ORIGINAL ARTICLE |
https://doi.org/10.5005/njem-11015-0006
|
Analysis of Blood Cultures of Patients Presenting to the Emergency Department in a Tertiary Healthcare Hospital in Mumbai
1,2Department of Emergency Medicine, Fortis Hospital Mulund, Mumbai, India
Corresponding Author: Deepak Kishor Sharma, Department of Emergency Medicine, Fortis Hospital Mulund, Mumbai, India, Phone: +91 8779299053, e-mail: dr.sharma3539@gmail.com
How to cite this article: Sharma DK, Gore SB. Analysis of Blood Cultures of Patients Presenting to the Emergency Department in a Tertiary Healthcare Hospital in Mumbai. Natl J Emerg Med 2023;1(1):12–17.
Source of support: Nil
Conflict of interest: Dr Sandeep B Gore is associated as the editorial board member of this journal and this manuscript was subjected to this journal’s standard review procedures, with this peer review handled independently of this editorial board member and her research group.
Received on: 27 March 2023; Accepted on: 15 May 2023; Published on: 14 August 2023
ABSTRACT
Aim and objectives: Analysis of blood cultures taken from patients attending emergency departments is an important exercise in determining the common pathogens prevalent in the region. The distribution of these infective pathogens keeps changing over time, and the rise in antimicrobial-resistant pathogens makes it difficult to routinely conduct effective empirical broad-spectrum antimicrobial therapy. This study aimed to analyse the results of blood cultures obtained from patients presenting to the Emergency Department of a Tertiary Healthcare Hospital in Mumbai and provide updated and detailed information on the distribution of causative pathogens in adult sepsis and study their antibiotic-susceptibility pattern.
Materials and methods: A hospital-based prospective cross-sectional study of 121 positive blood culture reports was conducted at the Department of Emergency Medicine, Fortis Hospital Mulund, Mumbai, which included all adult (age > 18 yrs) suspected sepsis patients arriving to the Emergency Department whose blood cultures were sent from the Emergency Department from January 2021 to December 2021.
Results: The study showed that mean age of the study cases was 59.3 years with 59.5% cases that belonged to the elderly age group with a male predominance (56.2% males–43.8% females). Overall, Gram-negative isolates were seen in 95% cases, while Gram-positive isolates were seen in only 1.7% cases. The most common organism isolated from cases with sepsis was Escherichia coli (45.5%) followed by Klebsiella (13.2%), Salmonella (10.7%), Stenotrophomonas (7.4%) and Pseudomonas (5%). Among Gram-positive organisms, Staphylococcus aureus was the most common organism isolated (1.7%). Escherichia coli isolates showed poor sensitivity towards fluoroquinolones and cephalosporins while good sensitivity towards aminoglycosides, carbapenems and combination drugs like Cefoperazone and Sulbactam and Piperacillin and Tazobactam. These findings suggest that Gram-negative organisms are the most common isolates observed in this study, with E. coli being the predominant pathogen followed by Klebsiella. High-level antimicrobial resistance was observed in sepsis cases for commonly used antimicrobials like fluoroquinolones and cephalosporins.
Keywords: Antibiotic stewardship, Blood culture, Emergency Department, Sepsis.
