eCommons@AKU

Department of Anaesthesia Medical College, Pakistan

January 2016

Incidence, outcome and risk factors for sepsis- a

two year retrospective study at surgical intensive
care unit of a teaching hospital in Pakistan
Ali Asghar
Aga Khan University

Madiha Hashmi
Aga Khan University, madiha.hashmi@aku.edu

Saima Rashid
Aga Khan University

Fazal Hameed Khan

Aga Khan University, fazal.hkhan@aku.edu

Follow this and additional works at: http://ecommons.aku.edu/pakistan_fhs_mc_anaesth

Part of the Anesthesiology Commons

Recommended Citation
Asghar, A., Hashmi, M., Rashid, S., Khan, F. (2016). Incidence, outcome and risk factors for sepsis- a two year retrospective study at
surgical intensive care unit of a teaching hospital in Pakistan. Journal of Ayub Medical College, 28(1), 79-83.
Available at: http://ecommons.aku.edu/pakistan_fhs_mc_anaesth/110
 J Ayub Med Coll Abbottabad 2016;28(1)

ORIGINAL ARTICLE
INCIDENCE, OUTCOME AND RISK FACTORS FOR SEPSIS - A TWO
YEAR RETROSPECTIVE STUDY AT SURGICAL INTENSIVE CARE
UNIT OF A TEACHING HOSPITAL IN PAKISTAN
Ali Asghar, Madiha Hashmi, Saima Rashid, Fazal Hameed Khan
Department of Anaesthesiology, Aga Khan University, Karachi-Pakistan

Background: Sepsis is amongst the leading causes of admission to the intensive care units and is
associated with a high mortality. However, data from developing countries is scares. Aim of conducting
this study was to determine the incidence, outcome and risk factors for sepsis on admission to surgical
intensive care unit (SICU) of a teaching hospital in Pakistan. Methods: Two year retrospective
observational study included all consecutive adult admissions to the surgical intensive care unit (SICU)
of a University Hospital, from January 2012 to December 2013. Results: Two hundred and twenty-
nine patients met the inclusion criteria. Average age of the patients was 46.35±18.23 years (16–85),
mean Acute Physiology and Chronic Health Evaluation II (APACHE II) score was 15.92±8.13 and
males were 67.6%. Median length of ICU stay was 4 [IQR 5]. 43% patients fulfilled the criteria of
sepsis at the time of admission to the SICU and incidence of severe sepsis/septic shock was 35%.
Abdominal sepsis was the most frequent source of infection (57.5%). The overall intensive care unit
mortality was 32.31% but the mortality of sepsis-group was 51.15% as compared to 17.7% of the non-
sepsis group. Stepwise logistic regression model showed that increasing age, female gender, non-
operative admission, admission under general surgery and co-morbidities like ischaemic heart disease
and chronic kidney disease were significant predictors of sepsis. Conclusion: The incidence of sepsis
and severe sepsis/septic shock, on admission to SICU is high and mortality of the sepsis group is nearly
three times the mortality of the non-sepsis group.
Keywords: Sepsis, severe sepsis, septic shock, intensive care units, incidence
J Ayub Med Coll Abbottabad 2016;28(1):79–83

INTRODUCTION with and without sepsis in order to identify risk factors

of sepsis in this cohort of patients. The secondary
Sepsis represents a significant socioeconomic burden
objective was to document the frequency of use of
worldwide. Extrapolating data from high-income
Surviving Sepsis Campaign (SSC)9 recommended
countries, approximately 31 million cases of sepsis are
interventions in the sepsis group.
reported globally with about 6 million deaths per year.1
The incidence and rate of hospitalization for severe MATERIAL AND METHODS
sepsis increases annually and sepsis is amongst the
This 2 year retrospective observational study was
leading causes of admission to the intensive care units
exempted for review from the institutional ethical
(ICUs) in the United States.2–4 The incidence of sepsis in
review committee. Files of all consecutive adult (non-
studies reported in the last decade ranges from 9–37%
cardiac) admissions to the surgical intensive care unit
for all patients admitted to the ICUs and severe sepsis
(SICU), from January 2012 to December 2013 were
remains a leading cause of death. Mortality rates for
reviewed. Cases with an incomplete record, death or
severe sepsis in patients admitted to intensive care units
discharge from ICU earlier than 24 hours and
vary from 30 to 50%.2,4–6
documentation of do not resuscitate orders within 24
The largest part of the global sepsis burden
hours of admission were excluded from the study. In
occurs in low and middle -income countries. 90% of the
case of re-admission, only the first admission was
worldwide deaths from pneumonia, meningitis or other
considered. Data was collected on predesigned forms by
infections occur in less developed countries and
the team of primary investigators. Department data entry
majority of deaths in neonates and infants attributable to
officer entered and stored all the data on SPSS. Data
sepsis occur in Asia and sub-Saharan Africa.7,8 Statistics
was reviewed periodically by the primary investigators
from developing countries however are limited to sepsis
and ambiguities resolved by a re-review of the patients
in under-five children and maternal sepsis.
medical record. The demographic information (age and
The prevalence and outcome of sepsis in
gender), admitting department, primary diagnosis,
intensive care units in Pakistan is largely unknown. The
presence of co-morbidities (i.e., diabetes mellitus (DM),
primary objective of this study was to estimate the
hypertension (HTN), ischaemic heart disease (IHD),
incidence of sepsis on admission to the surgical
chronic kidney disease (CKD), chronic obstructive
intensive care unit (SICU) of a tertiary care hospital and
pulmonary disease (COPD), malignancy or history of
compare the characteristics and outcome of patients

