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 Table of Contents  
ORIGINAL ARTICLE
Year : 2021  |  Volume : 5  |  Issue : 2  |  Page : 161-167

Clinicobacteriological study of pyoderma with trends in antibiotic sensitivity at a tertiary care center in western India


1 Department of Dermatology, B J Medical College and Sassoon Hospital, Pune, Karnataka, India
2 Department of Dermatology, KLE Academy of Higher Education and Research's, JNMC, Belagavi, Karnataka, India
3 Department of Microbiology, B J Medical College and Sassoon Hospital, Pune, Maharashtra, India

Date of Submission08-Apr-2020
Date of Decision19-Aug-2020
Date of Acceptance06-Oct-2020
Date of Web Publication26-Aug-2021

Correspondence Address:
Bhavana Ravindra Doshi
Department of Dermatology, KLE Academy of Higher Education and Research's, JNMC, Belagavi, Karnataka
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/CDR.CDR_67_20

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  Abstract 


Background: Pyoderma refers to any pus-forming infection of the skin. Antibiotic resistance has significantly downplayed the utility of established antibiotics and possesses a serious threat to public health. Objective: To study the causative organisms, their trends of antibiotic sensitivity pattern thus helping in prescribing appropriate antibiotics and study the response to the treatment in patients of pyoderma. Materials and Methods: A 2-month prospective study on a cohort of 30 pyoderma patients attending the outpatient and inpatient department in our tertiary care hospital under ICMR short-term studentship was undertaken. Statistical analysis was performed using the SPSS software version 24. Results: Those in 5th–6th decade were more predisposed. Higher incidence was seen in anemics. Staphylococcus spp. (26/30 case 86.66%) was the most common organisms to be isolated in 12/15 (80%) outpatients and 14/15 (93.33%) inpatients. Methicillin-resistant Staphylococcus aureus (MRSA) was isolated equally (33.33%) in both outpatient and inpatients, with increasing trend in MRSA in out-patients. Higher incidence of Pseudomonas aeruginosa in outpatients was noted. MRSA in superficial pyoderma group was sensitive to one first-line drug which was gentamycin, whereas in deep pyoderma, the only first-line drug to which the MRSA was 100% sensitive was ciprofloxacin. All MRSA, MSSA, MR CONS, and MS CONS were sensitive to all second-line drugs. Sixty-percent patients who showed no response to empirical primary line of treatment showed good response on changing the antibiotics according to the reports of culture and sensitivity. Conclusion: An increasing trend in MRSA in outpatients was noticed along with higher incidence of Pseudomonas infection. Limitation: Small sample size.

Keywords: Methicillin-resistant Staphylococcus aureus, pseudomonas, pyoderma


How to cite this article:
Chavan K, Doshi BR, Dohe V. Clinicobacteriological study of pyoderma with trends in antibiotic sensitivity at a tertiary care center in western India. Clin Dermatol Rev 2021;5:161-7

How to cite this URL:
Chavan K, Doshi BR, Dohe V. Clinicobacteriological study of pyoderma with trends in antibiotic sensitivity at a tertiary care center in western India. Clin Dermatol Rev [serial online] 2021 [cited 2021 Dec 1];5:161-7. Available from: https://www.cdriadvlkn.org/text.asp?2021/5/2/161/324572




  Introduction Top


Pyoderma presents clinically as any pus-forming infection of the skin accounting for nearly 25% of the patients attending the dermatology outpatient department in India.[1]

They can be either primary pyoderma, i.e., de novo or secondary pyoderma as a complication of other underlying systemic disease or due to immunocompromised status or when a lesion is already present and then bacterial infection sets in it, for example, trophic ulcers in leprosy patients. Staphylococcus aureus is considered to be the most common causative organism implicated in its etiology; however, other organisms such as those belonging to Streptococcus or Pseudomonas species have also been incriminated.[2],[3] Rarely organisms from Enterobactericeae family are also involved which is not confirmed though.

