Multi Drug Resistant Pathogens Causing Urinary Tract Infection in Children at Kathmandu Model Hospital

Abstract

Abstract

Introduction: Antibiotic resistance of urinary tract pathogens has increased globally. Updated knowledge of the antibiotic resistance patterns of uropathogens in the health institutes is important for the selection of an appropriate empirical antimicrobial therapy. The aim of this study was to evaluate the multi drug resistant urinary isolates in the children from 1 to15 years and evaluate the options for empiric antibiotic therapy.

Materials and Methods: The study was conducted from December 2011 to May 2012 in the Bacteriology laboratory, Kathmandu Model Hospital. Urine samples received in the laboratory were processed for routine, culture and its sensitivity. The antimicrobial susceptibility of bacterial isolates was determined following Clinical and Laboratory Standard Institute (CLSI) recommended Kirby-Bauer Disc Diffusion method.

Results: Of the total 372 urine samples received in the laboratory, 60 (16.13%) showed significant growth; of which 55.0 % (33/60) were MDR isolates. Escherichia coli were the predominant isolate from urine sample. Out of 49 Escherichia coli isolates, 27 (45.0%) were Multi drug resistant. Enterococcus faecalis (N=3) was the most predominant Gram positive isolate and 66.67 % (2/3) of this organism were multi drug resistant. Among the first line drugs used against gram negative isolates, nitrofurantoin was the most effective drug followed by quinolones, while among the second line drugs; meropenem was the most effective drug followed by chloramphenicol and amikacin, whereas; nitrofurantoin (100%) was the most effective drug for Gram positive isolates followed by norfloxacin and cefotaxime.

Conclusion: High percentages of multi drug resistant uropathogens were revealed in children. Nitrofurantoin was found to be the most effective drug for gram positive, gram negative and multi drug resistant isolates.

Full text

Original Article
<233>J. Nepal Paediatr. Soc.
Multi Drug Resistant Pathogens Causing Urinary Tract
Infections in Children at Kathmandu Model Hospital
Shrestha B1, Gurubacharya RL2, Maharjan B3, Shrestha S4
1Basudha Shrestha, MSc. Microbiology, Consultant Microbiologist, Department of Pathology, 2Dr. Rajesh Lal Gurubacharya,
MBBS, MD, Chief of Paediatric Services, Consultant Paediatrician, Department of Paediatric Medicine, 3Dr. Basanta
Maharjan, MPH, Community Health Development Program, 4Sanjit Shrestha, BMLT, Senior Laboratory Technologist,
Department of Pathology. All from Kathmandu Model Hospital, Kathmandu, Nepal.
Address for correspondence: Basudha Shrestha, E-mail: basudha111@hotmail.com
Abstract
Introduction: Antibiotic resistance of urinary tract pathogens has increased globally. Updated knowledge
of the antibiotic resistance patterns of uropathogens in the health institutes is important for the selection
of an appropriate empirical antimicrobial therapy. The aim of this study was to evaluate the multi drug
resistant urinary isolates in the children from 1 to15 years and evaluate the options for empiric antibiotic
therapy. Materials and Methods: The study was conducted from December 2011 to May 2012 in the
Bacteriology laboratory, Kathmandu Model Hospital. Urine samples received in the laboratory were
processed for routine, culture and its sensitivity. The antimicrobial susceptibility of bacterial isolates was
determined following Clinical and Laboratory Standard Institute (CLSI) recommended Kirby-Bauer Disc
Diffusion method. Results: Of the total 372 urine samples received in the laboratory, 60 (16.13%) showed
significant growth; of which 55.0 % (33/60) were MDR isolates. Escherichia coli were the predominant isolate
from urine sample. Out of 49 Escherichia coli isolates, 27 (45.0%) were Multi drug resistant. Enterococcus
faecalis (N=3) was the most predominant Gram positive isolate and 66.67 % (2/3) of this organism were
multi drug resistant. Among the first line drugs used against gram negative isolates, nitrofurantoin was
the most effective drug followed by quinolones, while among the second line drugs; meropenem was the
most effective drug followed by chloramphenicol and amikacin, whereas; nitrofurantoin (100%) was the
most effective drug for Gram positive isolates followed by norfloxacin and cefotaxime. Conclusion: High
percentages of multi drug resistant uropathogens were revealed in children. Nitrofurantoin was found to
be the most effective drug for gram positive, gram negative and multi drug resistant isolates.
Key words: Children, Multi drug resistance, Empirical antimicrobial therapy, Escherichia coli
Introduction
Urinary tract infection (UTI) is de ned as bac teriuria
along with urinary symptoms and is identi ed by
growth of a signi cant number of organisms of single
species in the urine. Urinary tract infections are common
medical problems in children and are important cause
of morbidity. UTI during childhood varies by age and
gender. UTI commonly a ects boys during the  rst year of
life1,but thereafter 3-5% of girls are a ec ted1, increasing
to 10% by the teenage years2. Although several di erent
microorganisms can cause UTI, including fungi and
viruses, bacteria are the major causative organisms and
responsible for more than 95% of UTI cases3. Treatment
of urinary tract infections is compromised worldwide by
the emergence of bacteria that are resistant to multiple
antibiotics4. Overuse and use of incomplete course of
antibiotics as well as empirical antimicrobial therapy has
been the major contributing factor in the development
of Multi Drug Resistant(MDR) bacteria5.
Multidrug resistance is de ned as resistance to
two or more di erent structural classes of antimicrobial
agents6. There is growing concern regarding the
resistance to uropathogens to antibiotics. The clinical
impact of drug resistance may be great or insigni cant,
depending on the level of resistance, the site of infection,
and the availability of e ective, nontoxic therapeutic
alternatives7. This prospective study was conducted to
identify UTI due to multidrug resistant uropathogens
among children and to evaluate empiric antibiotic
therapy.
September-December, 2012/Vol 32/Issue 3
doi: http://dx.doi.org/10.3126/jnps.v32i3.6771