INTRODUCTION
Sepsis is the combination of a known or suspected infection and an accompanying systemic inflammatory response. Sepsis, severe sepsis and septic shock are terms used to describe the body’s systemic responses to infection. Severe sepsis is sepsis with acute dysfunction of one or more organ systems, and septic shock is a subset of severe sepsis. It is common and frequently fatal. Underlying illness, increased age and multisystem organ failure are major risk factors for mortality from sepsis.1,2
The prognosis of the patient with severe sepsis is related to the number of dysfunctional organs. Progression from signs of the inflammatory response to sepsis/severe sepsis and septic shock is associated with incrementally higher mortality risk. The transition to serious illness may occur during the critical ‘golden hours’ when definitive recognition and treatment provide maximal benefit in terms of outcome. Therefore, early recognition of sepsis and its appropriate treatment is of paramount importance in reducing mortality.3
One of the essential facets of sepsis management to maximise survival rates is the rapid administration of appropriate antimicrobials. Several studies have reported that each hour’s delay in the administration of appropriate antimicrobials is associated with a measurable increase in mortality in patients with sepsis or septic shock.4 Further, failure to initiate appropriate empiric therapy in patients with sepsis and septic shock has been associated with a substantial increase in mortality.5,6
Based on this evidence, the Surviving Sepsis Campaign (SSC) guidelines strongly recommend that empiric broad-spectrum therapy be conducted with one or more antimicrobials as soon as possible after the recognition of sepsis or septic shock, to cover all likely pathogens, including bacterial, fungal or viral coverage7 ideally within 1 hour of sepsis recognition.8
However, the distribution of causative pathogens has changed over time,9 and the global rise in antimicrobial-resistant pathogens has made it difficult to routinely conduct empiric broad-spectrum antimicrobial therapy.9,10 To optimise the accurate selection of initial antimicrobial agents, clinicians should consider the various factors associated with the causative pathogens, including:
Patient pre-existing comorbidities,
Prior knowledge of pathogens known to colonise the patient,
Prior antibiotic exposures and
The local pattern of causative pathogens, antibiotic resistance and zoonotic pathogens.11,12
Furthermore, there is no one-size-fits-all empiric antimicrobial therapy for sepsis because the typical pathogen profile varies according to the anatomical site of infection. Although there are multiple lines of evidence related to the causative pathogens in paediatric sepsis,13,14 there are only limited reports in adult sepsis. Blood cultures taken from patients attending emergency departments are an important antibiotic stewardship tool, which directly influences patient management.15
Therefore, updating knowledge on the current distribution of causative pathogens in adult sepsis is required to initiate appropriate antimicrobial therapy. The aims of this study were to provide updated and detailed information on the distribution of causative pathogens in adult sepsis and study their antibiotic-susceptibility pattern.
AIM AND OBJECTIVES
Aim
To find out the common pathogens/microbes and their respective antimicrobial drug susceptibility in suspected sepsis patients presenting to the Emergency Department.
Objectives
To study the clinical spectrum of sepsis cases presenting to Emergency Department.
To study the microbiological profile of sepsis cases presenting to Emergency Department.
To study the antimicrobial drug-susceptibility pattern of isolated organisms in sepsis cases.
MATERIALS AND METHODS
Study Area
Emergency Department, Fortis Hospital Mulund, Mumbai.
Study Population
All suspected sepsis patients arriving at the Emergency Department whose blood cultures are being sent from the ER.
Study Design
A hospital-based cross-sectional study.
Sample-size Calculation
The sample size was calculated using the following formulae:
n – sample size.
Zα/2 – Z value at 5% error (1.96).
P – prevalence of septicaemia (taken as 28%).
E – allowable error (taken as 10%).
n –
N – 80 (approx.)
So, by rounding off, we will be taking 121 subjects.
Consecutive type of non-probability sampling will be followed for the selection of study subjects. A total of 121 patients fulfilling the eligibility criteria were taken for study after taking informed consent.
Study Duration
18 months.
Inclusion Criteria
Age >18 years.
Both genders.
Blood cultures reported positive for growth of organism.
Exclusion Criteria
Limitation of sustained life care or post cardiopulmonary arrest resuscitation status at the time of sepsis diagnosis.
Pregnant and lactating females.
METHODOLOGY
As per predefined, inclusion and exclusion criteria patients were included in the study.
All these patients were evaluated thoroughly by clinical, radiological and laboratory methods.
Most of the patients in the study sample were from the Mumbai region barring a few who were referred from other regions such as Kalyan, Thane and Navi Mumbai.
These patients were provisionally diagnosed to have sepsis in the ER, barring a few who were diagnosed elsewhere and referred here.
Blood cultures were collected from peripheral veins, other sites were excluded because these could confound the results.
Each patient was started on empirical therapy as per the current protocol.