Identification of the causative pathogen by pus culture and sensitivity helps in accurate treatment; but this may not be usually done due to logistic issues. Empirically antibiotics are given without knowing the complete profile of the causative organism. In today's scenario, many cases do not respond to those antibiotics that were previously known to be very effective in such cases. The indiscriminate use of topical and oral antibiotics has contributed to this current situation.[3] As a result, antibiotic resistance has downplayed the utility of established antibiotics and possesses a serious threat to public health worldwide, for example, methicillin-resistant S. aureus (MRSA). Hence, in order to maximize the treatment outcome in cases of pyoderma, detailed knowledge of the various causative organisms and their sensitivity pattern are needed.

Our project aimed to study the causative organisms of pyoderma and their antibiotic susceptibility pattern for prescribing appropriate antibiotic as per the sensitivity tests after correlating it with patient's clinical status. Patient's follow-up and records were maintained, and response was studied. An attempt to determine the response to change in the treatment after culture and sensitivity was also made.


  Materials and Methods Top


A prospective study under ICMR short-term studentship was undertaken on a cohort of 30 consecutive consenting patients attending the skin outpatient and inpatient department at Sassoon General Hospital, Pune, from July 1, 2013, up to August 31, 2013. The study included patients diagnosed with pyoderma who had not previously taken any systemic or topical antibiotics 1 month before presentation.

After the Institutional Ethics Committee approval, the demographic and clinical details of consenting patients were noted. After clinical examination, the affected area was cleaned with normal saline, and the pus was collected with the help of two swabs, one of which was sent for Gram stain and the other for culture. If adequate pus was seen in the lesion, then an aspirate was taken from the same and sent to the microbiology department. Empirically commonly used antibiotic was then prescribed, and the patient was asked to come for follow-up after a week to decide upon change in treatment medications if required.

Pus samples were inoculated into blood agar and MacConkey agar,[4] and organisms were identified by the standard conventional methods. Muller-Hinton agar was used to study antibiotic sensitivity pattern by the Kirby–Bauer disc-diffusion method as per the clinical laboratory standard institute (CLSI) guidelines.[5] Diameter of the zone of inhibition of growth was recorded and interpreted as susceptible or resistant by the criteria of CLSI. Organisms with “intermediate” levels of resistance were included in the percentage of resistant organisms. Extended-spectrum beta lactamase was detected using the CLSI guidelines.[5] Staphylococcus spp. was tested for methicillin resistance by using cefoxitin disk where the diameter of sensitivity for S. aureus is 22 mm and for coagulase-negative Staphylococcus (CONS) is 25 mm. D test[5] was performed for erythromycin and clindamycin to study inducible macrolide resistance. After the identification of causative organism, its sensitivity pattern was correlated with patient's condition and appropriately changed antibiotic was given, and response was studied in the subsequent follow-up after 1 week. The relevant data were recorded, and statistical analysis was analyzed using the SPSS software version 24.


  Results Top


Out of 30 patients in the study, 5 were <19 years. A total of seven patients were between 20 and 39 years age. 40–59 years' age group had the maximum, i.e., 11 patients, whereas only 6 were found in above 60 years' age group. Maximum number of patients (17) of pyoderma were above 40 years. The age range of involvement being between 2.5 and 71 years.

Of the 30 patients diagnosed with pyoderma, 18 were male and 12 were female. Male-to-female ratio was 3:2. It was seen that male patients have a greater rate of occurrence of pyoderma as compared to females.

The prevalence in outpatient (over 2 months period) - (15/5500) × 100 = 0.2727%.

Patients who had taken previously antibiotic were excluded; hence, the number of pyoderma patients included in this study dropped down and plus patients with other ailments had multiple visits.

The prevalence in inpatient (15/155) × 100 = 9.677%.

