a pooled estimate for percentage of iMLSB phenotype among
2683 samples of S. aureus was about 10% (95% confidence interval: 0.07-0.12). Using the fixed
effect model, the odds of positive iMLSB in methicillin-resistant S. aureus was about 5 times
more likely to occur in comparison with methicillin-susceptible S. aureus (95% CI: 3.49 to
7.76).
Conclusion: Fortunately, the relative frequency of inducible resistance to clindamycin in our
country is relatively low. However, we believe that D-test should be performed for all
erythromicin-resistant isolates in order to identify inducible resistance to clindamycin.
Moreover, reevaluation of inducible resistance to clindamycin in forthcoming years is highly
recommended.
Klevens RM, Edwards JR, Richards CL,
Horan TC, Gaynes RP, Pollock DA, et
al. Estimating health care-associated
infections and deaths in US hospitals,
Public Health Rep 2007; 122 (2):
Grundmann H, Aires-de-Sousa M,
Boyce J, Tiemersma E. Emergence and
resurgence of meticillin-resistant
Staphylococcus aureus as a publichealth threat. The Lancet 2006; 368
(9538): 874-85.
Noskin GA, Rubin RJ, Schentag JJ,
Kluytmans J, Hedblom EC, Jacobson C,
et al. National trends in Staphylococcus
aureus infection rates: impact on
economic burden and mortality over a
-year period (1998–2003). Clin Infect
Dis 2007; 45 (9): 1132.
Lowy FD. Staphylococcus aureus
infections. New England J of Med 1998;
(8): 520-32.
Sedighi I, Mashouf RY, Pak N, Rabiee
MAS. D-Test Method for Detection of
Inducible Clindamycin Resistance in
Staphylococcus aureus. Iranian J of
Pediatrics 2009; 19 (3): 293-7, 333.
Jawetz E, Melnick J, Adelberg E,
Brooks G, Butel J, Ornston L. Medical
microbiology: Prentice-Hall London;
Saderi H, Owlia P, Eslami M.
Prevalence of Macrolide-LincosamideStreptogramin B (Mls B) Resistance in
S. aureus Isolated from Patients in
Tehran, Iran. IJP 2009; 4 (4): 161-6.
Leclercq R. Mechanisms of resistance
to macrolides and lincosamides: nature
of the resistance elements and their
clinical implications. Clin Infec Dis
; 34 (4): 482.
Courvalin P, Leclercq R, Rice LB.
Macrolides, Lincosamides,
Streptogramins and Gram-Positive
Bacteria, LeClercq R. Antibiogram:
ESKA Publishing 2010: l299-322
Memariani m. Induction of clindamycin
resistance in clinical isolates of
Staphylococcus aureus enterotoxin gene
possessing. Tehran Univ Med J 1388;
(4): 250.
Daurel C, Huet C, Dhalluin A, Bes M,
Etienne J, Leclercq R. Differences in
potential for selection of clindamycinresistant mutants between inducible erm
(A) and erm (C) Staphylococcus aureus
genes. J of Clin Microb 2008; 46 (2):
NCCLS. Performance standards for
antimicrobial disk susceptibility test.
National Committee for Clinical
Laboratory Standards Wayne ePA PA;
Borenstein M, Hedges LV, Higgins JP,
Rothstein HR (2009) Publication bias.
In: Borenstein M, Hedges LV, Higgins
JP, Rothstein HR, editors. Introduction
to Meta-analysis. United Kingdom:
Wiley. 277–291.
Ansari Moghadam AR, Poorolajal J,
Haghdoost AA, Sadeghirad B, Najafi F,
editors (2011). Systematic review and
Meta-Analysis: Concepts, Applications
and Statistical Practices. Iran: Fanoos
Publishing. 175.
Deiham B, editor. Inducible
Clindamycin resistance in
Staphylococci isolated from clinical
samples in Dr.Ganjavian HospitalDezful. 4th Iranian Congress of Clinical
Microbiology 2010 9-11; Isfahan, Iran.
