doi:10.1111/jog.13687 J. Obstet. Gynaecol. Res.

2018

Maternal and perinatal complications in pregnant women with

urinary tract infection caused by Escherichia coli

José G. Dautt-Leyva1, Adrian Canizalez-Román2,3, Luis F. Acosta Alfaro4,

Fernando Gonzalez-Ibarra5 and Joel Murillo-Llanes3
1 4 3
Department of Neonatology, Department of Perinatology, Research Department, Women’s Hospital, Secretariat of Health,
2 5
Sinaloa, Research Department, Faculty of Medicine, Autonomous University of Sinaloa, Sinaloa, Mexico; Medicine Department,
Gulf Coast Medical Center, Panama City, Florida, USA

Abstract
Aim: The incidence of urinary tract infection (UTI) in pregnant women may vary from 5–10% and depends on parity,
race, socioeconomic status and anatomical and functional changes in pregnancy. In Mexico, pre-term birth accounts for
75% of perinatal deaths and 50% of the neurological sequelae attributable directly to prematurity. The objective of the
present study is to describe maternal and perinatal complications in preg-nant women with UTI caused by Escherichia
coli and to find out the antimicrobial susceptibility pattern.
Methods: A descriptive and longitudinal study of pregnant women admitted to the Women’s Hospital in Culiacan, Sinaloa,
Mexico, was carried out from January 2013 to December 2014. Patients with E. coli infec-tion were included, and
infections caused by other microorganisms were excluded. The sociodemographic variables, causes of hospitalization
and the type of maternal and perinatal complications were determined.
Results: The causes of admission to the hospital were threatened preterm labor, and fever and threatened abortion. Of 38
patients with threatened preterm labor, 33 went on to delivery, four were preterm births and two were neonatal deaths. E.
coli was sensitive to over 90% of piperacillin-tazobactam, amikacin, nitrofuran-toin and carbapenems.

Conclusion: According to this study in a Mexican population, the number one admission diagnosis in women with UTI
due to E. coli was threatened preterm labor, and fever and threatened abortion. E. coli was sensitive to more than 90% of
piperacillin-tazobactam, amikacin, nitrofurantoin and carbapenems.
Key words: antimicrobial resistance, Escherichia coli, perinatal complications, urinary tract infection.

Introduction
The incidence of urinary tract infection (UTI) in preg-nant
women depends on parity, race and socioeco-nomic status.
Also, anatomic and functional changes associated with
pregnancy, including hydronephrosis, increased urinary
volume, decrease in the tone and peristalsis of the urethra
and bladder (urinary stasis), partial obstruction of the ureters
by the gravid uterus and other factors such as glycosuria
induced by preg-nancy, aminoaciduria and changes in pH
and
osmolality. These factors are conditions that increase the risk
of UTI during pregnancy. Hygiene and sexual activity also
play an important role in the development of UTI during
pregnancy. UTI occur in 5–10% of preg-nant patients.
Although it may initially present as asymptomatic
bacteriuria (AB), if it is not diagnosed early and treated, it
can evolve into a more complex form of UTI such as cystitis
or pyelonephritis.1
It is well known that AB is a predisposing risk factor in
pregnant women that must be diagnosed and trea-ted early
due to its high frequency (2–11%) and risk

Received: October 16 2017.

Accepted: April 22 2018.
Correspondence: Dr Joel Murillo-Llanes, Research Department, Women’s Hospital, Culiacan, Sinaloa, Mexico.
Email: invhgc@gmail.com