Of the 30 patients, 14 had superficial pyoderma and 16 had deep pyoderma [Table 1]. Acne, folliculitis, and furunculosis were the most common skin condition associated with superficial pyoderma, and pemphigus was the most common skin condition associated with deep pyoderma, as shown in [Table 2].
Table 1: Pattern of infection and out-patient department/in-patient department patients

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Table 2: Clinical profile of pyodermas

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The average duration of lesions ranged between 7 days and 3 years. The common site of lesions was the lower limb (16), face (15), upper limb, (6) trunk, and (9) scalp (4). The common type of lesions encountered were erosions (9), ulcers (8), pustules (7), and nodules (6). Majority of the patients in the study had multiple skin lesions (12/30), whereas solitary lesion was found in seven patients (7/30). The most common underlying condition in outpatients was secondary pyoderma (5), whereas the common underlying condition in inpatients was pemphigus (5) [Table 3].
Table 3: Conditions associated with pyodermas in outpatient department and inpatient department patients

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Patients with abnormal total leukocyte count (<4000 or more than 11,000) were seen in four cases, whereas 15 patients had low hemoglobin (Hb) (<12 gm%). Underlying immunosuppression due to steroids and immunosuppressive agents was seen in (7) due to diabetes in (2) and secondary to HIV in (1) case [Table 4]. shows P < 0.001 which showed highly significant association between the presence of underlying systemic disease and type of infection indicating an increased association of deep pyoderma with underlying systemic diseases.
Table 4: Distribution of patients according to the pattern of infection and underlying disease

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The most common organism isolated from pus was methicillin-sensitive S. aureus (MSSA) and MRSA in 10 cases each followed by methicillin-resistant CONS (MR CONS) in four cases, Pseudomonas aeuroginosa in four cases, MS CONS in two cases, and Proteus mirabilis and Escherichia coli in one case each. The most common organism isolated in outpatients was MSSA, isolated in a total of 6 cases. MRSA in 5, Pseudomonas in 3 and MS CONS in 2 cases and Proteus mirabilis and E. coli in one case each. Most common organism isolated in inpatients was MRSA, isolated in 5 of the total inpatient cases. MR CONS and MSSA in four cases each. MS CONS and Pseudomonas aeruginosa were isolated in one case each [Table 5].
Table 5: Pathogens responsible for pyoderma total=32*

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MRSA among superficial pyoderma was sensitive to all 2nd-line drugs and only one 1st-line drug which was gentamicin in most of the cases, whereas in deep pyoderma, the only drug to the MRSA was sensitive was found to be ciprofloxacin. All MRSA, MSSA, MR CONS, and MS CONS were sensitive to all 2nd-line drugs, but Pseudomonas and other organisms were sensitive to only few 1st line and few 2nd line of drugs [Table 6].
Table 6: Culture and sensitivity pattern in superficial and deep pyodermas

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Sensitivity pattern to various antibiotics tested is shown in [Table 7].
Table 7: Sensitivity pattern observed in outpatient department and inpatient department patients

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A total of six patients responded well to empirical treatment started and hence continued on previous treatment as patients showed sensitivity to the same drug in vitro too. Eighteen patients showed no response to empirical therapy but responded well to treatment on changing the medication as per the sensitivity pattern. However, in six cases, some other antibiotic was given independent of culture sensitivity when due to some reasons certain drugs could not be prescribed to the said patient and the patients responded well, for example, in this study mupirocin and nadifloxacin were such type of drugs used [Table 8].
Table 8: Response to change of treatment

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  Discussion Top


In all, we studied 30 cases of pyoderma. The maximum number of patients of pyoderma belong to 40–59 years (11/30) 36.66%. Males were affected more than females in this study (18/30), as has also been reported by Malhotra et al.,[6] Patil et al.,[7] and others. The prevalence in outpatient over a 2-month period was noted to be 0.2727% and 9.677% in in-patients in our study.

In our study, primary pyoderma constituted 23.3% of cases which was similar to the study by Malhotra et al.,[6] i.e., 19.67% cases. A higher incidence of secondary pyoderma was seen in our study 23/30 (76.6%). Furthermore, in-patients showed high tendency of association with deep pyoderma than outpatients. On the other hand, superficial pyoderma was more common in outpatients.

Out of 7/30 (23.33%) cases of primary pyoderma, three cases (10%) were each of folliculitis and furunculosis. Folliculitis and furunculosis were the most common primary pyodermas, seen in 58.8% and 33.3% of cases, respectively, in a study by Patil et al.[7] on out patients in Western India. In the study by Singh et al.,[8] primary pyoderma was encountered in 61% cases and 39% presented with secondary pyoderma. However, their findings were limited to outpatients.

