572825
research-article2015
IJLXXX10.1177/1534734615572825The International Journal of Lower Extremity WoundsWu et al
Case Series and Case Reports
Bacteriological Investigation of Chronic Wounds in a Specialized Wound Healing Department: A Retrospective Analysis of 107 Cases
The International Journal of Lower Extremity Wounds 2015, Vol. 14(2) 178–182 © The Author(s) 2015 Reprints and permissions: sagepub.com/journalsPermissions.nav DOI: 10.1177/1534734615572825 ijl.sagepub.com
MinJie Wu, MMed1, Hong Ruan, BSc1, Yao Huang, MMed1, ChuanBo Liu, MMed2, PengWen Ni, MMed1, JunNa Ye, MMed2, ShuLiang Lu, PhD2, and Ting Xie, PhD1
Abstract To investigate the information of chronic wounds, especially in the aspect of microbiological profile and to explore the relationship between the wound culture result and chronic wounds infection, we retrospectively reviewed the medical records of 107 patients with chronic wounds from January 2011 to December 2013. The sociodemographic data, woundrelated information, therapeutic type, and wound infection status were extracted. Microbial specimens were obtained and processed using standard hospital procedure for wound culture. The predominant pathogen isolated was Staphylococcus aureus (n = 11, 26.2%), followed by Escherichia coli (n = 6, 14.3%), Enterobacter cloacae (n = 3, 7.1%), and Pseudomonas aeruginosa (n = 3, 7.1%). Sixty percent of the infectious chronic wounds had positive culture, and 96.2% of the noninfectious wounds had negative culture. In conclusion, the microbial characteristics were mostly in the site of lower extremity, gramnegative bacteria, and monopathogen, respectively. Furthermore, the relationship between the wound culture result and chronic wound infection was not exactly coincident. It may be useful for guiding the empiric therapy of chronic wounds. Keywords chronic wounds, microbiology, wound infection Wounds can be broadly classified as having either an acute or a chronic etiology.1 Multiple reasons can lead to the development of chronic wounds, such as impaired arterial supply, impaired venous drainage, and metabolic dysfunction. Wounds that have not shown a 20% to 40% reduction in area after 2 to 4 weeks of optimal treatment should be considered as chronic.2 As society ages and the lifestyle changes, chronic wounds gradually become a major challenge to medical professionals, and have an adverse impact on the life quality of patients with chronic wounds.3 Chronic wounds are contaminated or infected with a wide range of pathogens which might be involved in and contribute to the nonhealing of these wounds.4 Early recognition along with timely, appropriate and cost-effective intervention is very important to the wound management.5 However, there has been some debate on the literature regarding the microbiology features and spectrum of chronic wounds.6-9 Understanding the microbiological characteristics of different types of chronic wounds may be useful for guiding empiric therapy and managing the patients.5 In this study, our aims were (a) to investigate the information of chronic wounds, especially in the aspect of microbiological
profile and (b) to explore the relationship between the wound culture result and chronic wounds infection in a specialized wound healing department in China.
Patients and Methods We reviewed the medical records of patients with chronic wounds from January 2011 to December 2013. For the different definition on chronic wounds, any wounds with duration before admission at least 2 weeks were included irrespective of the etiology in a specialized wound healing department in Shanghai, China. Finally a total of 107 patients with chronic wounds were screened. 1
Ninth People’s Hospital Affiliated to Shanghai Jiao Tong University School of Medicine, Shanghai, China 2 Ruijin Hospital Affiliated to Shanghai Jiao Tong University School of Medicine, Shanghai, China Corresponding Author: Ting Xie, Wound Healing Department, Ninth People’s Hospital Affiliated to Shanghai Jiao Tong University School of Medicine, No. 639, Zhi Zao Ju Road, Shanghai, China. Email: [email protected]
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Wu et al The sociodemographic data, wound-related information, therapeutic type, and wound infection status were analyzed. The sociodemographic data included age, sex, medical expense, and hospitalization days; the wound-related information included wound duration before admission, dimension, site, etiology, morphology, and wound culture. According to an international consensus, wound localized infection was often characterized by signs and symptoms of inflammation.5 The chronic wound would be considered as localized infection if there were purulent secretions or two or more signs of inflammation, including erythema, warmth, tenderness, heat, and induration were presented.10 Osteomyelitis was diagnosed mainly by a positive bone-to-probe test or by X-ray test.11 Systemic inflammatory response was also recorded if existed.12 Microbial culture was obtained at the time of the first presentation. After debridement of the wound and thorough cleaning with sterile normal saline, the wound swab specimens were collected and transferred to microbiological lab immediately according to the standard hospital procedure, and identified by VITEK2 Compact automatic microbial analysis system. Data were analyzed by SPSS 17.0 software packet. Measurement data were presented as means ± standard deviations; enumeration data were presented as percentage.
