Eurosurveillance

ECDC

Surgical Site Infections and Antibiotic Resistance of Causal Agents in the Hospitals of Kiev, Ukraine

 Rediger
  Published: 14.12.09 Updated: 08.01.2010 12:51:28

A. Salmanov
Department of organization of epidemiological surveillance, Ministry of Health of Ukraine, Kiev, Ukraine

Citation: Salmanov A. Surgical site infections and antibiotic resistance of causal agents in the hospitals of Kiev, Ukraine.EpiNorth.2009;10(3):120-27.

Abstract
This article presents an analysis of the incidence of surgical site infections (SSIs) and describes the current views on etiology and the problems of antibiotic resistance of infectious agents in the surgical hospitals of Kiev. The etiological structure and data on antibiotic resistance of agents causing SSIs based on the results of microbiological investigations of clinical material is presented. In addition, some conditionally pathogenic microorganisms were identified as the main causal agents of nosocomial pyoinflammatory infections resistant to antimicrobial medicines. Recommendations concerning microbiological monitoring and antimicrobial therapy are provided.

Introduction
Challenges related to the prophylaxis and therapy of post-surgical pyoinflammatory infections are extremely relevant. According to the state statistical reports, surgical site infections (SSIs) are the most frequent post-surgical complications in Ukraine with incidences from 3% to 35% [1,2]. One of the reasons for SSIs is the wide spread of conditionally pathogenic microorganisms (CPMs) that are resistant to antimicrobial medicines and cause nosocomial infections [1]. Every year resistant nosocomial infections are becoming more and more pressing for medical specialists in Ukraine.

Current guidelines for the treatment of infections recommend the immediate prescription of antimicrobial medicines as soon as the infection is diagnosed. Broad spectrum antimicrobials should be prescribed even before the culture results are known in order to cure the most probable infection agents. Targeted antibacterial treatment should be provided following the identification of an etiological agent and resistance status [3]. However, the results of numerous investigations prove that the prescription of an inadequate starting therapy raises the mortality rate among patients with severe infections by 1.5 – 3 times [4-7]. In addition, inadequare therapy extends the duration of hospitalisation and provokes a need for additional courses of antimicrobial therapy that makes treatment more expensive [8].

Epidemiological control in surgical hospitals is provided through continuous microbiological monitoring to reveal, identify and register various infections, their symptoms, development tendencies and sensitivity to antimicrobial medicines. This data provides a foundation for developing a strategy for the use of antibiotics in surgery hospitals. The microbiological diagnostics of infections (identification of pathogens and sensitivity to antibiotics) is necessary  for optimal antimicrobial therapy. However, data on the etiology and resistance of pathogens associated with nosocomial infections in surgical hospitals varies considerably [9-11]. Thus it is necessary to continuously monitor SSIs in every surgical hospital to identify the prevailing causal agents of nosocomial infections and establish systematic epidemiological control over antibacterial resistance at the local, regional and national levels. The goal of this investigation was to analyse the results of  patients’ surgery, to determine the incidence rate of SSIs and to identify the prevailing pathogens and resistance to antimicrobial medicines in Kiev.

Materials and Methods
In accordance with state statistical reports, an average of 150,000 surgeries are conducted annually in surgical hospitals in Kiev. However, only 3 – 4 cases of SSIs are officially registered per year (0.0009% per 100 surgeries), 75 times less than the national average rate in Ukraine (0.07% per 100 surgeries) [2]. Results of our investigation revealed a much higher SSI incidence rate that reported in the official statistical data.

The investigation included 49,920 patients who underwent surgeries during 2008 in 7 of the 10 surgical hospitals in Kiev that are similar in terms of medical equipment, laboratory facilities and number of surgeries performed. In order to determine the incidence rates of SSIs in the participating hospitals, passive search (through records from medical officers) and active identification (through epidemiological diagnostics) were used. The investigation was based on the standard definition of an SSI as purulent discharge from a surgical wound and the identification of microorganisms in the liquid or tissue at the surgical site. The information was collected using tables for the standard criteria of SSI diagnostics that were developed by the Centers for Disease Control and Prevention (Atlanta, USA) [12] and adopted for use in Ukraine. Information from the microbiological laboratory reports and other types of medical documents was also considered.