Susceptibility testing was done by Kirby–Bauer disc diffusion method and interpreted according to the Clinical and Laboratory Standards Institute (CLSI) guidelines – 2012.
Empirical upgradation of antibiotics or change in antibiotics was done as per the culture sensitivity report.
Statistical Analysis
All the data were noted down in a pre-designed study proforma. Qualitative data were represented in the form of frequency and percentage. Quantitative data were represented using mean ± SD. SPSS Version 21.0 was used for most analyses, and Microsoft Excel 2010 for graphical representation.
RESULTS
Mean age of the study cases was 59.3 years with 59.5% cases that belonged to elderly age group (Fig. 1).
Male predominance was seen among cases of suspected sepsis with 56.2% males–43.8% females (Fig. 2).
The most common organism isolated from cases with sepsis was Escherichia coli (45.5%) followed by Klebsiella (13.2%), Salmonella (10.7%), Stenotrophomonas (7.4%) and Pseudomonas (5%). Among Gram-positive organisms, Staphylococcus aureus was the most common organism isolated (1.7%) (Table 1).
Organism | N | % |
---|---|---|
E. coli | 55 | 45.5 |
Klebsiella | 16 | 13.2 |
Salmonella | 13 | 10.7 |
Stenotrophomonas | 9 | 7.4 |
Pseudomonas | 6 | 5.0 |
Acinetobacter | 4 | 3.3 |
Proteus mirabilis | 4 | 3.3 |
Burkholderia | 3 | 2.5 |
Achromobacter | 1 | 0.8 |
Morganella morganii | 1 | 0.8 |
Serratia fonticola | 1 | 0.8 |
Shigella | 1 | 0.8 |
Sphingomonas | 1 | 0.8 |
MRSA | 1 | 0.8 |
S. aureus | 1 | 0.8 |
Not detected | 4 | 3.3 |
Total | 121 | 100.0 |
Overall Gram-negative isolates were seen in 95% of cases, while Gram-positive isolates were seen in only 1.7% cases (Table 2).
Organism | N | % |
---|---|---|
Gram-positive | 2 | 1.7 |
Gram-negative | 115 | 95.0 |
Not detected | 4 | 3.3 |
Total | 121 | 100.0 |
DISCUSSION
Sepsis is the combination of a known or suspected infection and an accompanying systemic inflammatory response. The prognosis of the patient with severe sepsis is related to the number of dysfunctional organs. One of the essential facets of sepsis management to maximise survival rates is the rapid administration of appropriate antimicrobials. Several studies have reported that each hour’s delay in the administration of appropriate antimicrobials is associated with a measurable increase in mortality in patients with sepsis or septic shock.4
Based on this evidence, the Surviving Sepsis Campaign (SSC) guidelines strongly recommend that empiric broad-spectrum therapy be conducted with one or more antimicrobials as soon as possible after the recognition of sepsis or septic shock, to cover all likely pathogens, including bacterial, fungal or viral coverage.7
However, the distribution of causative pathogens has changed over time,9 and the global rise in antimicrobial-resistant pathogens has made it difficult to routinely conduct empiric broad-spectrum antimicrobial therapy.9,10 Therefore, updating knowledge on the current distribution of causative pathogens in sepsis is required to initiate appropriate antimicrobial therapy.
In this study, we thus aimed to find out the common pathogens/ microbes and their respective antimicrobial drug susceptibility in suspected sepsis patients presenting to the Emergency Department. The study included 121 suspected sepsis patients arriving to Emergency Department whose blood cultures are being sent from the Emergency room (ER).
Demography
Mean age of the study cases was 59.3 years with 59.5% cases that belonged to elderly age group. Male predominance was seen among cases of suspected sepsis with 56.2% males–43.8% females.
The study by Todi S et al.16 had shown that sepsis is common in elderly age group (>50 years, 61%) and in males (57.71%). Peres Bota DP et al.,17 in a similar study observed the mean age as 59.76 years with male predominance (71% vs 29%). Dash et al.,18 in a similar study, observed the mean age of cases was 58.15 years, with male and female ratio as 1.63:1.