Results The records of a total of 107 participants (70 men and 37 women) were studied, the mean age was 53.47 ± 18.68 years and age ranged from 6 to 92 years; the mean hospitalization days was 19.39 ± 12.17 days and ranged from 3 to 65 days; and the mean medical expense was 12 300 ± 10 641 RMB ranging from 1179 to 63 626. The most used therapeutic type was negative pressure wound therapy (79.4%). In terms of wound-related information, the mean wound duration before admission was 21.53 ± 65.64 months ranging from 0.5 to 600 months; the mean wound dimension was 21.72 ± 47.39 cm2 with a range of 0.25 to 400 cm2. The result of wound etiology was as follows: surgical wound (42.1%), pressure ulcer (28%), burn (5.6%), venous leg ulcer (3.7%), radiation ulcer (3.7%), diabetic foot ulcer (2.8%), and others (14%). In the investigation into the site of chronic wounds, lower extremity accounted for the maximum (41.1%) number of wounds, as shown in Figure 1. With regard the morphology of the chronic wounds, simple ulcers (43%) were the maximum, followed by sinus (40.2%), undermined wound (10.3%), compound wound (4.7%), and necrosis (1.9%). Of all the 107 patients, 86 (80.4%) patients were accepted wound microbial culture at the first presentation, of which 49 (45.8%) samples had negative culture and 37 (34.6%) samples had positive culture. Among the positive culture, a total of 42 pathogens were isolated, where gram-negative
Figure 1. The distribution sites of the chronic wounds (n = 107).
bacteria (n = 23, 54.8%) outnumbered gram-positive (n = 18, 42.9%), and the other was fungi (n = 1, 2.4%). Meanwhile, monomicrobial specimens (n = 32, 86.5%) significantly outnumbered polymicrobial specimens (n = 5, 13.5%). A total of 22 species of pathogens were identified. The predominant pathogen isolated was Staphylococcus aureus (n = 11, 26.2%), Escherichia coli (n = 6, 14.3%), Enterobacter cloacae (n = 3, 7.1%), Pseudomonas aeruginosa (n = 3, 7.1%), methicillin-resistant Staphylococcus aureus (MRSA; n = 2, 4.8%), and other miscellaneous pathogens (n = 17, 40.5%). The relationship between the wound culture result and wound site, determined by means of further analysis, is shown in Table 1. The relationship between the wound culture result and wound etiology is shown in Table 2. The distribution of microbial profile on the different wound site is presented in Table 3 and the distribution of microbial profile on the main wound etiology is presented in Table 4. According to the clinical signs and symptoms of chronic wound inflammation, 63.6% (n = 68) of the patients had wound infection, and the other 36.4% (n = 39) of the patients were without infection. It was remarkable that the result of wound culture was not exactly consistent with the wound infection. Only 60.0% of the infectious chronic wounds had positive culture and 96.2% of the noninfectious wounds had negative culture. The total matching degree was 70.9% (Table 5).
Discussion The establishment of specialized, multidisciplinary wound healing clinics is getting more and more attention recently, especially in developing countries. This study was a comprehensive retrospective analysis of microbial profile and the infection condition as well as the relationship between them in patients with chronic wounds. The research data were collected in the first specialized wound healing department in Shanghai, China.
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Table 1. The Relationship Between Wound Culture Result and Wound Site. Wound Site
Maxillofacial Region
Culture Results
n
%
n
%
n
%
n
5 4 2 11
45.5 36.4 18.2 100
4 5 2 11
36.4 45.5 18.2 100
1 1 0 2
50.0 50.0 0.0 100
14 13 4 31
Negative Positive No culture Total
Thoracoabdominal Region
Lumbodorsal Region
Pelvis Region
Upper Extremity
Lower Extremity
%
n
%
n
%
45.2 41.9 12.9 100
6 1 1 8
75.0 12.5 12.5 100
19 13 12 44
43.2 29.5 27.3 100
Table 2. The Relationship Between Wound Culture Result and Wound Etiology. Wound Etiology
Pressure Ulcer
Culture Results
n
%
n
%
n
%
n
%
n
%
n
%
n
%
Negative Positive No culture Total
12 13 5 30
40.0 43.3 16.7 100
1 0 2 3
33.3 0.0 66.7 100
2 1 1 4
50.0 25.0 25.0 100
1 3 0 4
25.0 75.0 0.0 100
22 15 8 45
48.9 33.3 17.8 100
3 1 2 6
50.0 16.7 33.3 100
8 4 3 15
53.3 26.7 20.0 100
DFU
Radiation Ulcer
VLU
Surgical Wound
Burn
Others
Abbreviations: DFU, diabetic foot ulcer; VLU, venous leg ulcer.
