TITLE PAGE

FULL TITLE: Rising antimicrobial resistance among pathogens isolated from blood? A 6-year
retrospective study from a teaching tertiary hospital in East Sikkim, India.
SHORT TITLE: Antibiotic resistance of bloodstream pathogens.
Abstract
Background: Bloodstream infections (BSI) is one of the most frequent infections in our hospital.
Methods: Retrospective result analysis and multidrug resistance index were estimated based on the findings
of laboratory-confirmed BSI between January 2013 to December 2018.
Results: Total of 1340 (10.2%) BSI were reported from 13091 blood culture. Bacterial organisms
constituted 97.1% of isolates whereas 2.9% were by fungi. Gram-positive and gram-negative bacteria
isolated were 518 (39.8%) and 783 (60.2%), respectively. Common organisms were coagulase-negative
Staphylococci (29.4%), Escherichia coli (19.8%), Klebsiella species (13.5%), Salmonella species (9.4%)
and Staphylococcus aureus (7.5%). Majority of the organisms were multidrug (3 antibiotics) resistant; most
resistance to second-generation cephalosporins and least to carbapenems. Multidrug resistance index was
highest in Acinetobacter species followed by Pseudomonas aeruginosa and Staphylococcus aureus.
Conclusions: Majority of BSI were caused by gram negative organisms. Rising antibiotic resistance needs
attention with stricter infection control and robust antimicrobial policy in our hospital.
Key words: Blood stream infection, BSI, Laboratory-confirmed BSI, Multidrug resistance index.

Introduction
Bloodstream infection (BSI) is a cause of grave concern to a health care facility and BSI caused by drug-
resistant organisms are common causes of morbidity, mortality and increased hospital expenditure globally.
[1-4] The clinical and epidemiological impact of antimicrobial resistance (AMR) is a worrisome trend
posing several limitations and challenges to clinicians and health-care policymakers alike. [3,5,6]
In the epidemiological triad (organism, host and environment) of BSI, the role of infecting organism
is often the most complex to determine. Stringent identification based upon varying parameters is of utmost
importance in distinguishing a commensal flora from a pathogen. [7,8] Therefore, adherence to guidelines
help in avoiding unnecessary treatment of colonisation in the absence of infection.[9] Although antibiotics
usage exerts selective pressure on the selection of AMR organisms, it is the poor/lack of infection prevention
and control practices that facilitate the dissemination of these organism types.[6] Such organisms once
established in the environment becomes increasingly difficult to eradicate.
In our hospital and laboratory, samples from blood are the second most common after urine. The
AMR among pathogens, particularly in a hospital setting, are increasing and variations in local trends and
epidemiology of BSI requires constant surveillance. [2,7,10, sentry] Therefore, to understand the trend in the
local epidemiology of BSI and emergence of AMR, the objective of this study was to evaluate the species
distribution and the antimicrobial susceptibilities of the pathogens isolated from blood in our hospital over a
6-year duration.
Materials and Methods
Study design and data collection:
This is a 6-year retrospective study (retrospective chart review), from January 2013 to December 2018, from
blood culture records of patients admitted to Central Referral Hospital (CRH). CRH is a 500 bedded
teaching hospital located in the East district of Sikkim, which is the least populated state in India.
The study was approved by the Institutional Research Protocol and Evaluation Committee and
considering the retrospective nature of the study Ethics clearance was waived. This study is a data collection
from pre-existing records and all the data were kept confidential.
Included in the study were the organisms from established LCBSI reports. A total of 1340 LCBSI
reports that were maintained in the records section from 2013 till 2018 were evaluated over a duration of 4-5
months. The data of organisms collected were distributed by year of isolation, demography, location of the
patient, and the antimicrobial susceptibility results. To avoid repetitive sampling error from a patient having
>1 similar isolates (14 days apart) only the first isolate was included. If a patient had 2 BSI occurring 30
days after the first isolation, each BSI was considered as a new infection.[2] Blood reports that did not
conform to the definition criteria of the study were excluded.