© 2018 Japan Society of Obstetrics and Gynecology 1

J. G. Dautt-Leyva et al.
for developing more serious conditions such as pyelo-
nephritis (20–40%). There is evidence that eradication of
AB prevents around 80% of pyelonephritis episodes in
pregnant women. The most common clinical mani-festations
of UTI in pregnant patients are generalized malaise, dysuria,
increase urinary frequency, low back pain and fever in up to
30% of the cases.2–8
Escherichia coli is one of the most common gram-
negative organism found in hospital and community-
acquired bacteremia. Some series report E. coli as being the
culprit in up to 80–90% of the cases. It is also reported as
one of the most important culprits in recurrent UTI, which
may occur in up to 25% of patients that has developed a UTI
in the previous 6 months. The correct treatment of this
microorgan-ism can prevent the complications associated
8–10
with UTI in pregnant patients.
In Mexico, preterm birth is one of the most impor-tant
causes of perinatal morbidity and mortality, accounting for
75% of perinatal deaths, 50% of the neurological sequelae
attributable directly to prematu-
rity and its frequency is estimated to be around 5–10% of all
pregnancies.11,12
The Women’s Hospital, located in the city of Culia-can,
Sinaloa, Mexico, is a major reference center. It was founded
in 2009 and treats approximately 7000–8000 pregnant
women annually. Among the most common admission
diagnoses in our hospital are preterm birth, threatened
abortion and premature rupture of membranes. It is unknown
in our hospital what the complications in both the pregnant
patient and the fetus are due to UTI from specifically E. coli.
The main objective of the present study is to describe the
maternal and perinatal complications in pregnant women
with UTI caused by E. coli, and as a secondary objective to
determine the antimicrobial susceptibility pattern of E. coli
at the Women’s Hospi-tal of Culiacan, Sinaloa, Mexico.
Methods
A descriptive and longitudinal study of pregnant patients
admitted to the hospital with complications related with
pregnancy was carried out at the Obstet-rics and Gynecology
service at the Women’s Hospital of Culiacan, Sinaloa,
Mexico, from January 2013 to December 2014. Patients that
were included in the study signed a consent form, a urine
culture was obtained in all patients and only patients with
UTI caused by E. coli were included. Patients with UTI
2 © 2018 Japan Society of Obstetrics and Gynecology
from causes other than those caused by E. coli were
excluded. Also, immunocompromised patients, either due to
myeloproliferative diseases or those under
immunosuppressive treatment, were also excluded. A
nonprobabilistic sampling was performed for the con-
venience of consecutive patients with UTI.
The maternal variables analyzed were age at risk (≤19
years and ≥35 years), marital status, academic background,
a risky prenatal control (fewer than four prenatal visits),
weeks of gestation, number of preg-nancies, the type of
clinical manifestations of UTI and the frequency of those,
AB, threatened preterm labor (preterm birth was defined as
that occurring between 20.1 and 36.6 weeks gestation) and
maternal
death.7,13,14
The variables of the fetus or newborn were weight at birth,
the presence of macrosomia (over 4 kg), ade-quate weight
(2500–3999 g), low birthweight (1500–2499 g), very low
birthweight (1000–1499 g), extremely low birthweight
(500–999 g), spontaneous abortion and stillbirth or neonatal
death.15,16
UTI was defined as those pregnant patients with clinical
manifestations suggestive of UTI such as lum-bar pain,
dysuria, increase urinary frequency, bladder tenesmus,
urgency, nocturia and/or signs such as fever, pain at
palpation in the lower abdomen, costo-vertebral or flank
tenderness, pain at percussion in lumbar area, macroscopic
hematuria or those with at least two of the following findings
in the urinalysis: pH greater than 6.5, positive leukocyte
esterase, posi-tive nitrites, white blood cell count greater
than 10 cells per field, bacteriuria greater than two (++) and
the presence of erythrocytes.
Urine culture
Urine culture was considered positive when an organ-ism
was found and the colony count was greater than 10 5.17 We
analyzed the frequency and type of micro-organisms isolated
in the urine culture as well as the antimicrobial susceptibility
pattern for E. coli.
Sample collection and procedure
The sample was taken from the first micturition in the
morning, with previous hand washing with soap and water,
rinsed with water and dried with a clean towel, the genital
labia were separated and kept sepa-rated at all times until the
urine sample was completely collected, the vulva was
washed with a soapy gauze from front to back, and then the
process was repeated four times and rinsed carefully with
warm water to remove the remaining soap.
 Maternoperinatal effects of E. coli