The cases of primary pyoderma in our study were much less in their comparison. In a study done by Malhotra el al.[6] on in patients, impetigo formed the largest group followed by carbuncle and folliculitis. Similar high incidence of impetigo has been reported by others.[9] Majority of our patients were adults, which could account for the high frequency of folliculitis and furunculosis. Singh et al.[8] too reported that furunculosis (27.2%) followed by folliculitis (13.2%) was more common than impertigo (9.4%) in their study.

Among the secondary pyoderma with a specific diagnosis, infected pemphigus was the most common diagnosis (5/30), followed by Hansen's disease (4/30). Malhotra et al.[6] too reported pemphigus vulgaris as the most common secondary pyoderma in their study. Stevens Johnson syndrome was the second most common cause of secondary pyoderma in their study.

15/30 (50%) patients were found to have a low Hb (<12 gm%). Anemia as a predisposing cause that increases susceptibility to infection seems to be true to a certain extent. A few studies by Musher et al.[10] have already shown a strong association between anemia and infections due to Gram-positive bacteria. A total of 12/30 (40%) cases in our study had underlying immunosuppression of which 9 were secondary to use of corticosteroid alone (8) and in combination with cyclophosphamide (1). Two patients were immunosuppressed due to underlying diabetes and one secondary to HIV. 10/12 cases (83.3%) among these immunosuppressed showed the presence of deep pyoderma indicating a higher rate of occurrence in them. In bacteriological analysis, we observed that Staphylococcus spp. (26/30 case 86.66%) was the most common organisms to be isolated (12/15 [80%] outpatients and 14/15 [93.33%] in the inpatients). In similar study done by Patil et al.[7] on out-patients, 81.4% isolates were Staphylococcus spp. Malhotra et al.[6] in an inpatient study in Northern India had Staphylococcus spp. isolated in 59.01%. S. aureus was isolated from 78.26% samples followed by E. coli 4.79%, Streptococcus haemolyticus (2.17%), Citrobacter spp. (2.17%), coagulase-negative Staphylococcus (1.74%), and P. aeruginosa (1.74%) in the study by Singh et al.[8] In our study, a very high incidence of Staphylococcus spp. existed in both inpatients and outpatient groups, this could be due to a small sample size of our study.

S. aureus and Streptococci are considered to be the main etiological agents of cutaneous bacterial infections and these have been isolated in different proportions of cases in studies in India and abroad.[4] Among the Staphylococcal spp. in our study, MRSA and MSSA were isolated in ten cases (33.33%), respectively. Inpatient study by Malhotra et al.[6] reported MRSA in 6/61 cases (9.83%). Our study MRSA was isolated in 5/15 (33.33%) followed by MSSA in and MR CONS in 4/15 (26.6%) cases each in the inpatients studied. Among the outpatient group, MSSA was isolated in 6/15 (40%), MRSA in 5/15 (33.33%) and Pseudomonas spp. in 3/15 and MS CONS in 2/15 cases and Proteus mirabilis and E. coli in one case each. Staph isolates were most common in our study; similarly, a high incidence of coagulase-positive Staphylococcus in pyoderma has been reported by several workers.[11] Coagulase-negative strains have also been reported to be etiological agents.[12]

P. aeruginosa which is associated with deep pyoderma usually was isolated equally in 2/15 cases (13.33%) of superficial and deep pyoderma in our study. Furthermore, surprisingly, outpatient group 3/15 cases (20%) showed Pseudomonas spp. as the affecting organism. Pseudomonas spp. as an isolate was not found in the outpatient study by Patil et al.[7] nor in the in-patient study by Malhotra et al.[6] Hence, in our study, four cases with the isolates of Pseudomonas seem a little alarming as the primary line of treatment for pyodermas does not cover Pseudomonas and culture sensitivity thus proved important.