Definitions:
Laboratory confirmed BSI (LCBSI) are based upon the following criteria of Primary and Secondary BSI.
[7,8] Primary BSI is defined as a positive culture of one or more recognised pathogen from blood which is
not related to an infection at another site. LCBSI of commensal organism (diphtheroids, coagulase negative
Staphylococci, micrococci, viridans streptococci, aerococci, Propionibacterium species or Bacillus species
except B.anthracis) were from isolation of 2 blood specimen collected on separate occasions (same day or
consecutive days) with at least one of the following signs and symptoms: fever (>38C), chills and
hypotension (<90 mm Hg) in patients >1 year of age; fever (>38C), hypothermia (<36C), apnoea or
bradycardia in patients 1 year. Secondary BSI are those BSI determined to another site of infection
correlated with the definitions of site-specific infections. [8] A secondary BSI determination was done based
upon the guidelines and case-scenario provided by NHSN.[1,2,4] Polymicrobial growth was defined as
isolation of >1 clinically important organism from a single blood culture or from different blood culture
collected within 48 hours. [11]
Organism identification and antibiotic susceptibility tests (AST):
Processing of blood samples for culture and sensitivity was done in the Department of Microbiology.
Aseptically collected paired peripheral venepuncture blood samples were directly inoculated in a BacT/Alert
FA Plus and PF Plus bottles for adults and paediatric patients, respectively, and incubated in a BacT/Alert
systems (bioMérieux, Durham, NC) for a period of 7 days before declaring it sterile. Positive BacT/Alert
blood samples were then cultured in blood agar and MacConkey agar. Furthermore, isolated organism
identification and AST were done in Vitek 2 systems (bioMérieux, Durham, NC) using Vitek 2 identification
and AST cards for gram positive and gram negative organisms accordingly, in accordance to interpretive
MIC breakpoints as described by CLSI. [13]
Multidrug resistance index (MDRI):
Calculated as per the formula described by Krumperman: a/(b X c), where ‘a’ is the aggregate antibiotic
resistance of all isolates from blood, ‘b’ is the number of antibiotics used and ‘c’ is the number of isolates
from blood. [12] MDRI of <0.2 and >0.2 is taken as an indicator to differentiate between low and high-risk
source of resistance, respectively. Organisms such as A.baumannii complex, P.aeruginosa, Klebsiella
species and Enterococcus species have innate resistance to certain antibiotics.[13] These intrinsically
resistant antibiotics were excluded from the index calculation.
Statistical analysis:
Continuous variables are expressed as mean (standard deviation) and categorical data expressed as
frequencies and percentages; also compared using Chi-squared test and the risk ratio with 95% confidence
interval calculated using a 2X2 contingency tables. All significant P level <0.05 and two-tailed tests were
considered. Statistical analysis was done using IBM Corp. SPSS statistics for Windows, version 20.0
(Armonk, NY, USA) and GraphPad software (San Diego, CA, USA).
Results
Over a duration of 6 years, 13091 blood cultures was performed in the department of Microbiology. As per
the criteria of primary and secondary LCBSI diagnosis, a total of 1340 positive BSI were reported; 1301
(97.1%) isolates were of bacterial and 39 (2.9%) isolates were of fungal origin [Figure 1].
[Table 1] shows the distribution of BSI based upon the year, location and type of isolates. Patients <1 year
constituted 20.8% (n=279) of total positive samples, whereas 79.2% (n=1061) were of mean age 43.7 ± 21.5
(SD) years
[Table 2]. Male to female ratio was 1.09. Secondary BSI were seen associated with 188 (14.02%) isolates,
with similar organisms being isolated from samples of the respiratory tract (122, 64.8%), followed by urine
(36, 19.1%) and pus (30, 15.6%).
Significant polymicrobial bacterial growth constituted in 1.6% (21/1340) of LCBSI organisms. The
number of bacterial positive blood culture by gram positive organisms were 518 (39.8%) and 783 (60.2%)
by gram negative organisms. [Figure 1] represents the year-wise percentage distribution of BSI isolates.
[Table 3] represents the rank-wise distribution of commonly isolated organism in our study.
Most common isolates among the gram-positive bacteria were CoNS (coagulase-negative
Staphylococci; 383, 73.9%), followed by Staphylococcus aureus (97, 18.7%), Enterococcus species (30,
5.7%) and Streptococcus species (8, 1.5% [S.pyogenes 2, S.agalactiae 3, S.pneumoniae, S.anginosus and
Aerococcus species 1 each]).
Most common isolates among the gram-negative bacteria were Escherichia coli (257, 32.8%),
followed by Klebsiella species (175, 22.3%), Salmonella species (122, 15.2%), Acinetobacter species (54,
6.9%), Pseudomonas species (48, 6.1%), Burkholderia cepacia (32, 4.1%), Enterobacter species (26, 3.3%)