Our research results showed that the most sites of chronic wounds detected in this study were lower extremity. It was unexpected that only 34.6% samples had positive culture. We did not do the anaerobic bacteria culture because of the difficulty and high cost in isolating such bacteria. In other literature,6,7,13-16 the prevalence of anaerobic bacteria culture in chronic wounds ranged from 4.5% to 39.1%, and most cultures were done with the samples from diabetic foot infection. The most frequently isolated pathogens were gram-negative bacteria, which were compatible with reports of such findings in previous articles.6,8,9,15,17-19 However, this is still a matter of debate. Dezfulian et al13 and Mendes et al7 pointed out that gram-positive bacteria were the ones most frequently isolated. The inconsistency of the scenarios may be explained by the various factors in these research studies, such as different population, wound etiology, and culture technique. But generally speaking, gram-negative bacteria outnumbered the gram-positive in chronic wounds. Thus, it is critical to use antibiotics that are more effective against gram-negative bacteria in contrast to gram-positive pathogens.20 Moreover, the prevalence of fungi was scanty in this study, which may be the reason that only 2.8% patients with diabetic foot ulcer were included. The most frequently isolated pathogens were S aureus, E coli, E cloacae, and P aeruginosa. In the aspect of multiple
resistant bacteria, the isolation rate of MRSA was very low (4.8%), which was in accordance with previous studies in other countries where the isolation rate was less than 10%.6,21,22 The high rate of MRSA in the patients with diabetic foot infection could not be neglected since it may lead to wound healing delay or deterioration.7,23 Through analysis of the relationship between the culture result and wound site, we found that the isolation rate in the upper extremity was low; at the same time, the surgical wound was also with low isolation rate. This may be because surgical wound is usually prophylactic treated with antibiotics before and after surgery according to the convention. It was a matter of concern that the multiple resistant bacteria (MRSA and baumanii) were all isolated in the site of maxillofacial region, which may be related to the anatomical approach to the oral cavity. As regards limitation of this research, we could not obtain the results of quantitative culture. In order to judge the condition of chronic infection as reasonably as possible, we adopted the clinical criteria from American Diabetes Association.10 From the actual clinical practice perspective, it was practical and convenient to evaluate the infection status of chronic wounds on the basis of the clinical signs and symptoms without any extra cost. The relationship between the wound culture result and chronic wound infection was not exactly coincident. On one hand, only 60.0% of the
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Wu et al Table 3. The Distribution of Microbial Profile on the Different Wound Sites.
Table 4. The Distribution of Microbial Profile on the Main Etiology.
Site Maxillofacial region
Thoracoabdominal region
Lumbodorsal region Pelvic region
Upper extremity Lower extremity
Microbial Isolated
n
Etiology
Methicillin-resistant Staphylococcus aureus baumanii Acinetobacter lwoffii Stenotrophomonas maltophilia Staphylococcus aureus Escherichia coli Streptococcus viridans Neisseria Bacillus mycoides Enterobacter aerogenes Staphylococcus aureus Escherichia coli Pseudomonas aeruginosa baumanii Enterococcus faecalis citrobacter-koseri Bacillus prodigiosus Staphylococcus epidermidis Staphylococcus aureus Enterobacter cloacae Escherichia coli Pseudomonas aeruginosa Staphylococcus warneri Streptococcus dysgalactiae equlsimilis Bacillus prodigiosus Bacillus proteus vulgaris Candida
2
Pressure ulcer
1 1 1 2 1 1 1 1 1 4 4 2 1 1 1 1 1 5 3 1 1 1 1 1 1 1
Surgical wound
n
Staphylococcus aureus Escherichia coli Pseudomonas aeruginosa baumanii citrobacter-koseri Streptococcus viridans Enterococcus faecalis Bacillus prodigiosus Neisseria Staphylococcus aureus Enterobacter cloacae Escherichia coli Pseudomonas aeruginosa Staphylococcus epidermidis Bacillus mycoides Staphylococcus warneri Bacillus proteus vulgaris Stenotrophomonas maltophilia Bacillus prodigiosus Candida
4 4 1 1 1 1 1 1 1 4 3 2 1 1 1 1 1 1 1 1
Table 5. The Relationship Between the Wound Culture Result and Wound Infection. Wound Infection Yes
No