The investigation included the analysis of  4,027 strains of conditionally pathogenic microorganisms from biological material obtained from patients with clinical symptoms. The clinical sample consisted of laboratory-diagnosed SSIs that emerged no less than 48 hours after a surgery. Bacterial strains obtained for a second time from the same patients were not subject to analysis.
Analysis of biological material and interpretation of results were performed in accordance with the approved rules for clinical material selection, analysis and interpretation of results. Microorganisms were identified based on Bergey's classification and standard bacteriological methods [13].

Antibiotic resistance was studied using WHONET software version 5.1 developed by WHO [14]. The analysis of statistical data was performed using Microsoft Excel.

Results
Surgery results of 49,920 patients in 7 hospitals in Kiev during 2008 were analysed. The patients’ age ranged from 17 to 84. The surgeries were performed to cure diseases of digestive organs and abdominal cavity (24,932 cases), nonincarcerated hernias (4,312 cases), and skin and hypoderm diseases (20,676 cases). Data analysis demonstrated that 4,027 patients developed SSIs post surgery ( 8.1 per 100 surgeries, confidence interval 95% 7.2 – 9.0% per 100 operations).

The analyses of etiological SSI agents showed that 70.1% of the microorganisms obtained (2,824 of 4,027) from surgery wounds were gram-positive and 29.9% (1,203 of 4,027) were gram-negative (Table 1).

Table 1. Comparative analysis of SSI agents among patients in hospitals of Kiev in 2008 (n=4,027)

 

Microorganisms / Микроорганизмы

 

 

Number of strains / Количество

штаммов

Proportion (%) / Удельный вес

(%)

1

Staphylococcus aureus

1415

35.1

2

Staphylococcus epidermidis

816

20.3

3

Streptococcus рyogenes

207

5.1

4

Enterococcus faecalis

343

8.5

5

Enterococcus faecium

43

1.1

6

Escherichia coli

390

9.7

7

Enterobacter aerogenes

353

8.8

8

Klebsiella pneumoniae

15

0.4

9

Proteus vulgaris

9

0.2

10

Pseudomonas aeroginosa

292

7.3

11

Acinetobacter baumanni

144

3.6

Patients with SSI staphylococci had the highest proportion of CPM (55.4%) followed by enterobacteria (19%). The etiological role was lower for Streptococcaceae (14.7%) and Pseudomonadaceae(Pseudomonas aeruginosa) (7.3%). The remaining 3.6% included various other CPM.

Our results correspond to data of other investigators on the prevailing species of CPMs that cause SSIs in the hospitals. The distribution of various groups of microorganisms varies considerably [1, 15, 16]. This proves the necessity of carrying out microbiological monitoring in every surgery hospital.

The prevailing causal agents of SSIs were resistant to many antimicrobial medicines used in the hospitals. Resistant SSI agents were identified among gram-positive (Table 2) and gram-negative (Table 3) microorganisms.

Table 2. Resistance to antimicrobial medicines of the most common gram-positive agents causing SSIs in hospitals in Kiev in 2008 (n=2638)

 

Antimicrobal medicine / антимикробные

препараты

 

Microorganisms / микроорганизмы

S.aureus

S.epidermidis

S.рyogenes

E.faecalis

Tested

strains / исслед-

овано

штаммов

 

Resistance / резист-

тентность

(%)

 

Tested

starins / исслед-

овано

штаммов

 

Resistance / резист-

тентность

(%)

 

Tested

strains / исслед-

овано

штаммов

 

Resistance / резист-

тентность

(%)

 

Tested

strains / исслед-

овано

штаммов

 

Resistance / резист-

тентность

(%)

 

