Antibiotic Resistance in Urinary Tract Bacteria in Ouagadougou
Simplice D. Karou,
Denise P. Ilboudo,
Wendyame M.C. Nadembega,
Alfred S. Traore,
Comlan de Souza
The present study aimed to ascertain for the current situation of antimicrobial resistance of major urinary tract bacteria in Saint Camille Medical Centre. During two consecutive years, 794 urine specimens were analyzed for microorganism isolation and identification. The microorganisms were identified by conventional methods used in the centre and antimicrobial assays were performed by the NCCLS agar disk diffusion. Pathogenic microorganisms isolation was attempted for 89.04% samples. Escherichia coli (32.76%) was the most frequently isolated microorganism followed by Staphylococcus aureus (22.74%) and Klebsiella pneumoniae (10.45%). The antimicrobial screenings revealed very high antimicrobial resistance, to β-lactams. The resistance rates recorded with E. coli were 76.64, 74.01, 25 and 74.34% for ampicillin, amoxicillin amoxicillin/clavulanic acid and trimethoprime-sulfamethoxazole, respectively. Microorganisms were still susceptible to quinolones however, attention should be paid, because, the resistance rate already reached 10% for nalidixic acid and ciprofloxacin. Periodic performance of prevalence studies is a useful tool to know the current situation of microorganisms and their resistance patterns in an institution and it helps to access the emergence and the spread of antibiotic resistance.
to cite this article:
Simplice D. Karou, Denise P. Ilboudo, Wendyame M.C. Nadembega, Yaovi Ameyapoh, Djeneba Ouermi, Salvatore Pignatelli, Virginio Pietra, Alfred S. Traore, Comlan de Souza and Jacques Simpore, 2009. Antibiotic Resistance in Urinary Tract Bacteria in Ouagadougou. Pakistan Journal of Biological Sciences, 12: 712-716.
Urinary Tract Infection (UTI) is a problem that is frequently encountered by
health care providers. Over recent decades, the importance of UTI has been increasingly
recognized, in particular, the role of UTI as an occult cause of febrile illness
in infants. UTI is defined by the presence of organisms in the urinary tract,
which is usually sterile (Gérôme et al.,
2009). However, since asymptomatic colonization of the urinary tract can
occur, other features such as the presence of inflammatory markers or follow-up
cultures may be needed to definitively diagnose a UTI (Rubin
et al., 1992). Clinically important infections usually occur due
to bacteria, although viruses, fungi and parasites can also cause infections.
Common nonbacterial causes of UTI include hemorrhagic cystitis from Adenovirus
and Candida infections in immunocompromised individuals. Common bacterial
pathogens include gram-negative species such as E. coli, Klebsiella,
Proteus, Enterobacter, Pseudomonas and Serratia and
gram-positive organisms, including group B Streptococci, Enterococcus
and S. aureus (Zorc et al., 2005a).
The epidemiology of UTI during childhood varies by age, gender and other factors.
The incidence of UTI is highest in the first year of life for all children but
decreases substantially among boys after infancy (Jakobsson
et al., 1999). Estimates of UTI incidence among infant boys have
varied in different populations, likely due to factors such as circumcision,
which has been associated with a reduction in risk of UTI. The clinical significance
of UTI has been controversial (Foxman, 2007). In the
preantibiotic era, UTI had a mortality rate as high as 20% although, acute complications
in healthy children are now uncommon except in young infants, who may progress
to systemic infection. Long-term complications of UTI have been associated with
renal scarring and include hypertension, chronic renal failure and toxaemia
in pregnancy. Long-term follow-up data are limited, however, it has been reported
that children diagnosed with renal scarring due to pyelonephritis during the
1950s and 1960s developed high rates of hypertension and end-stage renal disease.
More recent studies questioned the association between pyelonephritis and end-stage
renal disease (Grünberg, 1998).
Although, the individual risks associated with UTI remain unclear, the high
prevalence of UTI and potential morbidity associated with complications require
careful attention to diagnosis and management. The appropriate treatment of
UTI has been relied on antibiotic use. The choice of antibiotic may be affected
by local resistance patterns and other considerations. Amoxicillin was traditionally
the first-line therapy for outpatient treatment of UTI (Wagenlehner
and Naber, 2006). However, increased rates of E. coli resistance
have made amoxicillin a less acceptable choice and studies have found higher
cure rates for trimethoprim-sulfamethoxazole (Fritsche et
al., 2009; Borsari et al., 2008; Zorc
et al., 2005b). The present study was conducted to evaluate the prevalence
of the microorganisms frequently involved in UTI and to access for the antimicrobial
resistance patterns of the most commonly implicated bacteria.