Thus, from the above observations, it was evident that sepsis mostly affects adult males after their fifth decade of life. The waning immunity in the elderly age group could be attributed to this observation.
Organisms Isolated
Overall, Gram-negative isolates were seen in 95% cases, while Gram-positive isolates were seen in only 1.7% cases. The most common organism isolated from cases with sepsis was E. coli (45.5%) followed by Klebsiella (13.2%), Salmonella (10.7%), Stenotrophomonas (7.4%) and Pseudomonas (5%). Among Gram-positive organisms, S. aureus was the most common organism isolated (1.7%).
In the ANZICS study,19 Gram-negative isolates were seen in 90% of the cases with E. coli being the most common (29.3%) Gram-negative organism and methicillin-sensitive S. aureus (3.1%), the most common Gram-positive organism. Chatterjee S et al.20 in their study observed that the majority of hospital-acquired infections were caused by Gram-negative organisms (73%). The commonly isolated microbes were Acinetobacter baumannii (21.2%), Pseudomonas aeruginosa (17%) and equal prevalence of Klebsiella and E. coli (15.4%). In the study by Kumalo et al.,21 observed 53.3% were for Gram-negative bacteria and 46.7% for Gram-positive bacteria. The predominant isolates were E. coli and S. aureus from the total isolate that constitutes for Gram-positive and Gram-negative organisms, respectively. Vendemiato AVR et al.22 observed prevalent microorganisms such as coagulase-negative Staphylococcus (15.87%), E. coli (13.0%), S. aureus (11.7%), Klebsiella (9.8%), Enterobacter (9.5%), Acinetobacter (9.2%), Pseudomonas (5.7%) and Candida (5.1%). Fuchs A et al.23 in their study observed that Gram-positive cocci (GPC) and Gram-negative rods (GNR) were isolated in the same proportion of 44.4% (n = 8) each. In 11.1% of cases (n = 2), Candida spp. were isolated. The most common bacterial isolates were S. aureus (n = 7, 38.9%) and E. coli (n = 4, 22.2%).
The difference in microbiological profile across studies can be attributed to the difference in prevalent organisms in a particular area and region, which also varies on time-to-time basis. However, Gram-negative organisms were the predominant organisms causing sepsis across most studies.
Antimicrobial Susceptibility
The most common organism isolated from cases with sepsis was E. coli (45.5%) followed by Klebsiella (13.2%), Salmonella (10.7%), Stenotrophomonas (7.4%) and Pseudomonas (5%). Among Gram-positive organisms, S. aureus was the most common organism isolated (1.7%).
Over half of the E. coli and Klebsiella isolates showed poor sensitivity towards fluoroquinolones and cephalosporins while good sensitivity towards aminoglycosides, carbapenems and combination drugs like Cefoperazone–Sulbactam and PipTaz. Salmonella isolates showed good sensitivity towards cephalosporins and ampicillin and resistance towards fluoroquinolones and nalidixic acid. Out of the 9 isolates of Stenotrophomonas, 7 showed sensitivity towards TMP–SFX and 2 showed resistance. Pseudomonas isolates showed resistance towards fluoroquinolones and imipenem, while moderate sensitivity was observed towards aminoglycosides, cephalosporin and good sensitivity towards meropenem. The isolate of MRSA was sensitive only towards clindamycin while resistant to fluroquinolones and beta-lactam antibiotics. A single isolate of S. aureus was sensitive towards clindamycin, oxacillin and TMP–SFX while resistant towards ampicillin and benzyl penicillin.