Furthermore, the patient was instructed to urinate by
discarding the first 20–25 mL, after which, and with-out
interrupting urination, the rest of the urine was collected in a
sterile container.
Culture and identification of E. coli
Samples were cultured on blood agar and MacCon-key agar,
then incubated for 24 h at 37 C. The macro-scopic
characteristics of the colonies (shape, size, pigment
production and odor) were observed. Posi-tive urine cultures
were tested for susceptibility to 25 antibiotics using the
MicroScan Walk Away 96 automated system, following the
manufacturer’s instructions; the strains were considered
resistant according to the minimum inhibitory concentration
as indicated by the interpretation criteria of the National
Committee for Clinical Laboratory Standards.18 To confirm
bacterial identification, biochemical tests were performed
(API E20, Bio Mérieux).
Statistical analysis
The data were collected in a database developed in Microsoft
Excel 2010. Descriptive analysis was per-formed for the
qualitative variables obtaining fre-quencies and percentages;
for the quantitative variables, we obtained measures of
central tendency such as the mean, median and mode, as well
as mea-sures of dispersion, maximum or minimum values,
standard deviations and confidence intervals. Stata
version 6.0 was used to analyze the data (Stata Corporation).
Results
Ninety-nine patients with UTI caused by E. coli were
included in the study, and the mean age was 24.1 5.6 years
with 25.6 9.4 weeks of gestation (minimum of 6 and
maximum of 41) with 3.13 2 days of hospitalization
(minimum of 1 and maximum of 10) and a median of two
pregnancies with a mini-mum of 1 and maximum of 7. In
general, 45.45% were primigravida, 20.20% were teenagers,
41.67% had inadequate prenatal control, 28.28% had urinary
symptoms such as dysuria, urinary urgency and blad-der
tenesmus, and the presence of symptoms such as
costovertebral angle tenderness (CVAT) (unilateral or
bilateral), and generalized malaise were present in 33.33%
of the cases. The frequency of fever outside the hospital was
45.45%; however, at the time of admission, a temperature
above 37.5 C was observed in only 20.20% of the cases. AB
occurred in 54.55%, and cesarean section was performed in
48.19%. The frequency of these variables varied according
to the trimester of the pregnancy in which the patient was
admitted to the hospital (Table 1).
The main causes of admission to the hospital were
threatened preterm labor in 38 cases (33.33%), fever in 20
cases (17.54%) and premature rupture of

Table 1 Clinical and sociodemographic characteristics of patients with urinary tract infection (UTI) due to Escherichia coli according
to the trimester of pregnancy in which they were hospitalized
Variable First trimester Second trimester Third trimester Total
(n = 13), n (%) (n = 39), n (%) (n = 47), n (%) (n = 99)
Primigravida 6 (46.15) 21 (53.84) 18 (38.29) 45
Teenager 3 (23.08) 12 (30.76) 5 (10.63) 20
35 years of age or older 0 (0) 0 (0) 4 (8.51) 4
Inadequate prenatal follow-up† 5 (38.46) 11 (28.20) 19 (40.42) 35
Single 2 (15.38) 7 (17.94) 15 (31.91) 24
Cohabitation 8 (61.53) 25 (64.10) 24 (51.06) 57
Married 3 (23.07) 6 (15.38) 7 (14.89) 16
Anemia (hemoglobin less or 3 (23.07) 15 (38.46) 13 (27.65) 31
equal to 11 g %)
Fever 4 (20) 11 (55) 5 (25) 20
Lower urinary symptoms 7 (53.84) 14 (35.89) 7 (14.89) 28
CVAT, unilateral or bilateral 7 (53.84) 15 (38.46) 11 (23.40) 33
Bacteriuria 5 (38.46) 14 (35.89) 19 (40.42) 38
Bacteriuria asymptomatic 4 (30.76) 16 (41.02) 34 (72.34) 54
Cesarean section 4 (30.76) 17 (43.58) 19 (40.42) 40
Admission to intensive care unit 2 (15.38) 3 (7.69) 2 (4.25) 7
†Defined as fewer than four prenatal visits. CVAT, costovertebral angle tenderness.