MATERIALS AND METHODS
Microorganism isolation and identification: From January 2006 to December 2007, a total of 794 urine specimens were collected from patients attending Saint Camille Medical Centre in Ouagadougou with urinary tract infection suspicion. Samples were cultured in appropriated media according to the conventional methods used in the centre. Yeast were isolated from sabouraud agar. Chapman medium was used for selective isolation of staphylococci. The other gram-positive cocci were isolated from blood agar and gram-negative bacilli specially Escherichia coli from Eosin Methylene Blue (EMB) agar. Microorganisms numeration was performed on with Cystine Lactose Electrolyte Deficient (CLED) medium. They were identified according to their colonies and their morphological characteristics. Identities were confirmed by API 20 system (Bio Merieux, France).
Antimicrobial assay: The antimicrobial screenings were performed using
Muller Hinton (MH) agar disk diffusion assay as recommended by the National
Committee for Clinical Laboratory Standards (NCCLS, 2003). Briefly, microorganisms
from growth on nutrient agar incubated at 37°C for 18 h were suspended in
saline solution 0.85% NaCl and adjusted to a turbidity of 0.5 Mac Farland standards
(108 cfu mL-1). The suspension was used to inoculate 90
mm diameter petri plates with a sterile non toxic cotton swab on a wooden applicator.
The antibiotic discs were directly placed onto the bacterial culture. After
24 h incubation in air at 37°C, antimicrobial activities were assayed by
measuring the inhibition zone diameter around the disk using a calliper. Antibiotic
break points were determined according to NCCLS guidelines. Escherichia coli
CIP 105182, S. aureus ATCC 25923 and S. aureus CIP 53154 were
used as control. All antibiotics and media were purchased from Bio Rad (France).
The following antibiotics were tested: ampicillin, amoxicillin, amoxicillin/clavulanic
acid, oxacillin, cefazolin, cefotaxim, oleandomycin, pristinamycin, erythromycin,
lincomycin, nalidixic acid, norfloxacin, ciprofloxacin, gentamicin, trimethoprime-sulfamethoxazole
The present study covered 2 consecutive years. During this period time, a total of 794 urine specimens were collected from patients with UTI suspicion. Pathogenic microorganisms isolation was attempted for 89.04% (707/794) samples. Cultivation of the other samples did not yield pathogens. Positive sample cultivation allowed us to isolate 928 microorganisms, indeed some samples showed dual or trial infections. Among the isolated microorganisms, 9.81% (91/928) were Candida species and 90.19% (883/928) were bacteria. Table 1 displays microorganism distribution. Overall microorganisms, E. coli (32.76%) was the most frequently isolated followed by S. aureus (22.74%) and K. pneumoniae (10.45%).
The most common microorganisms were tested for their susceptibilities to several
antimicrobial used in the centre. Table 2 shows the resistance
rates of gram positive cocci. According to the Table 2, S.
aureus has developed high resistance (resistance rate >10%) to the main
β-lactams (ampicillin, amoxicillin and amoxicillin/clavulanic acid) including
cephalosporin (cefazolin and cefotaxim). The highest rates were recorded with
ampicillin and amoxicillin (45.02 and 22.27%, respectively).
|| Isolated microorganisms distribution
|| Resistance rates of the isolated gram-positive cocci
|AMC: Amoxicillin/clavulanic acid, GDS: Group D Streptococcus
|| Antimicrobial resistance rates of the gram-negative bacilli
|AMC: Amoxicillin/clavulanic acid, SXT: Trimethoprim-sulfamethoxazole
Group D Streptococcus (GDS) remained susceptible to ampicillin, amoxicillin
and amoxicillin/clavulanic acid (resistance rate <10%), but it has developed
high resistance to oxacillin and cephalosporin (20.83, 20.83 and 14.58% for
oxacillin, cefazolin and cefotaxim, respectively). The two microorganisms have
developed high resistance to macrolides (oleandomycin, pristinamicin, erythromycin
and lincomycin). Resistance rates of 24.64 and 22.75% were recorded for oleandomycin
and lincomycin in S. aureus; 25 and 47.92% were recorded for these same
antibiotics in GDS. Finally, S. aureus was still susceptible to gentamicin
while there was an increasing resistance to this antibiotic in GDS (6.64% vs.