S. pyogenes from 2.3% was seen in outpatients study by Patil et al.[7] and 3.27% in inpatient by Malhotra et al.[6] However, Streptococcus spp. was not isolated in our study. The other organisms isolated in outpatients in this study were Proteus mirabilis and E. coli in 1/15 case each (6.66%). These organisms were not isolated in the outpatient study by Patil et al.[7] However, inpatients in the study by Malhotra et al.[6] isolated Klebsiella spp. in 4.92%, Streptococcus spp., Enterococcus spp., and Proteus spp. in 3.27% each and Citrobacter spp. and E. coli in 1.64%. A combination of Staphylococcus + Streptococcus was found in one case (1.64%), and combinations of Staphylococcus + Enterococcus and E. coli + Enterococcus in two cases (3.28%) each. No inpatient in our study showed the above isolates.

In our study, single affecting organism was isolated in 28/30 cases (93.33%), 2/30 (6.66%) cases showed more than one type of organism (Pseudomonas + Proteus in deep pyoderma and MSSA + E. coli in one case of superficial pyoderma). Malhotra et al.[6] reported a single infecting organism in 80.33% and more than one type of organism in 4.92% and no organism in 14.75%. Singh et al.[8] too reported the single organism in 94% samples, no organism in 5.22%, and two organisms in 0.43% samples.

The first-line drugs for MRSA, MSSA, MR CONS, and MS CONS tested in our study were as follows: Penicillin, ciprofloxacin, tetracyclines, gentamycin, erythromycin, clindamycin, and cotrimoxazole. Second-line drugs for MRSA, MSSA, MR CONS, and MS CONS tested were vancomycin, linezolid, and teicoplanin. In our study, both MRSA (6/14) among superficial pyodermas and deep pyoderma (4/14) were sensitive to all 2nd-line drugs (vancomycin 100%, linezolid 100%, and teicoplanin 100%). However, in 4/6 (66.6%) MRSA in superficial pyoderma group were sensitive one 1st line drug which was gentamicin, whereas in deep pyodermas, the only first-line drug to which the MRSA were 100% sensitive was found to be ciprofloxacin. As gentamicin could be administered on OPD basis, ciprofloxacin which was the second most sensitive drug was administered to the patient after the culture reports. MSSA isolates in both superficial (5/14) and deep pyoderma (5/16) were sensitive to almost all 1st line and all 2nd line drugs. All MRSA, MSSA, MR CONS, and MS CONS were sensitive to all 2nd line drugs. Pseudomonas and other organisms were 100% sensitive to only few 1st line (amikacin, ciprofloxacin, and imipenem) and few 2nd line of drugs.(piperacillin + tazobactum). All patients in case of Gram-negative or Pseudomonas infections were sensitive to piperacillin-tazobactam.

In outpatient series by Patil et al.,[7] the sensitivity of S. aureus strains to other antibiotics varied. All the strains were sensitive to vancomycin and sisomycin. They showed minimal resistance to first-generation cephalosporin and gentamicin (1.4%). Resistance was greatest to penicillin (87.2%), followed by that to erythromycin (42.9%) and framycetin (35.7%), an antimicrobial used for topical application. Resistance to ciprofloxacin was 17.2%. Inpatient study by Malhotra et al. showed most of coagulase-positive strains of Staphylococcus were susceptible to amikacin (100%), gentamicin (66%), and ciprofloxacin 52.4%. Coagulase-negative Staphylococci were largely susceptible to amikacin (77.7%) and gentamicin (66.6%) but showed relatively low susceptibility to ampicillin (55.5%), erythromycin (44.4%), and gatifloxacin (33.3%). In the study by Singh et al.,[8] S. aureus was highly susceptible (>80%) to amoxicillin plus sulbactam, amikacin, cefoperazone, tobramycin, and amoxicillin plus clavulanate, and moderately susceptible (70%–77.2%) to gentamicin, ampicillin plus sulbactam, linezolid, cefotaxime, and ceftizoxime. Low susceptibility (8.3%–14.6%) was noted to fluoroquinolones and cephalexin. S. haemolyticus was most susceptible (100%) to linezolid and amoxicillin plus sulbactam. E. coli was highly susceptible (>80%) to amikacin, tobramycin, and ceftriaxone plus sulbactam. P. aeruginosa showed a high susceptibility (100%) to polymyxin, and moderate susceptibility (75%) to piperacillin, levofloxacin, and ciprofloxacin. In our study, it was seen that for all Gram-positive organisms 84.61% out-patients were sensitive to gentamicin, 53.33% to ciprofloxacin, 46.15% to clindamycin, 38.4% to tetracycline, 30.77% to erythromycin, and 15.38% to cotrimoxazole. In the inpatient group, 35.71% were sensitive to gentamicin, 53.33% for ciprofloxacin, 28.57% to clindamycin, 21.43% to tetracycline, 28.57% to erythromycin, and 14.29% to cotrimoxazole. In case of penicillin, almost all patients were resistant. All outpatients and inpatients were sensitive to vancomycin, teicoplanin, linezolid.