<234> J. Nepal Paediatr. Soc.
Materials and Methods
This is the prospective study conducted at
Kathmandu Model Hospital on Pediatric patients (1-15
years) attending for the treatment of suspected UTI
case. Three hundred and seventy two urine samples
were examined from clinically suspected urinary tract
infection during the research period of six months
(December 2011- May 2012) using culture and sensitivity
tests. All the patient or parents of the patient were
instructed carefully for collection of morning mid-
stream urine specimens. They were given a sterile, dry
and clean collection bottles for urine collection. All the
urine specimens were processed within 30 minutes of
collection.
Culture of all urine specimens was done on 5%
Blood Agar and Mac Conkey Agar plate utilizing semi-
quantitative culture method (Fig 1). Shaking with hand
to ensure a uniform suspension of bacteria vigorously
mixed the urine specimens. Then, an inoculating loop of
standard dimension was used to take up approximately
 xed and known volume (0.001ml) of mixed urine and
placed on the center of the plate. The drop was spread in
a line and then over the entire surface of the agar plate.
After inoculation, the culture plates were incubated in
an inverted position at 37oC for 24 hours.8 After 24 hours,
the numbers of colonies were counted on each plate,
which was multiplied by 1000 to calculate the number
of organisms per ml in the specimen. Samples showing
105 or more organisms per ml of urine were taken as
signi cant. Colony counts less than this was considered
as non-signi cant8.
Gram’s staining and various biochemical tests
identi ed pure culture of bacterial growth. Di erent
biochemical media used were Triple Sugar Iron Agar,
Sulphite Indole motility Agar, Urease agar, Simmons’s
Citrate Agar, Methyl Red / Voges Proskauer Test and
Oxidation Fermentation medium. Catalase, Coagulase
and Oxidase Tests were also performed. The antibiotics
used as  rst line drugs for Gram negative bacteria were
Amoxycillin (10 mcg), Cefotaxime (30 mcg), Cipro oxacin
(5 mcg), Ce xime (5 mcg), Cotrimoxazole (1.25/23.75
mcg), Nor oxacin (10 mcg), Nitrofurantoin (300 mcg)
and O oxacin (5 mcg) and those used for Gram positive
bacteria were; Amoxycillin (10 mcg), Cefotaxime (30
mcg), Cipro oxacin (5 mcg), Nor oxacin (10 mcg),
Cotrimoxazole (1.25/23.75 mcg), Nitrofurantoin (300
mcg), Gentamicin (10 mcg) and Ceftriaxone (30
mcg). The antibiotics used as second line drugs were
Ceftriaxone (30 mcg), Ceftazidime (30 mcg), Gentamicin
(10 mcg), Amikacin (30 mcg), Chloramphenicol (30 mcg),
Piperacillin/Tazobactam (100/10 mcg), Cefoperazone/
Sulbactam (50/50 mcg) and Meropenem (10 mcg). All
the antibiotics were tested by Kirby Bauer’s Disc Di usion
Technique. The colonies picked up and suspended in
Nutrient broth and adjusted turbidity to 0.5 Mc Farland
standard.
Within 15 minutes, a sterilized cotton swab was
dipped into the adjusted suspension. Carpet culture was
done by streaking the swab over the entire sterile Mueller
Hinton agar plate (Fig 2). The antibiotic impregnated
discs were placed on the surface of the agar plate and
then incubated at 37oC for 18 hours9. The di erent
inhibition zones were measured and interpreted the
results on the basis of zone size compared with standard
interpretive table given by manufacturer. The organisms
which showed resistant to all  rst line antibiotics except
Nitrofurantoin were tested for second line drugs.
Fig 1: Signi cant Growth of E. coli in Mac Conkey Agar
Fig 2: Antibiotic Susceptibility Test of MDR E. coli in Mueller Hinton
Agar
Multi Drug Resistant Pathogens Causing Urinary Tract Infections in Children at Kathmandu Model Hospital