© 2018 Japan Society of Obstetrics and Gynecology 3

J. G. Dautt-Leyva et al.

Table 2 Main causes of hospitalization in pregnant women those 115 cases, 99 cases (86%) were positive for
with urinary tract infection due to Escherichia coli† E. coli, five cases (4.34%) for Proteus vulgaris, eight cases
(6.95%) for Klebsiella pneumoniae and one case (0.86%) for
Diagnosis Frequency % Candida albicans. E. coli demonstrated anti-microbial
Threatened preterm labor 38 38.38 sensitivity to more than 90% to cefotetan, piperacillin-
Fever 20 20.20 tazobactam, amikacin, all carbapenems and antimicrobial
Cervicovaginitis 11 11.11 resistance higher than 60% for ampicillin, cephalothin,
Premature delivery 8 9.41
Threatened abortion 10 7.84
piperacillin and trimetho-prim/sulfamethoxazole.
Hypertension 8 7.84
Spontaneous delivery 7 6.14
Premature rupture of 6 5.26
membranes
Spontaneous abortion 3 3.53
Discussion
Oligohydramnios 2 2.02
The most common clinical manifestations were low urinary
†We reported eight cases of pregnant women hospitalized for
polyhydramnios, lumbociatica and seizures, transvaginal bleeding,
symptoms compatible with cystitis such as dysuria, urinary
chorioamnionitis, fetal death, placental abruption, urinary lithiasis and frequency, bladder tenesmus in 28% of cases, and CVAT
hyperemesis gravidarum. and generalized malaise in 33%, similar results to those
observed in a study done in Colombia that included a sample
membranes in six cases (5.26%) (Table 2). Of the 38 patients of 1759 patients. In both studies, E. coli demonstrated a high
with threatened preterm delivery, 33 underwent delivery. antimicrobial
There were four preterm births, of which two were neonatal resistance to ampicillin, which fluctuated between 60% and
deaths. Of the 10 patients with threatened abortion, three 74%.19,20 In a study done in a Mexican popu-
underwent delivery, one was preterm birth, one was an lation, Acosta-Terriquez et al. demonstrated that up to 35%
abortion and in the other the result is unknown because the of the cases with threatened preterm labor had UTI and 32%
baby was born in another hospital (Table 3). of them ended in preterm births, a very similar finding as to
what we found in the present study.21 The incidence of
The patients with threatened preterm labor experi-enced preterm birth remains stable in several regions of the world
fever during pregnancy in 32% of the cases and patients with and fluctuates between 5% and 12%, but in some countries,
threatened abortion experienced fever during pregnancy in it tends to increase as in underdeveloped countries or in Latin
40% of the cases. Patients in the second trimester of America, where poverty has a negative impact in health care
pregnancy with fever account for two of three cases of to the point where infections and the incorrect use of
neonatal death and one of two intrauterine deaths; on the antibiotics in these group of patients may be more
other hand, in the three cases of spontaneous abortion in common.22 On the other hand, the annual incidence of
women in the first trimester of pregnancy, none of them epilepsy in children in developed countries is approximately
experienced fever; of the newborns 10.59% were 50–70 cases per 100 000 inhabitants and in developing
hospitalized, and of the preterm infants 7.06% were countries the figure is even higher. Although this varies
hospitalized. according to age, this is surely favored by preterm delivery
There were 245 cases of pregnant women admitted to the where there is a high prevalence of UTI in pregnant
hospital during the study period; of those, 115 cases women.23 Threatened preterm labor, fever, threatened
(46.93%) were diagnosed with UTI. From abortion and cervicovaginitis were the most common causes
of admission to the hospital in our study, and the com-
Table 3 Fetal outcomes in pregnant women with uri-nary plications in the newborns were low birthweight, neo-natal
tract infection caused by Escherichia coli death and abortion.
Variable Frequency %
Normal birthweight 65 65.66
Low birthweight 8 8.08 Changes in the levels of hormones during preg-nancy
Neonatal death 3 3.53 have been hypothesized to sensitize the uterus to different
Abortion 3 3.53 insults. When pregnancy is complicated by UTI, the
Stillbirth 2 2.35 endotoxin constituents of these microor-ganisms such as E.
Extremely low birthweight 2 2.02 coli can theoretically precipitate preterm labor because of
Very low birthweight 1 1.01
systemic inflammation