infectious chronic wounds had positive culture; on the other hand, 96.2% of the noninfectious wounds had negative culture. It was revealed that clinicians could not start antibiotics treatment depending totally on the wound culture. It is very important to recognize the clinical signs and symptoms of wound infection and avoid the indiscriminate use of antibiotics.9 According to the reports of Schmidt et al,24 when comparing the bacterial population in different chronic wounds, only 22% of the venous leg ulcers with a positive culture developed a clinical infection in contrast to 70% of the arterial and diabetic ulcers. We did not perform an in-depth analysis to explore the relationship between the culture result and wound etiology because of a relatively small sample in each wound etiology. In conclusion, the microbial characteristics were observed mostly in the site of lower extremity, gram-negative bacteria, and monopathogen isolation. The isolation rate of S aureus was the highest. The relationship between the wound culture result and chronic wound infection was not exactly coincident. In the future, we intend to carry out
Microbial Isolated
Wound Culture
n
%
Negative Positive No culture Negative Positive No culture
24 36 8 25 1 13
35.3 52.9 11.8 64.1 2.6 33.3
transnational comparison research studies on the basis of the presentation and analysis of microbiology condition. Acknowledgments We would like to thank the whole staff of the Wound Healing Department for their assistance with the clinical data collection and the microbiological laboratory staff for their contribution to the microbial data collection.
Authors’ Note MinJie Wu, Hong Ruan, and Yao Huang contributed equally to the work.
Declaration of Conflicting Interests The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.
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Funding The author(s) disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: This study was supported by grants from the National Natural Science Foundation of China (81071568, 81272111), Translational Medical Research Institute Stem Cells and Regenerative Medicine Base in Shanghai Jiao Tong University School of Medicine (TS201109), the National Scientific & Technology Pillar Program (2012BAI11B04), and the Major State Basic Research Development Program of China (2012CB518100)
References 1. Bowler PG, Duerden BI, Armstrong DG. Wound microbiology and associated approaches to wound management. Clin Microbiol Rev. 2001;14:244-269. 2. Leaper DJ, Durani P. Topical antimicrobial therapy of chronic wounds healing by secondary intention using iodine products. Int Wound J. 2008;5:361-368. 3. Snyder RJ, Cardinal M, Dauphinee DM, Stavosky J. A posthoc analysis of reduction in diabetic foot ulcer size at 4 weeks as a predictor of healing by 12 weeks. Ostomy Wound Manage. 2010;56(3):44-50. 4. Kirketerp-Møller K, Jensen PØ, Fazli M, et al. Distribution, organization, and ecology of bacteria in chronic wounds. J Clin Microbiol. 2008;46:2717-2722. 5. Wound infection in clinical practice. An international consensus. Int Wound J. 2008;5(suppl 3):iii-11. 6. Al Benwan K, Al Mulla A, Rotimi VO. A study of the microbiology of diabetic foot infections in a teaching hospital in Kuwait. J Infect Public Health. 2012;5:1-8. 7. Mendes JJ, Marques-Costa A, Vilela C, et al. Clinical and bacteriological survey of diabetic foot infections in Lisbon. Diabetes Res Clin Pract. 2012;95:153-161. 8. Tiwari S, Pratyush DD, Dwivedi A, Gupta SK, Rai M, Singh SK. Microbiological and clinical characteristics of diabetic foot infections in northern India. J Infect Dev Ctries. 2012;6:329-332. 9. de Souza JM, Vieira ÉC, Cortez TM, Mondelli AL, Miot HA, Abbade LP. Clinical and microbiologic evaluation of chronic leg ulcers: a cross-sectional study. Adv Skin Wound Care. 2014;27:222-227. 10. Consensus Development Conference on Diabetic Foot Wound Care: 7-8 April 1999, Boston, Massachusetts. American Diabetes Association. Diabetes Care. 1999;22:1354-1360. 11. Shone A, Burnside J, Chipchase S, Game F, Jeffcoate W. Probing the validity of the probe-to-bone test in the
diagnosis of osteomyelitis of the foot in diabetes. Diabetes Care. 2006;29:945. 12. Schaper NC. Diabetic foot ulcer classification system for research purposes: a progress report on criteria for including patients in research studies. Diabetes Metab Res Rev. 2004;20(suppl 1):S90-S95. 13. Dezfulian A, Salehian MT, Amini V, et al. Bacteriological study of diabetic foot infections in an Iranian hospital. Iran Red Crescent Med J. 2011;13:590-591. 14. Abdulrazak A, Bitar ZI, Al-Shamali AA, Mobasher LA. Bacteriological study of diabetic foot infections. J Diabetes Complications. 2005;19:138-141. 15. Parvez N, Dutta P, Ray P, et al. Microbial profile and utility of soft tissue, pus, and bone cultures in diagnosing diabetic foot infections. Diabetes Technol Ther. 2012;14:669-674. 16. Gjødsbøl K, Christensen JJ, Karlsmark T, Jørgensen B, Klein BM, Krogfelt KA. Multiple bacterial species reside in chronic wounds: a longitudinal study. Int Wound J. 2006;3:225-231. 