Four gram-negative bacteria, E. coli, K. pneumoniae, E. cloacae
and Acinetobacter sp. were tested for there susceptibility to the
antibiotics. According to Table 3, resistance to β-lactams (ampicillin,
amoxicillin and amoxicillin/clavulanic acid) is common within these gram negative
bacilli. The highest resistance rates were recorded with E. coli (76.64
and 71.01%) and K. pneumoniae (85.57 and 76.29%) for ampicillin and amoxicillin,
respectively. Resistance to trimethoprim-sulfamethoxazole was also common among
these microorganisms, the rates were greater than 25%, the highest rate (74.34%)
being recorded with E. coli. For chloramphenicol, the resistance rates
were greater than 15% and the highest rates were recorded with E. cloacae
and Acinetobacter sp. (34.15 and 34.07%, respectively). Excepted
E. coli which displayed resistance rates of 10.86 and 11.51% for ciprofloxacin
and nalidixic acid respectively, all these gram-negative bacteria were globally
susceptible to quinolones (norfloxacin, nalidixic acid and ciprofloxacin) to
cefazolin, pristinamycin and gentamicin.
The present study was undertaken to evaluate the prevalence of microorganisms implicated in UTI and to ascertain for their antimicrobial resistance patterns. During two consecutive years study, 794 urine samples were analyzed and 928 microorganisms were identified and isolated.
According to these results, E. coli (32.76%) was the leading agent responsible
for the UTI, followed by S. aureus (22.74%) and K. pneumoniae
(10.45%). These observations are supported by several studies conducted previously.
In a prospective study in Benin, a border country from 534 samples, Anagounou
et al. (1995) isolated E. coli in 36% cases. In another study
conducted on UTI in a geatric hospital, Haber et al.
(2007) found E. coli and Proteus mirabilis to be the main
bacterial species involved in 57 and 14%, respectively. A study conducted in
France, revealed that E. coli was the most prevalent pathogen followed
by P. mirabilis, Klebsiella sp., S. aureus, Staphylococcus
saprophyticus and Streptococcus agalactiae (De
Mouy et al., 2007). Similar observations were made in Tunis by Larabi
et al. (2003), who found that Enterobacteriaceae were the most frequently
identified strains including E. coli, while gram-positive strains were
often S. saprophyticus. However, it should be noted that there was a
high prevalence of S. aureus in the samples in comparison with the prevalence
recorded in these earlier studies.
In order to elucidate the current situation of antimicrobial resistance in
the centre the antimicrobial tests were performed for the most common isolated.
The results revealed that the problem of antimicrobial resistance is effective
in the centre. Antimicrobial resistance is a direct consequence of antimicrobial
use. Both continue to escalate despite many calls for moderation of antibiotic
use in hospitals and in community. Many surveillance studies have demonstrated
an increase in antimicrobial resistance in S. aureus, although they are
based on limited number of referral institutions per country (Fluit
et al., 2001). Similarly, uniformly high levels of methicillin resistance
and resistance to other antibiotics have been observed among S. aureus
isolates. This situation underlines the need for surveillance studies in different
geographical areas including all types of institutions. According to present
results, the resistance rates in S. aureus are less than what was observed
in Spain by Cuevas et al. (2004). In their study
the resistance rates were 31.2, 31.7 and 16.9% for oxacillin, erythromycin and
gentamicin, respectively. However, we must consider that our centre is in high
methicillin resistance area (oxacillin resistance rate >10%). The frequency
of Methicillin Resistant Staphylococcus aureus (MRSA) varies among countries
and hospital to hospital within each country. For example, in Europe MRSA are
rare in Nordic countries (<1%), but it is more frequent in Southern Europe
even exceeding 40% in France (Ferrara, 2007).