and Serratia species (15, 1.9%). Other less frequently isolated organisms were Sphingomonas species (8,
1.02%), Proteus species (8, 1.02%), Citrobacter species (7, 0.9%), Aeromonas species (5, 0.6%),
Achromobacter species (4, 0.5%), Morganella species (4, 0.5%), Cronobacter sakazakii (3, 0.4%) and one
(0.1%) isolate each of Elizabethkinga species, Chrysobacterium species, Shigella species and Alkaligenes
faecalis.
Fungi which accounted for 2.9% (39 isolates) of positive cultures were all caused by yeast-like
organisms, of which Candida albicans accounted for 28.1% of isolates, followed by Candida tropicalis
(25%). Candida species were commonly isolated from the ICU patients (82.1%). The mean age was 41.9 ±
23.7 (SD) years with male to female ratio of 1.05. Neonates contributed to 43.6% of total fungal BSI.
From the ICU’s, Klebsiella species were the commonly isolated organism, whereas CoNS were most
commonly isolated in the wards [Table 3]. On evaluation of organisms likelihood to be isolated from
patients in the ICUs versus the wards, Klebsiella species (Odds Ratio [95% Confidence Interval]; 6.5 [4.6 -
9.2], P <0.0001), Enterobacter species (6.0 [2.5 - 14.3], P <0.0001), Enterococcus species (2.5 [1.2 - 5.1], P
= 0.02), Acinetobacter species (1.9 [1.1 - 3.3], P=0.03) and Pseudomonas species (2.0 [1.1-3.6], P=0.02)
were commonly isolated in the ICU’s, whereas, CoNS, S.aureus, E.coli and Salmonella species were more
likely to be isolated in patients from the wards.
Table 4 represents the antibiotic susceptibility of the commonly isolated gram-negative organisms.
More than 50% resistance were displayed by E.coli to cefuroxime, ampicillin, nalidixic acid, ciprofloxacin,
co-trimoxazole, ceftriaxone, and cefepime. Klebsiella species displayed >50% of resistance to ampicillin,
cefuroxime, cefepime, ceftriaxone, gentamicin and co-trimoxazole. Acinetobacter species displayed >50%
resistance to almost all antibiotics tested except cefoperazone-sulbactam, tigecycline, carbapenems and
colistin.
For gram-positive organism maximum resistance were observed for benzylpenicillin, erythromycin
and ciprofloxacin [Table 5]. Percentage of vancomycin-resistance was low among Staphylococcus spp. than
Enterococci. Vancomycin resistance among Enterococcus species was 30%, highest in E.faecalis (50%),
followed by E.faecium (25%), E.casseliflavus and E.gallinarum isolates. High-level gentamicin resistance of
43.3% were found highest in E.faecium than in E.faecalis isolates.
On evaluation of MDRI of commonly isolated organism for a duration of 6-years, it is evident that
there is a significant increase in resistance pattern of all isolates particularly A.baumannii complex,
P.aeruginosa and S.aureus [Figure 2]. A.baumannii complex and P.aeruginosa were the isolates with the
highest number of multidrug resistance throughout the duration of study period.
Discussions
This study was undertaken to know the prevalence of organism isolated from BSI, the antibiotic sensitivity
profile and the evolution of AMR over a period of six years. Majority of pathogens in our study were
bacterial in origin and monomicrobial growth was recorded in 98.4% of LCBSI. Pathogens were most
frequently isolated from the younger population ( 20 years); the age group of  1 year contributing to the
maximum cases of BSI in our study (17.6%).
Similar to several studies, gram-negative bacilli were the most common isolates in our study.[10,14-
16] Incidentally, gram-positive cocci were the commonly isolated organisms at the beginning of our study in
2013 (70.8%), with CoNS as the most commonly isolated group. However, by 2014 onwards upward trend
of gram-negative bacilli isolation became regular due to a decrease in the frequency of CoNS isolation.
Overall, a gradual decline in isolation of both types of organisms, with gram-positive cocci more so, could
perhaps be attributed to a better understanding of sample collection, infection control and prevention.
[3,11,sentry]
In our study, methicillin resistance was seen in 57.9% of S.aureus and 44.3% of CoNS isolates. A rise
in multiple antibiotic resistance of S.aureus is of concern as the organism in the beginning of the study had
MDRI of <0.2 and by 2018, S.aureus isolates were largely resistant to all first-line antibiotics. Overall, low
numbers of gram-positive cocci were vancomycin resistant in our study but resistance to penicillin,
fluoroquinolones and erythromycin were seen in majority of isolates. [11,15]
The overall resistance among gram-negative isolates was observed highest to -lactams,
trimethoprim-sulfamethoxazole and quinolone antibiotics. Whereas, relatively good sensitivity was observed
for cefoperazone-sulbactam, tigecycline, carbapenems and colistin.[17] The high percentages of resistance
of gram-negative isolates to frequently used antibiotics such as third-generation cephalosporin (ceftriaxone),
fluoroquinolones and aminoglycosides is similar to a study by Djuric et al. The index of multidrug