17. Turhan V, Mutluoglu M, Acar A, et al. Increasing incidence of Gram-negative organisms in bacterial agents isolated from diabetic foot ulcers. J Infect Dev Ctries. 2013;7:707-712. 18. Bayram Y, Parlak M, Aypak C, Bayram I. Three-year review of bacteriological profile and antibiogram of burn wound isolates in Van, Turkey. Int J Med Sci. 2013;10:19-23. 19. Moremi N, Mushi MF, Fidelis M, Chalya P, Mirambo M, Mshana SE. Predominance of multi-resistant gramnegative bacteria colonizing chronic lower limb ulcers (CLLUs) at Bugando Medical Center. BMC Res Notes. 2014;7:211. 20. Hefni AA-H, Ibrahim A-MR, Attia KM, et al. Bacteriological study of diabetic foot infection in Egypt. J Arab Soc Med Res. 2013;8:26-32. 21. Raja NS. Microbiology of diabetic foot infections in a teaching hospital in Malaysia: a retrospective study of 194 cases. J Microbiol Immunol Infect. 2007;40:39-44. 22. Jockenhöfer F, Gollnick H, Herberger K, et al. Bacteriological pathogen spectrum of chronic leg ulcers: results of a multicenter trial in dermatologic wound care centers differentiated by regions. J Dtsch Dermatol Ges. 2013;11:1057-1063. 23. Zubair M, Malik A, Ahmad J. Clinico-microbiological study and antimicrobial drug resistance profile of diabetic foot infections in north India. Foot (Edinb). 2011;21:6-14. 24. Schmidt K, Debus ES, St Jessberger, Ziegler U, Thiede A. Bacterial population of chronic crural ulcers: is there a difference between the diabetic, the venous, and the arterial ulcer? Vasa. 2000;29:62-70.
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research-article2015
IJLXXX10.1177/1534734615572825The International Journal of Lower Extremity WoundsWu et al
Case Series and Case Reports
Bacteriological Investigation of Chronic Wounds in a Specialized Wound Healing Department: A Retrospective Analysis of 107 Cases
The International Journal of Lower Extremity Wounds 2015, Vol. 14(2) 178–182 © The Author(s) 2015 Reprints and permissions: sagepub.com/journalsPermissions.nav DOI: 10.1177/1534734615572825 ijl.sagepub.com
MinJie Wu, MMed1, Hong Ruan, BSc1, Yao Huang, MMed1, ChuanBo Liu, MMed2, PengWen Ni, MMed1, JunNa Ye, MMed2, ShuLiang Lu, PhD2, and Ting Xie, PhD1
Abstract To investigate the information of chronic wounds, especially in the aspect of microbiological profile and to explore the relationship between the wound culture result and chronic wounds infection, we retrospectively reviewed the medical records of 107 patients with chronic wounds from January 2011 to December 2013. The sociodemographic data, woundrelated information, therapeutic type, and wound infection status were extracted. Microbial specimens were obtained and processed using standard hospital procedure for wound culture. The predominant pathogen isolated was Staphylococcus aureus (n = 11, 26.2%), followed by Escherichia coli (n = 6, 14.3%), Enterobacter cloacae (n = 3, 7.1%), and Pseudomonas aeruginosa (n = 3, 7.1%). Sixty percent of the infectious chronic wounds had positive culture, and 96.2% of the noninfectious wounds had negative culture. In conclusion, the microbial characteristics were mostly in the site of lower extremity, gramnegative bacteria, and monopathogen, respectively. Furthermore, the relationship between the wound culture result and chronic wound infection was not exactly coincident. It may be useful for guiding the empiric therapy of chronic wounds. Keywords chronic wounds, microbiology, wound infection Wounds can be broadly classified as having either an acute or a chronic etiology.1 Multiple reasons can lead to the development of chronic wounds, such as impaired arterial supply, impaired venous drainage, and metabolic dysfunction. Wounds that have not shown a 20% to 40% reduction in area after 2 to 4 weeks of optimal treatment should be considered as chronic.2 As society ages and the lifestyle changes, chronic wounds gradually become a major challenge to medical professionals, and have an adverse impact on the life quality of patients with chronic wounds.3 Chronic wounds are contaminated or infected with a wide range of pathogens which might be involved in and contribute to the nonhealing of these wounds.4 Early recognition along with timely, appropriate and cost-effective intervention is very important to the wound management.5 However, there has been some debate on the literature regarding the microbiology features and spectrum of chronic wounds.6-9 Understanding the microbiological characteristics of different types of chronic wounds may be useful for guiding empiric therapy and managing the patients.5 In this study, our aims were (a) to investigate the information of chronic wounds, especially in the aspect of microbiological
profile and (b) to explore the relationship between the wound culture result and chronic wounds infection in a specialized wound healing department in China.