Ampicillin / ампициллин

1214

29.9

500

33.6

201

37.8

179

20.1

Oxacillin / оксациллин

1415

48.1

816

36.6

167

68.3

343

58.3

Ampicillin+sulbactam/  ампициллин+сульбактам

413

27.6

43

11.6

30

86.7

53

32.1

Аmoxicillin+clavulanate/

амоксициллин+клавуланат

256

31.3

NT/НТ*

NT/НТ

NT/НТ

NT/НТ

28

0

Imipenem / имипенем

890

6.6

450

4.2

180

3.3

118

5.1

Meropenem / меропенем

435

3.0

69

47.8

49

16.3

49

14.3

Cefazolin / цефазолин

876

16.2

434

11.5

91

38.5

307

34.5

Cephalothin / цефалотин

28

25.0

276

5.4

NT/НТ

NT/НТ

NT/НТ

NT/НТ

Cefamandole / цефамандол

59

32.2

NT/НТ

NT/НТ

NT/НТ

NT/НТ

NT/НТ

NT/НТ

Cefuroxime / цефуроксим

644

18.1

101

17.8

51

19.6

38

50.0

Cefoperazone / цефоперазон

437

29.1

411

12.2

76

18.4

77

80.5

Cefotaxime / цефотаксим

570

27.7

142

16.2

86

31.4

96

44.8

Ceftazidime / цефтазидим

392

27.6

52

38.5

54

87.0

67

71.6

Ceftibuten / цефтибутен

42

76.2

79

2.5

NT/НТ

NT/НТ

14

100.0

Ceftriaxone / цефтриаксон

1310

26.9

740

20.7

207

21.7

141

45.4

Cefepime / цефепим

125

43.2

99

34.3

52

94.2

50

96.0

Gentamicin / гентамицин

746

33.4

113

95.6

100

26.0

75

37.3

Amikacin / амикацин

429

18.9

70

30.0

46

32.6

268

10.1

Sisomicin / сизомицин

257

1.2

NT/НТ

NT/НТ

NT/НТ

NT/НТ

NT/НТ

NT/НТ

Erythromycin / эритромицин

664

23.2

162

1.2

100

22.0

73

17.8

Clarithromycin/ кларитромицин

59

40.7

11

63.6

15

60.0

16

87.5

Azithromycin / азитромицин

107

22.4

50

8.0

17

29.4

19

52.6

Lincomycin / линкомицин

377

7.2

186

7.5

46

4.3

104

16.3

Clindamycin / клиндамицин

430

25.1

40

45.0

50

14.0

19

52.6

Tetracycline / тетрациклин

375

17.3

30

13.3

34

23.5

47

10.6

Doxycycline / доксициклин

389

20.3

145

2.1

72

15.3

85

23.5

Vancomycin / ванкомицин

236

9.3

104

18.3

75

12.0

262

6.9

Teicoplanin / тейкопланин

38

58.0

26

57.7

16

83.3

12

100.0

Rifampicin / рифампицин

438

5.5

462

9.7

136

2.2

245

14.3

Ciprofloxacin / ципрофлоксацин

877

7.4

492

5.5

101

11.9

313

8.9

Ofloxacin / офлоксацин

383

7.8

39

20.5

37

13.5

251

12.7

Pefloxacin / пефлоксацин

42

38.1

10

40.0

NT/НТ

NT/НТ

18

50.0

Norfloxacin / норфлоксацин

109

6.4

10

0

14

0

21

0

Moxifloxacin / моксифлоксацин

21

19.0

13

38.5

12

0

12

50.0

Levofloxacin / левофлоксацин

290

14.8

66

28.8

23

26.1

32

18.7

Gatifloxacin / гатифлоксацин

150

0

23

8.7

14

0

19

5.3

Chloramphenicol / хлорамфеникол

85

52.9

12

50.0

16

33.3

18

100.0

Linezolid / линезолид

73

17.8

33

33.3

17

58.8

NT/НТ

NT/НТ

* NT – non-tested. The resistance rate over 50% is shown in bold type / НТ – не тестировали. Жирным шрифтом выделена устойчивость 50% и выше.

The investigations showed the maximum sensitivity of gram-positive CPMs to gatifloxacin (S. aureus 100%, S. epidermidis 91.3%, S. рyogenes 100%, E. faecalis 94.7%), meropenem (S. aureus 96.7%), vancomycin (E. faecalis 93.1%), imipenem (S. aureus 93.4%, S. epidermidis 95.8%, S. рyogenes 96.7%, E. faecalis 94.9%), sizomycin (S. aureus 98.8%), rifampicin (S. aureus 94.5%, S. epidermidis 90.3%, S. рyogenes 97.8%), norfloxacin (S. aureus 93.6%, S. epidermidis 100%, S. рyogenes 100%, E. faecalis 100%), amoxycillin/clavulanate (E. faecalis 100%), ciprofloxacin (S. aureus 92.6%, S. epidermidis 94.5%, S. рyogenes 88.1%, E. faecalis 91.1%), and lincomycin (S. aureus 92.8%, S. epidermidis 92.5%, S. рyogenes 95.7%, E. faecalis 83.7%).