In the study by Kumalo et al.,21 they observed antimicrobial resistance levels for the Gram-negative organisms, causing adult sepsis that ranged from 14.3% to 85.7%. A single P. aeruginosa isolate was sensitive to ciprofloxacin and gentamicin. An isolate of Enterobacter species was sensitive to all drugs, except cephalothin. The ranges of resistance for Gram-positive isolates were from 0% to 100%. All isolates of Gram positives showed resistance against penicillin-G (8/8, 100%), but they showed high susceptibility to most of the other antimicrobials tested: ceftriaxone (7/8, 87.5%), chloramphenicol (7/8; 87.5%), ciprofloxacin (7/8, 87.5%), amoxicillin–clavulanic acid (6/8, 75%), cephalothin (5/8, 62.5%) and erythromycin (5/8, 62.5%). From a total of six S. aureus, two (33.3 %) were methicillin-resistant (MRSA) (cefoxitin disc used), whereas the remaining four of them (66.7 %) were methicillin-sensitive (MSSA). Among S. aureus strains isolated from blood culture, 2/6, 33.3% were MRSA. In this study, 50% of S. aureus strains were MRSA. In general, ciprofloxacin was the effective drug against the tested Gram-positive and Gram-negative bacteria (86.7%, 13/15). But in this study, most of the organisms were resistant for ciprofloxacin.
Vendemiato AVR et al.22 revealed that 51% of the S. aureus isolates were MRSA. For A. baumannii, the ideal profile drugs were ampicillin–sulbactam and piperacillin/tazobactam, and for P. aeruginosa, they were piperacillin/tazobactam and ceftazidime. Enterobacteria showed on average 32.5% and 35.7% resistance to beta-lactams and ciprofloxacin, respectively. When all Gram-negative bacteria were considered, the resistance to beta-lactams rose to 40.5%, and the resistance to ciprofloxacin rose to 42.3%.
Fuchs A et al.23 in their study observed that 71.4% of the isolated strains of S. aureus were resistant to co-trimoxazole and 28.6% to clindamycin. Half of the isolated S. aureus strains were MRSA. Antimicrobial resistance in the isolated Gram-negative bacterial isolates was much more common. Enterobacterales were frequently resistant to aminopenicillins combined with beta-lactamase-inhibitors (83.3%), 3rd-generation cephalosporins (66.7%), quinolones (66.7%) and sulphonamides (83.5%). Resistance to aminoglycosides (33.3%) and carbapenems (n = 1) was less frequent but still considerably high.
The results of the studies showed high-level antimicrobial resistance in sepsis cases for commonly used antimicrobials. The difference in microbiological-susceptibility profile across studies shows the importance of regular surveillance to determine the local prevalence of organisms and antimicrobial susceptibilities in order to guide the proper empirical management of adults’ sepsis cases.
SUMMARY AND CONCLUSION
Summary
A hospital-based observational study was conducted at Emergency department, Fortis Hospital Mulund, Mumbai. The study aimed to find out the common pathogens/microbes and their respective antimicrobial drug susceptibility in suspected sepsis patients presenting to the Emergency Department. The study included 121 suspected sepsis patients arriving to the Emergency Department whose blood cultures are being sent from the Emergency room (ER) and reported positive for microbial infection. The following observations were made during the study:
Mean age of the study cases was 59.3 years with 59.5% cases that belonged to elderly age group.
Male predominance was seen among cases of suspected sepsis with 56.2% males–43.8% females.
The most common organism isolated from cases with sepsis was E. coli (45.5%) followed by Klebsiella (13.2%), Salmonella (10.7%), Stenotrophomonas (7.4%) and Pseudomonas (5%). Among Gram-positive organisms, S. aureus was the most common organism isolated (1.7%).
Overall, Gram-negative isolates were seen in 95% cases, while Gram-positive isolates were seen in only 1.7% cases.
E. coli isolates showed poor sensitivity towards fluoroquinolones and cephalosporins, while good sensitivity towards aminoglycosides, carbapenems and combination drugs like Cefoperazone–Sulbactam and PipTaz.
Klebsiella isolates also showed poor sensitivity towards fluoroquinolones and cephalosporins, while good sensitivity towards aminoglycosides, carbapenems and combination drugs like Cefoperazone–Sulbactam and PipTaz.
Salmonella isolates showed good sensitivity towards cephalosporins and ampicillin and resistance towards fluoroquinolones and nalidixic acid.