<235>J. Nepal Paediatr. Soc.
Results
Of the 372 urine samples processed, 60 (16.13%)
samples showed signi cant growth where as majority
of samples i.e. 284 (76.34%) showed no growth and 28
(7.53%) showed growth of no signi cance (Table 1).
Out of 372 patients, 192 (51.61%) were male, while
180 (48.39%) were female. Of the total samples, 350
(94.09%) were from outdoor patients, 7 (1.88%) were
from indoor patients and 15 samples (4.03%) were from
emergency Department. The age group of 1-5 years had
the maximum requests of 179 (48.12%) for urine culture,
while the age group 11-15 years was second with 102
(27.42%) requests. Age group of 6-10 years was the least
with 91 (24.46%) request.
The age and gender wise distribution of children
with UTI is shown in Table 2. UTI was commonly found
in young female children of age 1-5 years. MDR isolates
were common in young children (46.67%) of the 1-5
years age group. Children of age group 6-10 years
showed three (5.0%) and age group 11-15 years showed
only two (3.34%) MDR isolates. Of the total MDR isolates,
31.67 occurred in young female children of age 1-5 years.
UTI was signi cantly high in female children (p=0.004) in
comparison to male. There was no signi cant di erence
seen in MDR infection between male and female (p=0.8).
However, the signi cant di erence was seen in MDR
infection between age group 1 to 5 and above 5 year’s
group (p=0.0001)
Gram negative bacteria were predominant;
constituting 56 (93.33%) of the total 60 isolates
and 33(55.0%) were MDR. Among Gram negatives,
Escherichia coli were the most frequently isolated species
with 49 (81.67%). Gram positive organisms constituted
only 4 (6.67%) of total isolates, and 2 (3.33%) of them
were MDR. Both MDR isolates were Enterococcus faecalis
(Table 3).
Table 3: Pattern of microbial isolates
Organisms No. of Isolates
(%) MDR (%)
Gram Positive Bacteria
Staphylococcus
epidermidis
Enterococcus faecalis
1(1.67)
3(5.0) 2 (3.33)
TOTAL (Gram Positive) 4 (6.67) 2(3.33)
Gram Negative Bacteria
Escherichia coli
Citrobacter spp.
Enterobacter aerogenes
Enterobacter cloacae
Proteus vulgaris
Salmonella Paratyphi A
49 (81.67)
2 (3.33)
2(3.33)
1(1.67)
1(1.67)
1(1.67)
27(45.0)
1(1.67)
1(1.67)
1(1.67)
1(1.67)
0
TOTAL (Gram Negative) 56 (93.33) 33 (55.0)
Grand Total 60 (100)
Among the common antibiotics used as  rst
line against gram negative isolates, nitrofurantoin
showed a susceptibility of 55/56 (98.21%). Quinolones
(Cipro oxacin, Nor oxacin and O oxacin) followed
Nitrofurantoin with susceptibility of 38/56 (67.86%).
Among the second line antibiotics used, Meropenem
was found to be most e ective drug with susceptibility
of 16/17 (94.12%) followed by chloramphenicol and
Amikacin with a susceptibility of 15/17 (88.24%). Most of
the Gram negative isolates i.e. 45 (80.36%) were resistant
to Amoxycillin (Table 4, 5).
Among the gram positive isolates, Nitrofurantoin
was the most e ective drug with susceptibility of
4/4 (100%) which was followed by Cefotaxime and
Nor oxacin (Table 6).
Out of 60 isolates, 24 (40.0%) isolates were resistant
to >3 drugs where as only 3 isolates of Escherichia coli
and one isolate of Salmonella Paratyphi were sensitive
to all antibiotics used. Among 56 gram negative isolates,
31(51.67%) isolates were MDR whereas of the 4 gram
positive isolates, 2 (50.0%) isolates were MDR (Table 7).
Table 1: Growth pro le of urine sample
Specimen Total no.
of samples
Signi cant Growth No Signi cant Growth No Growth
No. % No. % No. %
Urine 372 60 16.13 28 7.53 284 76.34
Table 2: Age and gender wise distribution of infected patients with MDR isolates
Age Group (yrs)
Growth with MDR isolates
Total MDR (%)Male Female
Isolates (%) MDR (%) Isolates (%) MDR (%)
1-5 14 (23.33) 9 (15.0) 24 (40.0) 19 (31.67) 28 (46.67)
6-10 2 (3.33) 0 9(15.0) 3 (5.0) 3 (5.0)
11-15 3 (5.0) 1 (1.67) 8 (13.33) 1 (1.67) 2 (3.34)
Total 19 (31.67) 10 (16.67) 41 (68.33) 23 (38.33) 33 (55.0)
Shrestha B et al