Emaneini M, Eslampour M, Sedaghat
H, Aligholi M, Jabalameli F, Shahsavan
S, et al. Characterization of phenotypic
and genotypic inducible macrolide
resistance in Staphylococci in Tehran,
Iran. J of Chemotherapy 2009; 21 (5):
-7.
Hashemizadeh Z, Bazargania A, Rahimi
M, Emami A, editors. Detection of
inducible clindamycin resistant in
methicillin resistant staphylococcus
aureus in namazi hospital by using DTest: 1387. 3rd Iranian Congress of
Clinical Microbiology; 2009 october 6-
; Shiraz, Iran.
Naderinasab m. Determine the inducible
resistance phenotype in methicillin
resistance staphylococcus aureus and
coagulase negative staphylococci.
Iranian J of Med Microb 1386; 1 (3):
Nafisi m. Prevalence of constitutive and
inducible resistance to clindamycin in
staphylococci isolates from Hajar and
Kashani hospitals in Shahrekord, 2008.
J of shahrekord Univ of Med Sci 1389;
(1):13.
Rahbar M, Hajia M. A Cross-Sectional
Report. Pakistan J of Bio Sci 2007; 10
(1):189-92.
Saderi H, Emadi B, Owlia P.
Phenotypic and genotypic study of
macrolide, lincosamide and
streptogramin B (MLSB) resistance in
clinical isolates of Staphylococcus
aureus in Tehran, Iran. Medical science
monitor: Inter Med J of Exp and Clin
Res 2011; 17 (2): BR48.
Shoja s. Detection of Inducible
Clidamycin Resistance in
Staphylococcus aureus and
Staphylococcus epidermidis by Using
D-Test. Pharma Sci 2009; 15 (1): 1.
Valizadeh V, Hasani A, Hasani A,
editors. Phenotypic differentiation of
inducible erm mediated resistant from
those with msra mediated in clinical
isoltes of staphylococcus aureus from a
university teaching hospital. 2nd Iranian
Congress of Clinical Microbiology;
October 7-9; Shiraz, Iran.
Zamanlou S, Kalavan YK, Shoja S,
editors. Study of antimicrobial
susceptibility pattern of Staphylococcus
aureus isolate from imam reza hospital
of urmia. The first Iranian international
congress of Medical bacteriology; 2011
September 5-8; Tabriz, Iran.
Saadat S, Solhjoo K, Noruz-nejad MJ,
Kazemi A, Rouhi R, editors. Survey on
susceptibility of methicilin resistance
Staphylococcus aureus strains to
linezolid, teicoplaninand and
quinopristin dalfopristin. 5th Iranian
Congress of Clinical Microbiology;
November 8-10; Shiraz, Iran.
Mahdipour S, Esmaeilpanah S, Askari
E, Naderinasab M, editors. First
description of a new resistance pattern
to Macrolide, Lincozamide and
Streptogramins (MLS) from Iran: the
LSA phenotype. 5th Iranian Congress of
Clinical Microbiology; 2011 November
-10; Shiraz, Iran.
Shahsavan S, Emaneini M, Noorazar
Khoshgnab B, Khoramian B, Asadollahi
P, Aligholi M, et al. A high prevalence
of mupirocin and macrolide resistance
determinant among Staphylococcus
aureus strains isolated from burnt
patients. Burns 2011.
Seifi N, Kahani N, Askari E, Mahdipour
S, Naderi NM. Inducible clindamycin
resistance in Staphylococcus aureus
isolates recovered from Mashhad, Iran.
Iranian J of Microb 2012; 4 (2): 82.
Kiyni-Niya M, Hasani A, Hassani A,
Ghorbani Z, Fard MS, SeifollahPoor E,
et al., editors. Inducible Clindamycin
Resistance Due to Expression of Erm
and Msr Genes in Staphylococcus
aureus: Report from Teaching
Hospitals of Tabriz University of
Medical Science The 13th Iranian &
The Second International Congress of
Microbiology; 2012 July 14–16;
Ardabil University of Medical Sciences,
Iran.
Yilmaz G, Aydin K, Iskender S, Caylan
R, Koksal I. Detection and prevalence
of inducible clindamycin resistance in
staphylococci. J of Med Microbiol
; 56 (3): 342.