http://www.jamc.ayubmed.edu.pk 79
 J Ayub Med Coll Abbottabad 2016;28(1)

alcohol abuse), type of admission (elective surgery, the operative group 85% patients underwent emergency
emergency surgery or non-operative), APACHE II surgical procedures and 15% had elective surgeries.
score, length of ICU stay and outcome (discharge or Admissions under various departments are as shown in
death in ICU and hospital) were documented on the the figure-1. The overall intensive care unit mortality
study Performa. Cases were assigned to the sepsis group was 32.31% and the hospital mortality was 34%. The
if they fulfilled the American College of Chest median length of ICU stay was 4 [IQR 5] 2–45 days
Physicians/Society of Critical Care Medicine Consensus (min-max).
Conference criteria of defining sepsis10, i.e., presence A total of 99 (43%) patients fulfilled the
of two or more systemic inflammatory response criteria of sepsis at the time of admission and 81% of
syndrome (SIRS) criteria along with suspected or these patients were in severe sepsis or septic shock.
documented source of infection, either in the surgeon’s Presence of SIRS criteria in both septic and non-septic
notes, nursing notes, positive culture report or patients is shown in table-1.
radiological evidence. The most likely source of Abdominal sepsis was the most frequent
infection was classified as lungs, urinary tract, abdomen, source of infection (57.5%) in this cohort of SICU
musculoskeletal, central nervous system, or peripartum. patients, rest are shown in figure-2. The characteristics
In case of more than one likely source of infection, the of patients with and without sepsis are compared in
source of most severe infection at the time of table-2.
presentation was considered. The sepsis and non-sepsis The incidence of sepsis was highest in the non-
groups were compared for mean age, gender, Acute operated group (52%), followed by emergency surgery
Physiology and Chronic Health Evaluation II group (43%) and elective surgery group (16%). The
(APACHE II) score, type of admission, co morbidities, incidence of sepsis was highest in the patients admitted
admitting departments, ICU mortality and length of ICU under the care of departments of orthopaedics (9/10) and
stay. In the sepsis group compliance with the SSC- urology (7/10) followed by general surgery (63/97) and
recommended-interventions carried out after admission it was the lowest in the neurosurgical patients (11/84).
to SICU were recorded. Key interventions recorded The sepsis group was associated with a higher incidence
included serum lactate, blood cultures, broad spectrum of comorbid as shown in figure-3.
antibiotic cover, central venous access, ScvO2, fluid In univariate analysis, age, APACHE II score,
challenge, and vasopressor use. type of admission, DM, IHD and CKD and general
All statistical analyses were performed with surgery were significant independent predictor of sepsis
the software SPSS-19. Statistical analysis results were while in multivariate analysis, stepwise logistic
expressed as mean±standard deviations for continuous regression model showed that increasing age, female
variables and numbers and percentages for categorical gender, non-operative admission, admission under
variables. Independent sample t-test and Mann-Whitney general surgery and co-morbidities like IHD and CKD
U test were used as per condition of normality checked were significant predictor of sepsis in the final model as
by Kolmogorov-smirnov and histogram for quantitative shown in table-3.
observations and chi-square test was applied to compare Except for measuring central venous oxygen
categorical observation between sepsis and non-sepsis saturation (34/99), compliance with most of the
groups. Unadjusted odd ratio were computed by logistic interventions recommended by the SSC guidelines in the
regression and for adjusted Odd ratio step wise multiple patients diagnosed with sepsis on admission or during the
logistic regression was applied to build model to predict SICU stay was more than 90%, i.e., serum lactate (93%),
sepsis. p≤0.05 was considered as significant blood cultures (93%), antibiotics (100%), fluid boluses
(96%), CVP (96%), and vasopressors (78%).
RESULTS
Five hundred and forty seven surgical admissions in two
years, from January, 2011 till December, 2012 were
evaluated. Three hundred and eighteen (58%) patients
were excluded from the study due to missing files or
incomplete data recorded or not meeting the inclusion
criteria. The study group, therefore, consisted of 229
patients. Patients admitted to the SICU were
predominantly male (67.6%), average age was
46.35±18.23 years (16–85) and the mean APACHE II
score was 15.92. One hundred and fifty-six patients
were received from the operating rooms (68%) and
seventy-three non-operative (32%) patients were Figure-1: Primary departments admitting patients
received from emergency room and surgical wards. In to SICU