resistance in commonly isolated bacterial organisms was alarmingly high and remained consistently high
throughout the study period. The types of organisms and the resistance pattern is similar to many studies
conducted elsewhere in the world indicating a predictable rise of MDR organisms in the future. [3,6,15]
Carbapenem resistance in our study was the highest for Acinetobacter spp. (40.7%), which have been duly
reported in other findings. [3,6,17,18] Carbapenem resistance >20% were seen in Pseudomonas spp. and
Burkholderia spp. Resistance was seen least in Enterobacteriaceae contrary to studies done by Datta et al.
[19] Nevertheless, close monitoring and improvement of infection control practices should be implemented
to avoid the emergence of carbapenem-resistant Enterobacteriaceae (CRE).[6] Colistin is the drug of choice
in treating CRE and in our study it is the only antibiotic all the gram-negative isolates were largely sensitive
to. However, Vitek 2 GN-AST cards use agar dilution method and according to the CLSI-EUCAST 2018
guidelines, broth microdilution is the only acceptable method for detection of colistin resistance. [17]
Consequently, the importance of the few resistant isolates remains uncertain.
In our study, E.coli is the most common isolate which is also reported as the most common cause of
BSI in Europe and in the SENTRY surveillance. [6,15,sentry] Though the MDRI of E.coli and Klebsiella
spp. remained fairly constant it was consistently high throughout the duration of study.
Acinetobacter baumannii complex during 2013 were the organisms with the second highest MDRI
and by the end of 2018 were the organisms with the highest MDRI. Acinetobacter spp. displayed resistance
to mostly all the antibiotics tested, except tigecycline and colistin, which is also reported in other studies
[15,17] Similarly, surveillance studies of antimicrobials in Europe have revealed that among Acinetobacter
spp. there is an alarmingly high level of AMR to routinely used antibiotic groups of fluoroquinolones,
aminoglycosides and carbapenems. [6,15]
In this study, the isolation rate of Pseudomonas spp. is relatively less (3.6%) but its resistance to many
antibiotics (excluding colistin) increased significantly over the 6-year duration. P.aeruginosa is an organism
responsible for the majority of healthcare-associated infections worldwide; intrinsic resistance and an
additional acquired resistance to several antibiotics is adding weight to a pre-existing burden.[6]
The current scenario of BSI in India is rather complex to quantify as regional variations abound and the
strategies adopted are more in tune with western standards rather than adopting a more indigenous protocol.
[16] The Centre for Disease Control and Prevention and the SCOPE (Surveillance and Control of Pathogens
of Epidemiological Importance) project in the United States of America monitor BSI via a nationwide
network of hospitals, similar to the SENTRY Antimicrobial Surveillance Program, the European
Antimicrobial Resistance Surveillance Network (EARS-Net), Central Asian and Eastern European
Surveillance of Antimicrobial Resistance (CAESAR) network and the Asian-Pacific Research Foundation
for Infectious Diseases (ARFID) of South Korea. [1,7,14,15,20] The SCOPE nationwide collective effort is
also adopted by Brazil. [10] Such surveillance programmes are the need of the hour in India as there is
inadequate national database and no repository of resistant pathogens that can streamline active surveillance
programs (to guide clinical decisions on use of antimicrobials). [21] Hopefully, the Antimicrobial Resistance
Surveillance and Research Network (AMRSN) and National Action Plan on Antimicrobial Resistance
(NAP-AMR) will provide some solutions in tackling the problem of emerging MDR pathogens collective
for the Indian sub-continent in the near future. [3,21]
Limitations
There were several limitations to this study. The major limitations was that the data collected were
dependent upon the medical records which was inconsistent with the exact timings of hospital admissions
due to which the BSI could not be classified as either hospital or community-acquired. Due to the
retrospective nature of our study, many isolates could not be assessed for molecular studies to evaluate the
genetic determination of AMR. Also, BSI caused by anaerobic organisms and fungal antibiotic sensitivity
testing is not done routinely in our hospital, therefore, the rate of anaerobic BSI and fungal antibiogram
remains unknown.
Conclusion
This study was undertaken to guide clinical decision and appropriate use of antibiotics in our hospital which
has never been done previously. To optimise treatment and control antimicrobial resistance among
pathogens interventions in the form of an active or passive surveillance is urgently required.
Conflict of interest: None to declare.
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23.