Fiebelkorn K, Crawford S, McElmeel
M, Jorgensen J. Practical disk diffusion
method for detection of inducible
clindamycin resistance in
Staphylococcus aureus and coagulasenegative staphylococci. J of Clin
Microbiol 2003; 41 (10): 4740.
Adaleti R, Nakipoglu Y, Ceran N,
Tasdemir C, Kaya F, Tasdemir S.
Prevalence of phenotypic resistance of
Staphylococcus aureus isolates to
macrolide, lincosamide, streptogramin
B, ketolid and linezolid antibiotics in
Turkey. Braz J Infect Dis 2010; 14 (1):
-4.
Gunduz T, Akgul S, Ozcolpan G,
Limoncu ME. Investigation of Inducible
Clindamycin Resistance among Clinical
Isolates of Staphylococci. Afr J
Microbiol Res 2012; 6 (10): 2294-2298.
Gul HC, Kilic A, Guclu AU, Bedir O,
Orhon M, Basustaoglu AC. Macrolidelincosamide-streptogramin B resistant
phenotypes and genotypes for
methicillin-resistant Staphylococcus
aureus in Turkey, from 2003 to 2006.
Pol J Microbiol 2008; 57 (4): 307-12.
Huang H, Flynn NM, King JH,
Monchaud C, Morita M, Cohen SH.
Comparisons of community-associated
methicillin-resistant Staphylococcus
aureus (MRSA) and hospital-associated
MSRA infections in Sacramento,
California. J Clin Microbiol 2006 Jul;
(7): 2423-7.
Mishra SK, Rijal BP, Pokhrel BM.
Emerging threat of multidrug resistant
bugs--Acinetobacter calcoaceticus
baumannii complex and methicillin
resistant Staphylococcus aureus. BMC
Res Notes 2013; 6 (98).
Patil NR. Inducible clindamycin
resistance among clinical isolates of
methicillin resistant staphylococcus
aureus. Int J Cur Res Rev 2013; 5 (1):
-48.
Mohanasoundaram KM. The prevalence
of inducible clindamycin resistance
among gram positive cocci from various
clinical specimens. J Clin Diagn Res
; 5 (1): 38-40.
Sasirekha B, Usha MS, Amruta JA,
Ankit S, Brinda N, Divya R. Incidence
of constitutive and inducible
clindamycin resistance among hospitalassociated Staphylococcus aureus.
Biotech 2011; 1-5.
Abimanyu N, Murugesan S, Krishnan P.
Emergence of methicillin-resistant
Staphylococcus aureus ST239 with
high-level mupirocin and inducible
clindamycin resistance in a tertiary care
center in Chennai, South India. J Clin
Microbiol 2012; 50 (10): 3412-3.
Lavallée C, Rouleau D, Gaudreau C,
Roger M, Tsimiklis C, Locas MC,
Gagnon S, Delorme J, Labbé AC.
Performance of an agar dilution method
and a Vitek 2 card for detection of
inducible clindamycin resistance in
Staphylococcus spp. J Clin Microbiol
; 48 (4): 1354-7.
Pardo L, Vola M, Macedo-Viñas M,
Machado V, Cuello D, Mollerach M,
Castro M, Pírez C, Varela G, Algorta G.
Community-associated methicillinresistant Staphylococcus aureus in
children treated in Uruguay. J Infect
Dev Ctries 2013; 7 (1): 10-6.
Amorim ML, Faria NA, Oliveira DC,
Vasconcelos C, Cabeda JC, Mendes
AC, Calado E, Castro AP, Ramos MH,
Amorim JM, de Lencastre H. Changes
in the clonal nature and antibiotic
resistance profiles of methicillinresistant Staphylococcus aureus isolates
associated with spread of the EMRSA-
clone in a tertiary care Portuguese
hospital. J Clin Microbiol 2007; 45 (9):
-8.
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| Issue | Vol 4 No 1-2 (2015) | |
| Section | Original Articles | |
| Keywords | ||
| Staphylococcus aureus Inducible resistance Cindamycin Iran Systematic review | ||
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