Staphylococci had the highest resistance rate to gentamycin (S. epidermidis 95.6%) and ceftibuten (S. aureus 76.2%). MRSA and MRSE  (methicillin/oxacillin-resistant staphylococci) comprised 48.1% and 36,6% respectively, while VRSA and VRSE (vancomycin-resistant staphylococci) comprised 9.3% and 18.3% respectively. The S. рyogenes strains were the most resistant to cefepime (94.2%), ceftazidime (87%), ampicillin/sulbactam (86.7%) and teicoplanin (83,3%).

It is widely known that enterococci are by nature resistant to cephalosporins and can also acquire resistance to almost any class of antibiotics including penicillins, aminoglycosides, and glycopeptides. We focused on E. faecalis, the resistance of which to ceftibuten, chloramphenicol, moxifloxacin, and teicoplanin was 100% and to cefepime and clarithromycin 96% and 87.5%, respectively. The proportion of vancomycin-resistant enterococci (VRE) was 6.9%.

Table 3. Resistance to Antimicrobial Medicines of the Most Common Gram-Negative Agents Having Caused SSIs in Hospitals of Kiev in 2008 (n =1203)

 

 

Antimicrobial medicines / антимикробные

препараты

 

           Microorganisms /микроорганизмы

E.coli

Enterobacter spp.

P.aeroginosa

A.baumanni

Tested

strains / исследо

вано

штам

мов

 

Resistan

ce / устойчи

вость

(%)

 

Tested

strains / исследо

вано

штам

мов

 

Resistan

ce / устойчи

вость

(%)

 

Tested

straines / исследо

вано

штам

мов

 

Resistan

ce / устойчи

вость

(%)

 

Tested

strains / исследо

вано

штам

мов

 

Resistan

ce / устойчи

вость

(%)

 