Table 1: Distribution of organisms causing blood stream infection (BSI) based upon the location of isolation from 2013 to 2018.

Location Total bacterial isolates (n = 1301) Total fungal isolates (n=39)

Gram positive isolates Gram negative isolates

(n=518) (n=783)
Medicine wards 305 (58.9) 397 (50.7) 6 (15.4)
Paediatric wards 44 (8.5) 22 (2.8) Not Recorded
Surgical wards 15 (2.9) 35 (4.5) Not Recorded
Private wards 15 (2.9) 22 (2.8) Not Recorded
Obstetrics 3 (0.6) 1 (0.1) Not Recorded
Orthopaedics 1 (0.2) Not Recorded Not Recorded
NICU and PICU 53 (10.2) 204 (26.1) 21 (53.8)
MICU and CCU 58 (11.2) 55 (7.0) 10 (25.6)
Surgical ICU 11 (2.1) 34 (4.3) 2 (5.1)
Dialysis 13 (2.5) 13 (1.7) Not Recorded
Figures in parentheses are in percentages.
NICU: Neonatal Intensive care unit; PICU: Paediatric Intensive care unit; MICU: Medical Intensive care unit; CCU: Cardiothoracic care
unit.

Table 2: Age and sex wise distribution of bacterial organism causing nosocomial blood stream infection (n=1340) f rom 2013 to 2018.

Total bacterial Gram positive Gram negative

isolates isolates isolates P
(n=1301) (n=518) (n=783)

IQR* 45 (58-13) 39 (58-19) 57 (58-1)

New born to 20 418 (32.1) 144 (27.8) 274 (34.9) 0.007*

Age in years 21 to 40 335 (25.7) 139 (26.8) 196 (25) 0.47

41 to 60 272 (20.9) 126 (24.3) 146 (18.6) 0.01*

>61 276 (21.2) 109 (21.04) 167 (21.3) 0.9

Table 2: Age and sex wise distribution of bacterial organism causing nosocomial blood stream infection (n=1340) f rom 2013 to 2018.

Male 679 (52.2) 277 (53.5) 402 (51.3)

Sex 0.45
Female 622 (47.8) 241 (46.5) 381 (48.7)
Figures in parentheses are in percentages.
*IQR: Interquartile range expressed in years; parentheses for upper and lower quartile.
Significant value (P ≤0.05)

Table 3: Common bacterial isolates in the ICU and the wards from 2013 to 2018.
Pathogens Total ICU Wards
(Rank-wise distribution) (n=1301) (n=415) (n=886)
Coagulase negative Staphylococci 383 85 298
Escherichia coli 257 45 212
Klebsiella species 175 122 53
Salmonella species 122 2 120
Staphylococcus aureus 97 19 78
Acinetobacter species 54 25 29
Pseudomonas species 48 23 25
Enterococcus species 30 16 14
Enterobacter species 26 19 7