Out of the 9 isolates of Stenotrophomonas, 7 showed sensitivity towards TMP–SFX and 2 showed resistance.
Pseudomonas isolates showed resistance towards fluoroquinolones and imipenem, while moderate sensitivity was observed towards aminoglycosides, cephalosporin and good sensitivity towards meropenem.
The isolate of MRSA was sensitive only towards clindamycin, while resistant to fluroquinolones and beta-lactam antibiotics.
A single isolate of S. aureus was sensitive towards clindamycin, oxacillin and TMP–SFX, while resistant towards ampicillin and benzyl penicillin.
CONCLUSION
This study observed the microbiological profile and antibiotic-susceptibility pattern of adult sepsis cases. Gram-negative organisms are the most common isolates observed in this study with E. coli being the predominant pathogen followed by Klebsiella. High-level antimicrobial resistance was observed in sepsis cases for commonly used antimicrobials like fluoroquinolones and cephalosporins.
This knowledge is very necessary to treat sepsis cases empirically in the hospital settings. Hence, regular surveillance should be carried out to determine the local prevalence of organisms and antimicrobial susceptibilities in order to guide the proper management of adults’ sepsis cases.
Post cardiac-sustained life care or post cardiopulmonary arrest resuscitation status at the time of sepsis diagnosis have been excluded from the study as these result in changes in the body that mimic sepsis-like syndrome and could act as a confounding factor in the study. Pregnant females have been excluded from the study as the evaluation and management of maternal sepsis are complicated because of physiological changes that occur during pregnancy.
ORCID
Deepak Kishor Sharma https://orcid.org/0009-0005-3162-6414
Sandeep B Gore https://orcid.org/0009-0004-0585-2015
REFERENCES
1. Angus DC, Linde-Zwirbe WT, Lidicker J, et al. Epidemiology of severe sepsis in the United States: Analysis of incidence, outcome, and associated costs of care. Crit Care Med 2001;29(7):1303–1310. DOI: 10.1097/00003246-200107000-00002.
2. Vincent JL, Sakr Y, Sprung CL, et al. Sepsis occurrence in acutely III patients investigators. Sepsis in European intensive care units: Results of the SOAP study.Crit Care Med 2006;34(2):344–353. DOI: 10.1097/01.ccm.0000194725.48928.3a.
3. Tarassenko L, Hann A, Young D. Integrated monitoring and analysis for early warning of patient deterioration. Br J Anaseth 2006;97(1):64–68. DOI: 10.1093/bja/ael113.
4. Ferrer R, Martin-Loeches I, Phillips G, et al. Empiric antibiotic treatment reduces mortality in severe sepsis and septic shock from the first hour: Results from a guideline-based performance improvement program. Crit Care Med 2014;42(8):1749–1755. DOI: 10.1097/CCM.0000000000000330.
5. Barie PS, Hydo LJ, Shou J, et al. Influence of antibiotic therapy on mortality of critical surgical illness caused or complicated by infection. Surg Infect (Larchmt) 2005;6(1):41–54. DOI: 10.1089/sur.2005.6.41.
6. Paul M, Shani V, Muchtar E, et al. Systematic review and meta-analysis of the efficacy of appropriate empiric antibiotic therapy for sepsis. Antimicrob Agents Chemother 2010;54(11):4851–4863. DOI: 10.1128/AAC.00627-10.
7. Rhodes A, Evans LE, Alhazzani W, et al. Surviving sepsis campaign: international guidelines for management of sepsis and septic shock: 2016. Intensive Care Med 2017;43(3):304–377. DOI: 10.1007/s00134-017-4683-6.
8. Evans L, Rhodes A, Alhazzani W, et al. Executive Summary: Surviving Sepsis Campaign: International Guidelines for the Management of Sepsis and Septic Shock 2021. Crit Care Med 2021;49(11):1974–1982. DOI: 10.1097/CCM.0000000000005357.