Three Enterobacteria (E. coli, K. pneumoniae and E. cloacae)
and Acinetobacter sp. were tested in the present study. The results revealed
that both Acinetobacter and the Enterobacteria have developed resistance
to many antibiotics principally β-lactams. Acinetobacter species
are opportunistic pathogens of low virulence. However, their contribution to
nosocomial infection has been increasing over the past 30 years. Though widely
prevalent in nature and generally regarded as commensals of human skin and respiratory
and genitourinary tracts, they have been implicated as the cause of serious
infectious diseases such as meningitis, pneumonia, tracheobronchitis, endocarditis,
wound infections, septicaemia and UTI, mostly involving patients with impaired
host defenses. We should note that in the present study Acinetobacter
is the fourth microorganism implicated in UTI with a prevalence of 9.81%. Treatment
of serious infections due to Acinetobacter sp. is complicated by the
widespread multidrug resistance of the organism. Over the last 15 years, interest
in Acinetobacter species has grown rapidly, due to the emergence and
outbreak of multidrug-resistant Acinetobacter isolates. They are intrinsically
resistant to many antimicrobial agents and resistance to β-lactams is most
commonly associated with the production of high levels of naturally produced
cephalosporinase (Yong et al., 2003).
In the present study the resistance rate of enterobacteria to ampicillin and
amoxicillin were globally greater than 50%. The same findings were reported
by several studies. Working on microorganisms isolated from UTI, Haber
et al. (2007) found that E. coli strains were 59% resistant
to amoxicillin, 55% resistant to amoxicillin-clavulanic acid and 39% resistant
to fluoroquinolones. In a similar study of Larabi et
al. (2003) found resistance rates of 57.9% to β-lactams and 46.9%
to trimethoprim-sulfamethoxazole in E. coli, 13.8% K. pneumoniae
were found to produce extended spectrum bêtalactamase.
By the end of 1990s the increasing resistance to antibiotics such as β-lactams
in the country and in particular in our centre became very crucial. This prompted
studies that enable the identification of K. pneumoniae and E. coli
with atypical blaSHV-11 that was responsible for the high resistance
of these microorganisms to β-lactams. In addition isolates of Chryseobacterium
indologenes producing metallo-β-lactamase were also identified (Zeba
et al., 2005). In 2002, in the centre, a large number of E. coli
strains were resistant to aminopenicillins (>90%) and cotrimoxazole (80%),
only norfloxacin appeared to be very efficient, however, the antibiotic was
not widely used in the country (Bonfiglio et al.,
2002). According to the present results, there is a decrease of resistance
to β-lactams. This may be due to the fact that by the end of 1990s a nationwide
restriction in the prescription of the main β-lactams was adopted with
the introduction of ciprofloxacin and norfloxacin that were first found to be
too expensive for the patients. The decrease of resistance to β-lactams
and the susceptibility to the quinolones may be the results of the selective
pressure. Reduction of antimicrobial resistance by the modulation of antibiotic
policies was found in France, where studies have demonstrated reduced prevalence
of gentamicin-resistant MRSA on reducing gentamicin prescribing (Aubry-Damon
et al., 1997). In Finland also, a trebling of community prescribing
of erythromycin in the late 1980s and early 1990s, to treat group A streptococcal
throat and skin infections, led to an increase in erythromycin resistance from
5% in 1988 to 19% in 1993. A subsequent 50% reduction in erythromycin consumption
then led to resistance rates falling to 8.6% in 1996, indeed resistance rates
may decline without total removal of the antibiotic, probably by reduced selection
allowing suppressed, sensitive strains to become dominant (Gould,
Antimicrobial resistance is a major challenge to take up in the near future. The phenomenon results in the increase of mortality and morbidity, as well as an increase in the cost for health care system. In Burkina Faso as in many other developing countries, where, there is a lack of bacteriology laboratories and where antibiograms are not affordable for the majority of the patients, clinicians only relied on empirical therapy to prescribe antibiotics. This is the first study conducted on the ethiology of urinary tract infection and the antimicrobial resistance pattern of the implicated bacteria in the country. Present results indicate that a periodical survey on the susceptibility of the major pathogenic microorganisms is useful for the therapeutic choice and the rationale use of antimicrobial agents.
The authors gratefully thank M. Charles Dabire, M. Oscar Zoungrana and Mme Fatou Nana for their technical assistance.
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