Table 4: Antimicrobial resistance among gram negative organism (n=783) most frequently
isolated from bloodstream infection over a period of six years (2013-2018)
Pseudomon Enterobacte
Escherichia Klebsiella Salmonella Acinetobacter
as r
coli species species species
Antimicrobials species species
n = 257 n = 175 n = 122 n = 54
n = 48 n = 26
Ampicillin 196 (76.3) 167 (95.4) 12 (9.8) 49 (90.7) 42 (87.7) 19 (73.1)
Amoxycillin-Clavulanic 95 (36.9) 78 (44.6) 4 (3.3) 46 (85.2) 33 (68.6) 23 (88.5)
Piperacillin/Tazobactam 42 (16.3) 43 (24.6) 4 (3.3) 32 (59.3) 17 (35.4) 4 (15.4)
2nd gen Cephalosporin 192 (74.7) 148 (84.6) NR* 48 (88.9) 42 (87.7) 24 (92.3)
Ceftriaxone 171 (66.5) 138 (78.9) 10 (8.2) 43 (79.6) 34 (70.8) 18 (69.2)
Cefoperazone/sulbactam 32 (12.5) 37 (21.1) 2 (1.6) 23 (42.6) 20 (41.7) 5 (19.2)
Cefepime 157 (61.1) 141 (80.6) 9 (7.4) 39 (72.2) 24 (50) 10 (38.5)
Amikacin 14 (5.4) 30 (17.1) NR* 30 (55.6) 16 (33.3) 3 (11.5)
Gentamicin 81 (31.5) 91 (52) NR* 31 (57.4) 21 (43.8) 15 (57.7)
Nalidixic acid 180 (70) 70 (40) 103 (84.4) 32 (59.3) 34 (70.8) 8 (30.8)
Ciprofloxacin 148 (57.6) 52 (29.7) 33 (27) 28 (51.9) 26 (54.2) 4 (15.4)
Tigecycline 23 (8.9) 22 (12.6) 2 (1.6) 11 (20.4) 30 (62.5) 3 (11.5)
Carbapenem 12 (4.7) 17 (9.7) 2 (1.6) 22 (40.7) 14 (29.2) 4 (15.4)
Co-Trimoxazole 146 (56.8) 96 (54.8) 10 (8.2) 34 (62.9) 37 (77.1) 9 (34.6)
Colistin 16 (6.2) 9 (5.1) 5 (4.1) 10 (18.5) 4 (8.3) 3 (11.5)
Figures in parentheses are in percentages.
2nd generation cephalosporin includes Cefuroxime and Cefuroxime axetil.
Carbapenem includes Ertapenem, Imipenem and Meropenem.
Co- Trimoxazole: Trimethoprim-sulfamethoxazole
NR*: Not reported. According to CLSI, Salmonella spp. susceptibility to second generation cephalosporin and
aminoglycoside should not be reported as they may appear active in vitro but are ineffective clinically.

Table 5: Antimicrobial resistance among gram positive organism (n=518) most

frequently isolated from bloodstream infection over a period of six years (2013-2018)
Coagulase negative Staphylococcus
Enterococcus species
Antimicrobials Staphylococci aureus
n = 30
n = 383 n = 97
Benzylpenicillin 326 (85.1) 81 (83.5) 19 (63.3)
Oxacillin 222 (57.9) 43 (44.3) Not done
Ciprofloxacin 126 (32.9) 40 (41.2) 20 (66.7)
Levofloxacin 99 (25.8) 37 (38.1) 16 (53.3)
Gentamicin 46 (12.0) 12 (12.4) Not done
High-level gentamicin Not done Not done 13 (43.3)
Erythromycin 230 (60.1) 44 (45.4) 20 (66.7)
Clindamycin 130 (33.9) 27 (27.8) Not reported*
Tetracycline 39 (10.2) 5 (5.2) 11 (36.7)
Trimethoprim-sulfamethoxazole 135 (35.2) 43 (44.3) Not reported*
Vancomycin 7 (1.8) 6 (6.2) 5 (16.7)
Teicoplanin 14 (3.7) 5 (5.2) 4 (13.3)
Linezolid 9 (2.3) 0 0
Daptomycin 4 (1.0) 2 (2.1) 0
Figures in parentheses are in percentages.
*According to CLSI, Enterococcus spp. susceptibility to aminoglycoside, clindamycin and co-
trimoxazole should not be reported as they may appear active in vitro but are ineffective clinically.
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25.