80 http://www.jamc.ayubmed.edu.pk
 J Ayub Med Coll Abbottabad 2016;28(1)

Figure-3: Comorbidities in SICU admissions,

Figure-2: Source of infection on admission to SICU sepsis, non-sepsis and overall
Table-1: SIRS criteria in sepsis and non-sepsis groups on admission to SICU, n=229
SIRS Criteria Sepsis Non-sepsis p-value
n=99 n=130
Temperature >38 or <36 C 93 (93%) 14 (10.8%) 0.0005
Heart rate >100/min 91 (91.1%) 33 (25.6%) 0.0005
Respiratory rate >28/min 81 (81.8%) 18 (14%) 0.0005
WCC >14,000 OR <4,000/min 76 (76.8%) 4 (3%) 0.0005

Table-2: Comparison of characteristics of patients with and without sepsis n=229

Variables Overall Sepsis n=99 Non-Sepsis n=130 p-Value
APACHE II score 15.92±8.13 19.47±8.40 13.13±6.43 0.005
Average age 46.35±18.23 52.81±18.87 41.44±16.14 0.0005
Male 155 (67.7%) 62 (62.6%) 93 (71.5%) 0.15
Female 74 (32.3%) 37 (34.7%) 37 (28.5%)
Non-Operative 73 (31.9%) 38 (38.4%) 35 (26.9%) 0.01
OR-Emergency 132 (57.6%) 57 (57.6%) 75 (57.7%)
OR-Elective 24 (10.5%) 4 (4%) 20 (15.4%)
Co-morbidities 85 (37.1%) 49 (49.5%) 36 (27.7%) 0.001
DM 37 (16.2%) 27 (27.3%) 10 (7.7%) 0.005
HTN 54 (23.6%) 26 (26.3%) 28 (21.5%) 0.404
IHD 31 (13.5%) 23 (23.2%) 8 (6.2%) 0.005
CKD 12 (5.2%) 10 (10.1%) 2 (1.5%) 0.004
COPD 09 (3.9%) 6 (6.1%) 3 (2.3%) 0.18
Malignancy 9 (3.9%) 4 (4%) 5 (3.8%) 0.99
Alcohol 3 (1.3%) 2 (2%) 1 (0.8%) 0.41
Admitting Departments
Neuro Surgery 84 (36.7%) 11 (11.1%) 73 (56.2%) 0.0005
General Surgery 97 (42.4%) 63 (63.6%) 34 (26.2%) 0.0005
Obs and Gynae 14 (6.1%) 6 (6.1%) 8 (6.2%) 0.977
Ortho 10 (4.4%) 9 (9.1%) 1 (0.8%) 0.003
Urology 10 (4.4%) 7 (7.1%) 3 (2.3%) 0.106
CTS 3 (1.3%) 1 (1%) 2 (1.5%) 0.990
ENT 5 (2.2%) 0 (0%) 5 (3.8%) 0.070
Vascular 6 (2.6%) 2 (2%) 4 (3.1%) 0.701
ICU Stay 0.023
Median [ IQR] 4 [5] 5 [4] 3 [4]
Min-Max 2–45 2–42 2–38
Mortality in ICU 74 (32.3%) 51 (51.5%) 23 (17.7%) 0.0005