Patients and Methods We reviewed the medical records of patients with chronic wounds from January 2011 to December 2013. For the different definition on chronic wounds, any wounds with duration before admission at least 2 weeks were included irrespective of the etiology in a specialized wound healing department in Shanghai, China. Finally a total of 107 patients with chronic wounds were screened. 1
Ninth People’s Hospital Affiliated to Shanghai Jiao Tong University School of Medicine, Shanghai, China 2 Ruijin Hospital Affiliated to Shanghai Jiao Tong University School of Medicine, Shanghai, China Corresponding Author: Ting Xie, Wound Healing Department, Ninth People’s Hospital Affiliated to Shanghai Jiao Tong University School of Medicine, No. 639, Zhi Zao Ju Road, Shanghai, China. Email: [email protected]
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179
Wu et al The sociodemographic data, wound-related information, therapeutic type, and wound infection status were analyzed. The sociodemographic data included age, sex, medical expense, and hospitalization days; the wound-related information included wound duration before admission, dimension, site, etiology, morphology, and wound culture. According to an international consensus, wound localized infection was often characterized by signs and symptoms of inflammation.5 The chronic wound would be considered as localized infection if there were purulent secretions or two or more signs of inflammation, including erythema, warmth, tenderness, heat, and induration were presented.10 Osteomyelitis was diagnosed mainly by a positive bone-to-probe test or by X-ray test.11 Systemic inflammatory response was also recorded if existed.12 Microbial culture was obtained at the time of the first presentation. After debridement of the wound and thorough cleaning with sterile normal saline, the wound swab specimens were collected and transferred to microbiological lab immediately according to the standard hospital procedure, and identified by VITEK2 Compact automatic microbial analysis system. Data were analyzed by SPSS 17.0 software packet. Measurement data were presented as means ± standard deviations; enumeration data were presented as percentage.
Results The records of a total of 107 participants (70 men and 37 women) were studied, the mean age was 53.47 ± 18.68 years and age ranged from 6 to 92 years; the mean hospitalization days was 19.39 ± 12.17 days and ranged from 3 to 65 days; and the mean medical expense was 12 300 ± 10 641 RMB ranging from 1179 to 63 626. The most used therapeutic type was negative pressure wound therapy (79.4%). In terms of wound-related information, the mean wound duration before admission was 21.53 ± 65.64 months ranging from 0.5 to 600 months; the mean wound dimension was 21.72 ± 47.39 cm2 with a range of 0.25 to 400 cm2. The result of wound etiology was as follows: surgical wound (42.1%), pressure ulcer (28%), burn (5.6%), venous leg ulcer (3.7%), radiation ulcer (3.7%), diabetic foot ulcer (2.8%), and others (14%). In the investigation into the site of chronic wounds, lower extremity accounted for the maximum (41.1%) number of wounds, as shown in Figure 1. With regard the morphology of the chronic wounds, simple ulcers (43%) were the maximum, followed by sinus (40.2%), undermined wound (10.3%), compound wound (4.7%), and necrosis (1.9%). Of all the 107 patients, 86 (80.4%) patients were accepted wound microbial culture at the first presentation, of which 49 (45.8%) samples had negative culture and 37 (34.6%) samples had positive culture. Among the positive culture, a total of 42 pathogens were isolated, where gram-negative
Figure 1. The distribution sites of the chronic wounds (n = 107).