<236> J. Nepal Paediatr. Soc.
Table 4: Antibiotic Susceptibility Pattern of Gram-negative Isolates towards  rst line antibiotics
Antibiotic used Susceptible Intermediate Resistant Total
Frequency % Frequency % Frequency %
Amoxycillin 9 16.07 2 3.57 45 80.36 56
Cefotaxime 26 46.43 2 3.57 28 50.0 56
Cipro oxacin 38 67.86 2 3.57 16 28.57 56
Cotrimoxazole 28 50.0 1 1.79 27 48.21 56
Ce xime 33 58.93 1 1.79 22 39.28 56
Nitrofurantoin 55 98.21 0 0 1 1.79 56
Nor oxacin 38 67.86 2 3.57 16 28.57 56
O oxacin 38 67.86 1 1.79 17 30.35 56
Table 5: Antibiotic Susceptibility Pattern of gram negative isolates towards second line antibiotics
Antibiotic used Susceptible Intermediate Resistant Total
Frequency % Frequency % Frequency %
Amikacin 15 88.24 0 0.00 2 11.76 17
Gentamicin 10 58.82 0 0.00 7 41.18 17
Chloramphenicol 15 88.24 0 0.00 2 11.76 17
Ceftriaxone 1 5.88 0 0.00 16 94.12 17
Ceftazidime 1 5.88 1 5.88 15 88.24 17
Cefoperazone/Sulbactam 11 64.71 2 11.77 4 23.52 17
Piperacillin/Tazobactam 13 76.47 1 5.88 3 17.65 17
Meropenem 16 94.12 0 0.00 1 5.88 17
Table 6: Antibiotic Susceptibility Pattern of Gram-positive Isolates
Antibiotic used Susceptible Intermediate Resistant Total
Frequency % Frequency % Frequency %
Amoxycillin 2 50.0 0 0 2 50.0 4
Cipro oxacin 2 50.0 1 25.0 1 25.0 4
Cotrimoxazole 2 50.0 0 0 2 50.0 4
Cefotaxime 3 75.0 0 0 1 25.0 4
Nor oxacin 3 75.0 0 0 1 25.0 4
Nitrofurantoin 4 100.0 0 0 0 0 4
Gentamicin 2 50.0 0 0 2 50.0 4
Ceftriaxone 2 50.0 0 0 2 50.0 4
Table 7: Status of antibiotic resistance among MDR isolates
Organism Total
Isolates
Resistance to
0
Drug
1
Drug
2
Drugs
MDR isolates
2 Drugs
(di erent classes)
3
Drugs
> 3
Drugs Total %
Escherichia coli 49 3 18 7 7 0 20 27 45.0
Citrobacter spp 2 0 1 0 0 0 1 1 1.67
Ent. aerogenes 2 0 1 0 0 0 1 1 1.67
Ent. Cloacae 1 0 0 1 1 0 0 1 1.67
Proteus vulgaris 1 0 0 1 1 0 0 1 1.67
Salmonella Paratyphi 1 1 0 0 0 0 0 0 0
Staph. epidermidis 1 0 1 0 0 0 0 0 1.67
E. faecalis 3 0 0 0 0 0 2 2 3.33
Total 60 4 21 9 9 0 24 33 55.04
Multi Drug Resistant Pathogens Causing Urinary Tract Infections in Children at Kathmandu Model Hospital