4 © 2018 Japan Society of Obstetrics and Gynecology


occurring and during which there is a release of cyto-kines
such as Interleukin (IL)-6, IL-8, tumor necrosis factor-α or
by the activation of the complement system.24–26 Although
cervicovaginal infections and vaginosis are within the causes
of premature rupture of membranes, there is no strong
evidence about the influence of UTI as a risk factor.
However, in a study conducted in Cuba, 14.7% of patients
with premature rupture of membranes were diagnosed with
UTI,
which was very similar to what we found in our pop-
ulation.27,28 AB and UTI have been associated with
threatened abortion and miscarriage, and it is believed that
decreases in levels of progesterone in the first trimester of
pregnancy can predict the risk of spontaneous abortion.
Although it is important to note that as pregnancy
progresses, the microflora of the genital tract tends to be less
harmful to the fetus.29–32 We observed that the frequency of
cervicovaginitis and pelvic inflammatory disease were
higher in the second and third trimester of pregnancy, which
coincides with three cases of neonatal deaths in pregnancies
less than 32 weeks of gestation. There are studies carried out
in humans that have shown that exposure to fever during
preg-nancy can cause internucleosomal DNA fragmenta-
tion, which is a risk factor for fetal resorption, miscarriage
or malformations. Other studies have also shown that
pregnant women exposed to fever between the fifth and
eighth week of gestation have a higher risk of neural tube
defects such as spina bifida, anencephaly and cardiac
malformations.26
On the other hand, large cohort studies conducted in
Europe, the United States, Indonesia and case– control
studies conducted in the United States, Swe-den and
Australia have shown that there is a statisti-cally significant
association between an abnormal genital microflora and
adverse pregnancy outcomes; therefore, it is recommended
that treatment should be given before 24 weeks of gestation
to avoid a late abortion or a preterm birth. These conditions
could be increased if associated with pelvic inflammatory
dis-ease, endometritis or UTI.26 This is something that
occurred in our population in 9% of the cases. In stud-ies
conducted in Egypt, similar to our results, the most common
pathogen causing UTI was E. coli in 83% of cases, and they
reported that lack of genital grooming before and after
intercourse, having sex more than thrice per week are risk
factors for UTI during pregnancy, and failure to empty the
bladder after intercourse increased the risk of UTI by eight
times.1 In Mexico City, the prevalence of UTI due to
© 2018 Japan Society of Obstetrics and Gynecology
Maternoperinatal effects of E. coli
E. coli and AB in type 2 diabetics was 68.6% and 12.5%,
respectively, and this is lower than that observed in our
patients. This may indicate that there is a higher risk of UTI
in our population of pregnant women.19 The most effective
antibiotics against E. coli in our study were carbapenems,
piperacillin-tazobac-tam, followed by amikacin and
ciprofloxacin, and we observed antimicrobial resistance
greater than 60% in antibiotics such as ampicillin,
cephalothin, piperacillin and
trimethoprim/sulfamethoxazole. A common empiric
treatment for obstetric infections is ampicillin, but antibiotic
resistance can be quite high. There are several other
relatively safe options available for treat-ment such as
nitrofurantoin, amoxicillin and certain cephalosporins (e.g.
cephalexin, cefpodoxime).33 Duration of treatment is
typically 5–7 days. The deci-sion should be made based on
the stage of pregnancy, presence of contraindications in the
expectant mother, consideration of the side effect profile for
each medi-cation and resistance patterns in the population.
These are very similar results to those reported by