Table-3: Factors associated with sepsis, univariate and multivariate stepwise logistic regression analysis model
Predictors Univariate Multivariate
OR 95%CI p-Value Crud OR 95%CI p-Value
Age (Per years increase)) 1.037 1.02–1.05 <0.001 1.04 1.02–1.06 <0.001
APACHE Score 1.06 1.03–1.10 <0.001
Male 0.66 0.38–1.16 0.15 0.35 0.16–0.79 0.012
Female 1 1.00
Type of admission
Non-Operative 5.42 1.68–17.44 <0.01 38.42 5.35–275.63 <0.001
OR-E 3.8 1.23–11.73 0.02 13.06 2.07–82.12 0.006
OR-Elect 1 1.00
Co-Morbidities
DM 4.5 2.05–9.83 <0.001
HTN 0.41 0.70–2.39 0.41 0.198 0.065–0.602 0.004
IHD 4.62 1.96–10.84 <0.001 3.7 1.00–13.97 0.05
CKD 7.19 1.53–33.61 0.012 56.16 6.89–457.2 <0.001
Admitting Departments
Neuro Surgery 0.098 0.048–0.20 <0.001 0.125 0.041–0.384 <0.001
General Surgery 4.94 2.81–8.71 <0.001 3.54 1.40–8.97 0.008
Obs & Gyn 0.98 0.33–0.29 0.97
Ortho 6.86 0.78–59.70 0.081
Multivariate, forward step wise logistic regression applied to predict sepsis

http://www.jamc.ayubmed.edu.pk 81
 J Ayub Med Coll Abbottabad 2016;28(1)

DISCUSSION orthopaedics and urology with infected fractures,

urinary tract infections and wound infections, admitted
Nearly 43% (99/229) patients presenting to SICU
either directly from the emergency department or
during the study period fulfilled the sepsis criteria on
surgical floors after undergoing surgery more than 48
admission. It is difficult to compare the sepsis rate with
hours prior to SICU admission. The incidence of
other studies due to variation in definitions used to
infection was very low in the neurosurgical (13%) and
identify ‘sepsis’ cases and the different patient
elective post-operative cases (4%). The most common
populations in medical, surgical or mixed ICUs. The
source of infection described in the previously quoted
SOAP study11, which is a large pan-European study also
studies is lung/respiratory tract, i.e., SOAP11 (64%),
used ACCP/SCCM definition of sepsis and described
EPIC II12 (63.5), Finfer15 (50.3%), MOSAIC14 (37.4%).
that 37% of adult patients admitted to predominantly
In this study lungs were considered as primary reason
medical ICUs, had sepsis. However, there was
for admission only in 5% of cases. The reason could be
considerable variation in the rates of sepsis reported
that we considered the most severe infection at the time
from the participating countries. For example higher
of admission, patients could have a respiratory tract
rates were reported from Portugal (73%), UK and
infection in addition to the most obvious surgical source
Ireland (52%) and Eastern Europe (48%), a nearly
or may have developed pneumonia during the course of
similar rate from Greece (43%) and France (41%) and
ICU stay but it was not captured in this study.
lower rates of sepsis as compared to this study were
The ICU mortality in this study was 32%
reported from countries like Netherlands (39%), Italy
which is less than the mortality reported from Asian
(38%), Spain (35%) and Switzerland (18%). The EPIC
intensive care units14 (36.7%). However, the mean
II study12 included predominantly surgical patients from
APACHE II score of predominantly medical/non-
Western Europe, Central and South America, Asia,
operated patients in that study was higher (22.8) as
Eastern Europe, North America, Oceania and Africa and
compared to the mean APACHE II score of our study
considered 51% patients to be infected on the day of the