bacteria (n = 23, 54.8%) outnumbered gram-positive (n = 18, 42.9%), and the other was fungi (n = 1, 2.4%). Meanwhile, monomicrobial specimens (n = 32, 86.5%) significantly outnumbered polymicrobial specimens (n = 5, 13.5%). A total of 22 species of pathogens were identified. The predominant pathogen isolated was Staphylococcus aureus (n = 11, 26.2%), Escherichia coli (n = 6, 14.3%), Enterobacter cloacae (n = 3, 7.1%), Pseudomonas aeruginosa (n = 3, 7.1%), methicillin-resistant Staphylococcus aureus (MRSA; n = 2, 4.8%), and other miscellaneous pathogens (n = 17, 40.5%). The relationship between the wound culture result and wound site, determined by means of further analysis, is shown in Table 1. The relationship between the wound culture result and wound etiology is shown in Table 2. The distribution of microbial profile on the different wound site is presented in Table 3 and the distribution of microbial profile on the main wound etiology is presented in Table 4. According to the clinical signs and symptoms of chronic wound inflammation, 63.6% (n = 68) of the patients had wound infection, and the other 36.4% (n = 39) of the patients were without infection. It was remarkable that the result of wound culture was not exactly consistent with the wound infection. Only 60.0% of the infectious chronic wounds had positive culture and 96.2% of the noninfectious wounds had negative culture. The total matching degree was 70.9% (Table 5).
Discussion The establishment of specialized, multidisciplinary wound healing clinics is getting more and more attention recently, especially in developing countries. This study was a comprehensive retrospective analysis of microbial profile and the infection condition as well as the relationship between them in patients with chronic wounds. The research data were collected in the first specialized wound healing department in Shanghai, China.
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Table 1. The Relationship Between Wound Culture Result and Wound Site. Wound Site
Maxillofacial Region
Culture Results
n
%
n
%
n
%
n
5 4 2 11
45.5 36.4 18.2 100
4 5 2 11
36.4 45.5 18.2 100
1 1 0 2
50.0 50.0 0.0 100
14 13 4 31
Negative Positive No culture Total
Thoracoabdominal Region
Lumbodorsal Region
Pelvis Region
Upper Extremity
Lower Extremity
%
n
%
n
%
45.2 41.9 12.9 100
6 1 1 8
75.0 12.5 12.5 100
19 13 12 44
43.2 29.5 27.3 100
Table 2. The Relationship Between Wound Culture Result and Wound Etiology. Wound Etiology
Pressure Ulcer
Culture Results
n
%
n
%
n
%
n
%
n
%
n
%
n
%
Negative Positive No culture Total
12 13 5 30
40.0 43.3 16.7 100
1 0 2 3
33.3 0.0 66.7 100
2 1 1 4
50.0 25.0 25.0 100
1 3 0 4
25.0 75.0 0.0 100
22 15 8 45
48.9 33.3 17.8 100
3 1 2 6
50.0 16.7 33.3 100
8 4 3 15
53.3 26.7 20.0 100
DFU
Radiation Ulcer
VLU
Surgical Wound
Burn
Others
Abbreviations: DFU, diabetic foot ulcer; VLU, venous leg ulcer.
Our research results showed that the most sites of chronic wounds detected in this study were lower extremity. It was unexpected that only 34.6% samples had positive culture. We did not do the anaerobic bacteria culture because of the difficulty and high cost in isolating such bacteria. In other literature,6,7,13-16 the prevalence of anaerobic bacteria culture in chronic wounds ranged from 4.5% to 39.1%, and most cultures were done with the samples from diabetic foot infection. The most frequently isolated pathogens were gram-negative bacteria, which were compatible with reports of such findings in previous articles.6,8,9,15,17-19 However, this is still a matter of debate. Dezfulian et al13 and Mendes et al7 pointed out that gram-positive bacteria were the ones most frequently isolated. The inconsistency of the scenarios may be explained by the various factors in these research studies, such as different population, wound etiology, and culture technique. But generally speaking, gram-negative bacteria outnumbered the gram-positive in chronic wounds. Thus, it is critical to use antibiotics that are more effective against gram-negative bacteria in contrast to gram-positive pathogens.20 Moreover, the prevalence of fungi was scanty in this study, which may be the reason that only 2.8% patients with diabetic foot ulcer were included. The most frequently isolated pathogens were S aureus, E coli, E cloacae, and P aeruginosa. In the aspect of multiple
resistant bacteria, the isolation rate of MRSA was very low (4.8%), which was in accordance with previous studies in other countries where the isolation rate was less than 10%.6,21,22 The high rate of MRSA in the patients with diabetic foot infection could not be neglected since it may lead to wound healing delay or deterioration.7,23 Through analysis of the relationship between the culture result and wound site, we found that the isolation rate in the upper extremity was low; at the same time, the surgical wound was also with low isolation rate. This may be because surgical wound is usually prophylactic treated with antibiotics before and after surgery according to the convention. It was a matter of concern that the multiple resistant bacteria (MRSA and baumanii) were all isolated in the site of maxillofacial region, which may be related to the anatomical approach to the oral cavity. As regards limitation of this research, we could not obtain the results of quantitative culture. In order to judge the condition of chronic infection as reasonably as possible, we adopted the clinical criteria from American Diabetes Association.10 From the actual clinical practice perspective, it was practical and convenient to evaluate the infection status of chronic wounds on the basis of the clinical signs and symptoms without any extra cost. The relationship between the wound culture result and chronic wound infection was not exactly coincident. On one hand, only 60.0% of the
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Wu et al Table 3. The Distribution of Microbial Profile on the Different Wound Sites.