9. Balkhy HH, El-Saed A, Alshamrani MM, et al. Ten-year resistance trends in pathogens causing healthcare-associated infections; reflection of infection control interventions at a multi-hospital healthcare system in Saudi Arabia, 2007–2016. Antimicrob Resist Infect Control 2020;9(1):21. DOI: 10.1186/s13756-020-0678-0.
10. Avery LM, Nicolau DP. Investigational drugs for the treatment of infections caused by multidrug-resistant Gram-negative bacteria. Expert Opin Investig Drugs 2018;27(4):325–338. DOI: 10.1080/13543784.2018.1460354.
11. Zaidi AK, Thaver D, Ali SA, et al. Pathogens associated with sepsis in newborns and young infants in developing countries. Pediatr Infect Dis J 2009;28(1 Suppl):S10–S18. DOI: 10.1097/INF.0b013e3181958769.
12. Han BA, Kramer AM, Drake JM. Global patterns of zoonotic disease in mammals. Trends Parasitol 2016;32(7):565–577. DOI: 0.1016/j.pt.2016.04.007.
13. Aku FY, Akweongo P, Nyarko K, et al. Bacteriological profile and antibiotic susceptibility pattern of common isolates of neonatal sepsis, Ho Municipality, Ghana–2016. Matern Health Neonatol Perinatol 2018;4:2. DOI: 10.1186/s40748-017-0071-z.
14. Dong H, Cao H, Zheng H. Pathogenic bacteria distributions and drug resistance analysis in 96 cases of neonatal sepsis. BMC Pediatr 2017;17(1):44. DOI: 10.1186/s12887-017-0789-9.
15. Boyles TH, Davis K, Crede T, et al. Blood cultures taken from patients attending emergency departments in South Africa are an important antibiotic stewardship tool, which directly influences patient management. BMC Infect Dis 2015;15:410. DOI: 10.1186/s12879-015-1127-1.
16. Todi S, Chatterjee S, Sahu S, et al. Epidemiology of severe sepsis in India: A update. Crit Care 2010;14(Suppl 1):P382. DOI: 10.1186/cc8614.
17. Peres Bota D, Melot C, Lopes Ferreira F, et al. The Multiple Organ Dysfunction Score (MODS) versus the Sequential Organ Failure Assessment (SOFA) score in outcome prediction. Intensive Care Med 2002;28(11):1619–1624. DOI: 10.1007/s00134-002-1491-3.
18. Dash L, Singh LK, Murmu M, et al. Clinical profile and outcome of organ dysfunction in sepsis. Int J Res Med Sci 2018;6(6):1927–1933. DOI: 10.18203/2320-6012.ijrms20182045.
19. Finfer S, Bellomo R, Lipman J, et al. Adult-population incidence of severe sepsis in Australian and New Zealand intensive care units. Intensive Care Med 2004;30(4):589–596. DOI: 10.1007/s00134-004-2157-0.
20. Chatterjee S, Bhattacharya M, Todi SK. Epidemiology of adult-population sepsis in India: A single center 5-year experience. Indian J Crit Care Med 2017;21(9):573–577. DOI: 10.4103/ijccm.IJCCM_240_17.
21. Kumalo A, Kassa T, Daka D, et al. Bacterial profile of adult sepsis and their antimicrobial susceptibility pattern at Jimma University specialized hospital, south West Ethiopia. Health Sci J 2016;10(2):10–16. Available from: https://api.semanticscholar.org/.
22. Vendemiato AVR, von Nowakonski A, Marson FAdL, et al. Microbiological characteristics of sepsis in a University hospital. BMC Infect Dis 2015;15:58. DOI: 10.1186/s12879-015-0798-y.
23. Fuchs A, Tufa TB, Hörner J, et al. Clinical and microbiological characterization of sepsis and evaluation of sepsis scores. PLos One 2021;16(3):e0247646. DOI: 10.1371/journal.pone.0247646.
________________________
© The Author(s). 2023 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (https://creativecommons.org/licenses/by-nc/4.0/), which permits unrestricted use, distribution, and non-commercial reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.