(15.92). The mortality of the sepsis-group in this study
study, but infection rate was 32% in those patients
was nearly three times (51%) as compared to the non-
where the pre-study duration of ICU stay was 0-1 day.
sepsis group (17.7%). Alberti and co-workers16 reported
However in the EPIC II study ‘infection’ was defined
a similar mortality in non-infected (16.9%) and infected
according to the International Sepsis Forum definition11.
cases (53.6%) in 2002. Mortality of septic patients in
The incidence of severe sepsis in this study was 35%,
this study was twice as high as the mortality of infected
which is comparable to the incidence of severe sepsis
surgical patients in the EPIC II study12 (25%), the
reported in the SOAP study11 from countries like Italy
predominantly medical septic patients in the SOAP
(32%), Netherlands (34%), Eastern Europe (43%), UK
study11 (27%), Finfer’s study15 (26.5%) and a study
and Ireland (45%), but is very high as compared to
from US4 (28.6%). One reason could be that excluding
10.9% incidence of severe sepsis in Asian intensive care
19 patients, the rest of the patients in the sepsis-group
units (Phua)14 and 11.8% in Australian and New
had severe sepsis or septic shock (81%) on admission to
Zealand intensive care units (Finfer)15. A delay in
SICU, whereas the proportion of patients in severe
recognition of sepsis and inadequate resuscitation prior
sepsis varies from 10–64% in the other studies. The
to admission to the SICU in the non-operative group,
hospital where this study is was conducted is a tertiary
along with underlying disease severity in the emergency
referral centre for complicated general surgical patients
surgery group could explain the high incidence of severe
from other hospitals of the city as well as far-flung areas
sepsis/septic shock at the time of presentation to the
and is one of the few trauma centres in the city. Highest
SICU. The most common source of infection in this
admissions were for surgical emergencies like gut
study was abdominal sepsis (57.5%), followed by
perforations, gunshot injuries and blunt trauma,
musculoskeletal infections (16%). This reflects the
necrotizing fasciitis and necrotizing pancreatitis
unique case-mix of the SICU that predominantly admits
associated with a high mortality. High mortality could
emergency post-operative cases with highest admissions
also be due to the presence of comorbidities like
under general surgery. Admitting diagnoses of these
diabetes, ischaemic heart disease and chronic kidney
patients were intestinal perforations, intestinal
diseases in the sepsis group.
obstruction, abdominal gun-shot injuries, pancreatitis,
The SSC9 recommended interventions for
bowel ischaemia, obstructed hernias, abdominal
early recognition and management of sepsis and
malignancies, abdominal tuberculosis, blunt trauma and
compliance with the bundles has shown to improve
blast injuries and necrotizing fasciitis.
survivor17. To qualify as compliance with the
The non-operative group included patients
resuscitation bundles, predefined targets of mean arterial
who had no surgical intervention in the preceding 48
pressure (MAP), central venous pressure (CVP) or
hours and showed a very high incidence of sepsis
lactate clearance should be met. As this was a
(52%). Most of the patients in this group belonged to
retrospective study it was not possible to determine the