Ampicillin / ампициллин

362

54.1

272

51.8

241

29.9

135

58.5

Oxacillin / оксациллин

34

85.3

36

97.2

52

100.0

47

100.0

Ampicillin+sulbactam / ампициллин+сульбактам

51

23.5

26

7.7

60

10.0

NT/НТ*

NT/НТ

Piperacilin+tazobactam / пиперацилин+тазобактам

25

12.0

10

100.0

15

13.3

80

20.0

Imipenem / имипенем

217

3.2

266

4.1

278

14.0

139

5.7

Meropenem / меропенем

108

9.3

25

12.0

175

11.4

22

0

Cefazolin /цефазолин

315

18.1

284

61.3

143

46.9

35

65.7

Cefuroxime / цефуроксим

82

39.0

85

47.1

137

41.6

22

90.9

Cefoperazone / цефоперазон

348

13.8

353

15.9

292

27.4

122

35.2

Cefotaxime /цефотаксим

390

13.9

167

25.7

86

93.0

46

87.0

Ceftriaxone / цефтриаксон

266

34.6

284

30.6

275

32.7

144

47.2

Ceftazidime / цефтазидим

172

38.4

270

22.2

246

42.7

113

29.2

Ceftibuten / цефтибутен

15

53.3

20

60.0

18

100.0

25

100.0

Cefepime / цефепим

57

57.9

46

69.6

172

33.7

14

92.9

Kanamycin / канамицин

81

11.1

NT/НТ

NT/НТ

67

3.0

31

100.0

Gentamicin /гентамицин

355

16.3

264

66.3

113

34.5

48

100.0

Tobramycin / тобрамицин

15

93.3

20

0

22

59.1

NT/НТ

NT/НТ

Netilmicin /нетилмицин

29

3.4

26

15.4

72

47.2

14

25.0

Amikacin / амикацин

172

15.7

99

57.6

213

46.0

42

78.6

Erythromycin/эритромицин

21

95.2

NT/НТ

NT/НТ

NT/НТ

NT/НТ

NT/НТ

NT/НТ

Clarithromycin/кларитромицин

27

66.7

29

6.9

292

27.4

NT/НТ

NT/НТ

Azithromycin/ азитромицин

44

40.9

15

60.0

22

18.2

15

80.0

Lincomycin/ линкомицин

24

75.0

14

75.0

NT/НТ

NT/НТ

NT/НТ

NT/НТ

Tetracycline/ тетрациклин

30

50.0

57

33.3

17

100.0

11

0

Doxycycline / доксициклин

69

34.8

27

29.6

63

81.0

22

95.5

Vancomycin / ванкомицин

25

8.0

26

11.5

60

86.7

NT/НТ

NT/НТ

Teicoplanin /тейкопланин

11

100.0

14

75.0

NT/НТ

NT/НТ

NT/НТ

NT/НТ

Rifampicin / рифампицин

21

80.9

37

21.6

69

31.9

NT/НТ

NT/НТ

Ciprofloxacin / ципрофлоксацин

175

42.9

74

85.1

127

76.4

40

95.0

Ofloxacin / офлоксацин

100

38.0

153

43.1

123

57.7

73

49.3

Norfloxacin / норфлоксацин

22

63.6

28

39.3

24

33.3

12

66.7

Moxifloxacin / моксифлоксацин

27

66.7

14

75.0

NT/НТ

NT/НТ

NT/НТ

NT/НТ

Levofloxacin / левофлоксацин

57

33.3

62

40.3

125

56.0

11

90.9

Gatifloxacin / гатифлоксацин

35

31.4

28

11.1

54

35.2

NT/НТ

NT/НТ

Chloramphenicol / хлорамфеникол

33

90.9

18

33.3

17

41.2

14

85.7

Laevomycetin / левомицетин

218

5.5

NT/НТ

NT/НТ

12

100.0

NT/НТ

NT/НТ

Linezolide /линезолид

14

50.0

10

40.0

NT/НТ

NT/НТ

NT/НТ

NT/НТ

*NT – non-tested. The resistance rate over 50% is shown in bold type / НТ – не тестировали. Жирным шрифтом выделена устойчивость 50% и выше.

Data analysis of gram-negative CPMs causing SSIs showed their wide spread antimicrobial resistance in the surgery hospitals in Kiev. Resistance rates of gram-negative microorganisms found in patients’ samples vary. E. coli had the maximum resistance to teicoplanin (100%), erythromycin (95.2%), tobramycin (93.3%), and chloramphenicol (90.9%). Enterobacter spp. strains were resistant to piperacillin/tazobactam (100%), oxacillin (97.2%) and ciprofloxacin (85.1%). P. aeroginosa strains were 100% resistant to oxacillin, ceftibuten, tetracycline, erythromycin, and laevomycetin. These strains also had a high resistance to cefotaxime (93%), vancomycin (86.7%), and doxycycline (81%). Among the most common agents causing SSIs, the highest resistance was among  A.baumanni strains; 100% to oxacillin, ceftibuten, kanamycin, and gentamycin. Theses strains were also highly resistant to doxycycline (95.5%), ciprofloxacin (95%), cefepime (92.9%), cefuroxime (90.9%), levofloxacin (90.9%), cefotaxime (87%), chloramphenicol (85.7%), azithromycin (80%), and amikacin (78.6%).

The gram-negative CPMs were reported to have the maximum sensitivity to imipinem (E. coli 96.8%, Enterobacter spp. 95.9%, P. aeroginosa 86%, A. baumanni 94.2%), meropenem (E. coli 90.7%, Enterobacter spp. 88%, P. aeroginosa 88.6%, A. baumanni 100%), ampicillin/sulbactam (Enterobacter spp. 92.3%, P. aeroginosa 90%), kanamycin (E. coli 88.9%, P. aeroginosa 97%), lomefloxacin (E. coli 100%), netilmicin (E. coli 96.6%, Enterobacter spp. 84.6%), clarithromycin (Enterobacter spp. 93.1%), vancomycin (E.coli 92%, Enterobacter spp. 88.5%), laevomycetin (E. coli 94.5%), and gatifloxacin (Enterobacter spp. 89%).

Discussion
The results of this investigation indicate that the official statistical data fail to report the actual scale of nosocomial infection transmission in Kiev’s surgery hospitals due to the lack of reliable SSI registration. To estimate the epidemiological situation correctly, it is necessary to assess SSI incidence rates based on diagnostic information determined by medical officers (passive method) and epidemiological data (active method) using commonly applied standard criteria of case definition.

Thus, the investigation demonstrated that in the surgery hospitals in Kiev the incidence rate of SSI causal agents resistant to antimicrobial medicines is quite high. This poses a serious problem for curing patients from nosocomial infections. Hospital strains resistant to antimicrobial medicines were found both among gram-positive and gram-negative bacteria. This documents the need for systematic microbiological monitoring of the main causal agents of nosocomial infections in every surgery hospital as a basic measure of epidemiological control over antimicrobial resistance. Antibiotics should be prescribed in accordance to available data on SSI resistance. Microbiological monitoring will enable to follow the recommendations for rational antibacterial therapy of patients.

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