For other Gram-negative bacilli and P. aeruginosa it was found that in outpatient group 60% were sensitive to amikacin, 75% to imipenem, meropenam and 66.67% to cefotaxime, 75% to aztreonam. Among the in-patients those sensitive to amikacin were 75%. 100% toimipenem. 75% in-patients were sensitive to aztreonam. All out-patient and in-patients in case of Gram-negative or Pseudomonas infections were sensitive to piperacillin-tazobactam.

6/30 cases (20%) patients in our study showed response to primary line of treatment (amoxycillin/azithromycin/ciprofloxacin and framycetin, clindamycin topically), hence treatment in these were continued irrespective of the culture sensitivity report. 18/30 (60%) patients who showed no response to empirical primary line of treatment showed good response on changing the antibiotics according to the reports of culture and sensitivity.

In 6/30 (20%) patients due to other reasons leading to prescription restrictions due to underlying medical condition; independent of culture sensitivity some other antibiotic was given which was not tested in vitro and patient responded well. In this study, mupirocin and nadifloxacin were such type of drugs used. Hence, culture sensitivity in these cases helped to avoid prescription of the large number of antibiotics to which patients would not have responded and thus to reduce the cost of overall treatment and patient's exposure to many antibiotics which were unnecessary.


  Conclusion Top


Staphylococcus spp. (26/30 case 86.66%) was the most common organisms to be isolated in (12/15 (80%) outpatients and 14/15 (93.33%) in the inpatients. MRSA was isolated equally in (33.33%) in both outpatients and inpatients, showing the increasing trend in MRSA infection in out-patient group. Whether a higher incidence of P. aeruginosa in out-patient group is suggestive of new trend in infection pattern is true or speculative is difficult to say. A bigger sample size would be required to comment clearly on this finding.

MRSA in superficial pyoderma group was sensitive one 1st line drug which was gentamicin, whereas in deep pyodermas the only first-line drug to which the MRSA were 100% sensitive was found to be ciprofloxacin. All MRSA, MSSA, MR CONS, and MS CONS were sensitive to all 2nd line drugs.

More than one organism was isolated in two of our case both of which had a difference in sensitivity pattern, hence emphasizing the need for culture sensitivity to be done for further treatment. Forty percent cases of pyoderma in our study had underlying immunosuppression with increased the occurrence of deep pyoderma.

Sixty percent patients who showed no response to empirical primary line of treatment showed good response on changing the antibiotics according to reports of culture and sensitivity emphasizing that in-vitro testing is essential as knowledge of the causative organisms and resistance patterns can help us select appropriate antibiotics without wasting time in using resistant drugs.

However, a study with much larger sample size would be required to validate the findings of our study.

Declaration of patient consent

The authors certify that they have obtained all appropriate patient consent forms. In the form the patient (s) has/have given his/her/their consent for his/her/their images and other clinical information to be reported in the journal. The patients understand that their names and initial s will not be published and due efforts will be made to conceal their identity, but anonymity cannot be guaranteed.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
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    Tables

  [Table 1], [Table 2], [Table 3], [Table 4], [Table 5], [Table 6], [Table 7], [Table 8]



 

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