<237>J. Nepal Paediatr. Soc.
Discussion
The emergence of multi drug resistance in
uropathogens is of great public health concern.
Prevalence of these organisms varies according to
species, antibiotic use and geographical area. The
increasing prevalence of infections caused by antibiotic
resistant bacteria makes the empirical treatment of UTIs
di cult. In the current study, we isolated 60 (16.13%)
uropathogens among 372 urine culture samples. The
study demonstrates that E. coli (81.67%) remains the
leading uropathogen responsible for UTIs which was
supported by several previous studies.10,11 The frequency
of UTI is greater in female children as compared to
male10,11,12 and our results were similar to these reports
showing 68.33% of patients were female.
Paediatric UTI causing bacteria are becoming
increasingly resistant to commonly used antibiotics such
as  uroquinolones and third generation cephalosporins.
Cotrimoxazole (Trimethoprim-sulphamethoxazole),
 uroquinolones, or nitrofurantoin are recommended
for empirical treatment of uncomplicated UTI13,14.
However, several reports from worldwide indicated the
excessive increase in the emergence of trimethoprim-
sulphamethoxazole resistant E. coli15,16. Cotrimoxazole
was replaced by  uroquinolones and cephalosporins
because of high level of resistance to this drug but
unfortunately after sometime resistance to these drugs
was also detected and published. Our study also showed
the similar  ndings with 28.5-30.35% resistance to
quinolones, 39.2-50.0% resistance to cephalosporins
and 48.21% resistance to cotrimoxazole for gram
negative isolates17. The results showed a considerable
increase in resistivity of gram negative isolates to
amoxycillin (80.36%) which was supported by several
studies11,12,18. Nitrofurantoin demonstrated better
activity against gram negative (98.21% susceptible) as
well as gram positive isolates (100.0% susceptible), in
agreement with data published by others17,18,19. The high
level susceptibility of uropathogens to nitrofurantoin
may be the narrow spectrum of activity, narrow tissue
distribution (low or undetectable serum concentration)
and limited contact with bacteria outside the urinary
tract20. According to our study, the  rst line antibiotics to
be used for the treatment of UTI is nitrofurantoin.
In our study, we de ned those organisms as MDR
which were resistant to two or more di erent structural
classes of antibiotics6. According to this, 33 (55.0%)
MDR isolates were detected. Of the 33 MDR isolates,
27(45.0%) were E. coli. This result was supported by
previous other studies21,22,23. Our study demonstrated
the highest resistance to Ceftriaxone (94.12%) among
17 MDR isolates. This may be due to the production of
ESBL enzymes or other resistance mechanisms which
could not be addressed because of limited resources.
The resistance to cephalosporin is explained though the
enzymatic mechanisms and e ux pumps24. It has been
reported that pathogenic E. coli isolates have relatively
high potential for developing resistance.25 Among the
antibiotics used in the second line, meropenem was the
most active drug with susceptibility of 94.12% followed
by amikacin and chloramphenicol with susceptibility
of 88.24%. These  ndings reveals stronger propensity
of uropathogens towards multiple drugs resistance
limiting few therapeutic options for the treatment.
Conclusion
The results of the present study suggest that
prevalence of MDR E. coli is alarmingly high and the most
appropriate  rst line oral antibiotic for empiric treatment
of uri nary tract infection at our hospital is nitrofu rantoin
and meropenem, amikacin and chloramphenicol as
second line agents. Antibacterial resistance patterns
need to be up dated periodically to ensure proper
empiric treatment of UTI.
Acknowledgements: None
Funding: None
Con ict of Interest: None
Permission of IRB: Yes
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Multi Drug Resistant Pathogens Causing Urinary Tract Infections in Children at Kathmandu Model Hospital
How to cite this article ?
Shrestha B, Gurubacharya RL, Maharjan B, Shrestha S. Multi Drug Resistant Pathogens Causing Urinary Tract Infections in
Children at Kathmandu Model Hospital. J Nepal Paediatr Soc 2012;32(3):233-238.