Mohammed et al.34 in a study carried out in Libya
with 1153 patients with UTI due to E. coli, including men,
women and children.35,36 We considered that
the use of antibiotics before hospital admission may be a
predisposing factor for antibiotic resistant in our setting,
because around 86% of our patients received empiric
antibiotic treatment prior to their hospitaliza-tion. According
to the systematic review and meta-analysis conducted in
2010 by Costelloe et al. in the UK, people who are prescribed
an antibiotic as an outpatient for respiratory or UTI may
develop antimi-crobial resistance to that antibiotic, and that
effect increases after the first month of treatment and may
persist for up to 12 months.37 Inappropriate empirical
antimicrobial therapy in quinolone-resistant strains, or the
presence of extended spectrum beta-lactamase-producing
strains is the primary independent risk fac-tor for mortality
in cases of E. coli bacteremia.38 Con-sidering the
weaknesses of our study, we believe that the sample size of
99 cases may be the most impor-tant; however, we carried
out a longitudinal descrip-tive study so we could observe the
maternal and perinatal complications in patients hospitalized
for UTI caused by E. coli. Although we know that the
microorganisms Proteus vulgaris and Klebsiella pneumo-
niae were isolated in urine cultures of these patients, they
were not included in the study because these were not the
objective of the investigation and these are isolated more
commonly in immunocompromised patients and in those
with sepsis secondary to
5
J. G. Dautt-Leyva et al.
obstruction of urinary tract.39 However, the strength of this
work is that it allowed us to see that the preva-lence of
asymptotic bacteriuria during pregnancy in our population is
high, which is why we consider that all women should be
screened for bacteriuria in the first trimester, and women
with recurrent UTI should be subjected to repeated
urinalysis during pregnancy for timely detection. Treatment
should be based on the antibiogram report because
recurrence may occur in up to one third of patients, and early
treatment is necessary to prevent complications. In addition,
we believe that greater importance should be given to the
impact that fever has on pregnant women, especially in the
first trimester, given the damage it could cause to fetal DNA.
Of which, the consequences are already known, a close
monitoring of patients who suffered temperatures higher
than 38.5 C is recommended.26
Finally, the frequency of UTI due to E. coli in hospi-
talized pregnant women was similar to that reported in other
countries, and the main complication was threatened preterm
labor; however, 85% went on to delivery. The frequency of
AB was higher than that reported at the national average and
in other coun-tries. We observed that AB increases as the
pregnancy progresses and doubles by the end of pregnancy.
Neonatal deaths and intrauterine deaths were more frequent
in pregnant women exposed to fever during the second
trimester. Thus, we conclude that these results should alert
us even more regarding the importance of proper
management of UTI in pregnant women.
Acknowledgments
The authors thank Sinaí Palma Serrano, a third-year medical
student of the Faculty of Medicine of the Autonomous
University of Sinaloa, for her valuable contribution in the
data collection and the elaboration of the database of this
study, Elva E. Arce Vargas, a chemist, and all personnel in
the area of bacteriology of the Women’s Hospital laboratory,
and also to Jason Darr, a third-year medical student from the
Alabama College of Osteopathic Medicine at Gulf Coast
Regional Medical Center for his commitment and assistance
in the editing and proofing of this paper.
Disclosure
None declared.
6 © 2018 Japan Society of Obstetrics and Gynecology
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