Table 4. The Distribution of Microbial Profile on the Main Etiology.
Site Maxillofacial region
Thoracoabdominal region
Lumbodorsal region Pelvic region
Upper extremity Lower extremity
Microbial Isolated
n
Etiology
Methicillin-resistant Staphylococcus aureus baumanii Acinetobacter lwoffii Stenotrophomonas maltophilia Staphylococcus aureus Escherichia coli Streptococcus viridans Neisseria Bacillus mycoides Enterobacter aerogenes Staphylococcus aureus Escherichia coli Pseudomonas aeruginosa baumanii Enterococcus faecalis citrobacter-koseri Bacillus prodigiosus Staphylococcus epidermidis Staphylococcus aureus Enterobacter cloacae Escherichia coli Pseudomonas aeruginosa Staphylococcus warneri Streptococcus dysgalactiae equlsimilis Bacillus prodigiosus Bacillus proteus vulgaris Candida
2
Pressure ulcer
1 1 1 2 1 1 1 1 1 4 4 2 1 1 1 1 1 5 3 1 1 1 1 1 1 1
Surgical wound
n
Staphylococcus aureus Escherichia coli Pseudomonas aeruginosa baumanii citrobacter-koseri Streptococcus viridans Enterococcus faecalis Bacillus prodigiosus Neisseria Staphylococcus aureus Enterobacter cloacae Escherichia coli Pseudomonas aeruginosa Staphylococcus epidermidis Bacillus mycoides Staphylococcus warneri Bacillus proteus vulgaris Stenotrophomonas maltophilia Bacillus prodigiosus Candida
4 4 1 1 1 1 1 1 1 4 3 2 1 1 1 1 1 1 1 1
Table 5. The Relationship Between the Wound Culture Result and Wound Infection. Wound Infection Yes
No
infectious chronic wounds had positive culture; on the other hand, 96.2% of the noninfectious wounds had negative culture. It was revealed that clinicians could not start antibiotics treatment depending totally on the wound culture. It is very important to recognize the clinical signs and symptoms of wound infection and avoid the indiscriminate use of antibiotics.9 According to the reports of Schmidt et al,24 when comparing the bacterial population in different chronic wounds, only 22% of the venous leg ulcers with a positive culture developed a clinical infection in contrast to 70% of the arterial and diabetic ulcers. We did not perform an in-depth analysis to explore the relationship between the culture result and wound etiology because of a relatively small sample in each wound etiology. In conclusion, the microbial characteristics were observed mostly in the site of lower extremity, gram-negative bacteria, and monopathogen isolation. The isolation rate of S aureus was the highest. The relationship between the wound culture result and chronic wound infection was not exactly coincident. In the future, we intend to carry out
Microbial Isolated
Wound Culture
n
%
Negative Positive No culture Negative Positive No culture
24 36 8 25 1 13
35.3 52.9 11.8 64.1 2.6 33.3
transnational comparison research studies on the basis of the presentation and analysis of microbiology condition. Acknowledgments We would like to thank the whole staff of the Wound Healing Department for their assistance with the clinical data collection and the microbiological laboratory staff for their contribution to the microbial data collection.
Authors’ Note MinJie Wu, Hong Ruan, and Yao Huang contributed equally to the work.
Declaration of Conflicting Interests The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.
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The International Journal of Lower Extremity Wounds 14(2)
Funding The author(s) disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: This study was supported by grants from the National Natural Science Foundation of China (81071568, 81272111), Translational Medical Research Institute Stem Cells and Regenerative Medicine Base in Shanghai Jiao Tong University School of Medicine (TS201109), the National Scientific & Technology Pillar Program (2012BAI11B04), and the Major State Basic Research Development Program of China (2012CB518100)
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