82 http://www.jamc.ayubmed.edu.pk
 J Ayub Med Coll Abbottabad 2016;28(1)

time of diagnosis of sepsis, study the effect of using the Med 2007;35(5):1244–50.
3. Martin GS, Mannino DM, Eaton S, Moss M. The epidemiology
interventions in achieving the specific targets, account
of sepsis in the United States from 1979 through 2000. N Engl J
for confounding factors like lead-time bias or Med 2003;348(16):1546–54.
standardize treatment received prior to admission to 4. Angus DC, Linde-Zwirble WT, Lidicker J, Clermont G, Carcillo
SICU. Therefore like a few other authors18,19 we also J, Pinsky MR. Epidemiology of severe sepsis in the United
States: analysis of incidence, outcome, and associated costs of
considered any attempt to measure lactate, central
care. Crit Care Med 2001;29(7):1303–10.
venous pressure, central venous oxygen saturation, send 5. Friedman G, Silva E, Vincent JL. Has the mortality of septic
blood cultures, given antibiotics, give fluids for shock changed with time. Crit Care Med 1998;26(12):2078–86.
resuscitation, or use vasopressors as compliance. This 6. Padkin A, Goldfrad C, Brady AR, Young D, Black N, Rowan K.
Epidemiology of severe sepsis occurring in the first 24 hrs in
explains the high compliance shown in this study with
intensive care units in England, Wales and Northern Ireland. Crit
the SSC recommendations in addition to the fact that the Care Med 2003;31(19):2332–8.
study was done in a university hospital where facilities 7. Cheng AC, West TE, Limmathurotsakul D, Peacock SJ.
for measuring lactate, arterial blood gas analysis, central Strategies to reduce mortality from bacterial sepsis in adults in
developing countries. PLoS Med 2008;5(8):e175.
venous oxygen saturation, blood cultures etc. are readily
8. Black RE, Cousens S, Johnson HL, Lawn JE, Rudan I, Bassani
available along with institutional protocols to manage DG, et al. Global, regional, and national causes of child mortality
sepsis. The major limitation of this study was the in 2008: a systematic analysis. Lancet 2010;375(9730):1969–87.
retrospective study design which resulted in exclusion 9. Dellinger RP, Levy MM, Rhodes A, Annane D, Gerlach H, Opal
SM, et al. Surviving Sepsis Campaign: International Guidelines
of a large number of cases admitted to the SICU during
for Management of Severe Sepsis and Septic Shock 2012. Crit
the study period, due to incomplete information. This Care Med 2013;42(2):580–637.
study also reflects the incidence of sepsis in surgical 10. American College of Chest Physicians/Society of Critical Care
patients in one hospital and may not reflect the Medicine Consensus Conference. Definitions for sepsis and
organ failure and guidelines for the use of innovative therapies in
incidence in other types of intensive care units and other
sepsis. Crit Care Med 1992;20(6):864–74.
hospitals. Multi centre hospital based studies and 11. Vincent JL, Sakr Y, Sprung CL, Ranieri VM, Reinhart K,
population studies are required to determine the true Gerlach H, et al. Sepsis in European intensive care units: Results
prevalence of sepsis at a national level. of the SOAP study. Crit Care Med 2006;34(2):344–53.
12. Vincent JL, Rello J, Marshall J, Silva E, Anzueto A, Martin CD,
CONCLUSION et al. International Study of the Prevalence and Outcomes of
Infection in Intensive Care Units. JAMA 2009;302(21):2323–9.
This study shows a high incidence of sepsis (43.23%) in 13. Calandra T, Cohen J. The International Sepsis Forum consensus
patients admitted to the SICU of a teaching hospital in conference on definitions of infection in the intensive care unit.
Karachi associated with a very high mortality (51.1%), Crit Care Med 2005;33(7):1538–48.
14. Phua J, Koh Y, Du B, Tang YQ, Divatia VJ, Tan C, et al.
as compared to the non-sepsis group. Stepwise logistic Management of severe sepsis in patients admitted to Asian
regression model showed that increasing age, female intensive care units: prospective cohort study. BMJ
gender, non-operative admission to SICU, admission 2011;342:d3245.
under general surgery and co-morbidities like IHD and 15. Finfer S, Bellomo R, Lipman J, French C, Dobb G, Myburgh J.
Adult-population incidence of severe sepsis in Australian and
CKD were significant predictor of sepsis in this cohort New Zealand intensive care units. Intensive care Med
of patients. 2004;30(4):589–96.
16. Alberti C, Brun-Buisson C, Burchardi H, Martin C, Goodman S,
ACKNOWLEDGEMENT Artigas A, et al. Epidemiology of sepsis and infection in ICU
patients from an international multicentre cohort study. Intensive
We are greatly indebted to Mr. Amir Raza: Research Care Med 2002;28(2):108–21.
coordinator, Department of Anaesthesiology, Aga Khan 17. Levy MM, Dellinger RP, Townsend SR, Linde-Zwirble WT,
University for statistical assistance. Marshall JC, Bion J, et al. The Surviving Sepsis Campaign:
Results of an international guideline-based performance
AUTHOR’S CONTRIBUTION improvement program targeting severe sepsis. Intensive Care
Med 2010;36(2):222–31.
All the authors contributed equally. 18. Lefrant JY, Muller L, Raillard A, Jung B, Beaudroit L, Favier L,
et al. Reduction of the severe sepsis or septic shock associated
REFERENCES mortality by reinforcement of the recommendations bundle: a
1. Fleischmann C, Scherag A, Adhikari NK, Hartog CS, Tsaganos multicenter study. Ann Fr Anesth Reanim 2010;29(9):621–8.
T, Schlattmann P, et al. Global burden of sepsis: A systematic 19. Cardoso T, Carneiro AH, Ribeiro O, Teixeira-Pinto A, Costa-
review. Crit Care 2015;19(suppl 1):P21. Pereira A. Reducing mortality in severe sepsis with the
2. Dombrovskiy VY, Martin AA, Sunderram J, Paz HL. Rapid implementation of a core 6-hour bundle: results from the
increase in hospitalization and mortality rates for severe sepsis in Portuguese community acquired sepsis study (SACiUCI study).
the United States: a trend analysis from 1993 to 2003. Crit Care Crit Care 2010;14(3):R83.

Address for Correspondence:

Ali Asghar, Department of Anaesthesiology, Aga Khan University, Karachi-Pakistan
Cell: +92 21 486 4631
Email: asghar.ashraf@aku.edu

http://www.jamc.ayubmed.edu.pk 83