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Obstetrics & Gynecology 2000;96:113-119
© 2000 by The American College of Obstetricians and Gynecologists
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ORIGINAL RESEARCH

Urinary Tract Infections During Pregnancy and Mental Retardation and Developmental Delay

SUZANNE MCDERMOTT, PhD, WILLIAM CALLAGHAN, MD, LISA SZWEJBKA, MSPH, HEATHER MANN, MSPH and VIRGINIE DAGUISE, MSPH

From the Department of Family and Preventive Medicine, University of South Carolina School of Medicine, Columbia, South Carolina, and the South Carolina Budget and Control Board, Office of Research and Statistics, Columbia, South Carolina.

Address reprint requests to: Suzanne McDermott, PhD, University of South Carolina School of Medicine, Family Practice Center, 6 Richland Medical Park, Columbia, SC 29203, E-mail: scmdermott{at}rmh.edu


   Abstract
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Abstract
Materials and Methods
 Results
 Discussion
 References
 
Objective: To investigate the association between urinary tract infections during pregnancy and mental retardation or developmental delay in infants.

Methods: An inception cohort design was used to analyze Medicaid maternal and infant-linked records and vital records for 41,090 pregnancies from 1995–1998.

Results: The relative risk (RR) for mental retardation or developmental delay among infants of mothers with diagnosed urinary tract infections but no antibiotic claims was 1.31 with a 95% confidence interval (CI) of 1.12, 1.54 compared with the group without urinary tract infections. The RR for infants of mothers with urinary tract infections without antibiotic claims was 1.22 (95% CI 1.02, 1.46) compared with infants of mothers with urinary tract infections and antibiotic claims. The RR was significant in the first trimester (1.46, 95% CI 1.07, 1.99) and third trimester (1.41, 95% CI 1.11, 1.79) after controlling for race and gestational age at birth.

Conclusion: There was a statistically significant association between maternal urinary tract infections without evidence of antibiotics and mental retardation or developmental delay in infants. The relationship persisted when we assumed that over 30% of women who had antibiotic claims filled but did not take the medicine, and 40% of the women who did not have antibiotic claims did take the medication.

Urinary tract infections are the most common medical complication of pregnancy, occurring in approximately 4–7%.1–6 When all potentially offending genitourinary pathogens are included, and when the spectrum of asymptomatic bacteriuria is considered, those factors might increase frequency of maternal bacteriuria to 25%.5,7

Numerous studies during the past 30 years have reported associations between urinary tract infections during pregnancy and adverse outcomes, including pyelonephritis, anemia, renal failure, and hypertension in mothers; and preterm delivery, fetal growth restriction, low birth weight, and fetal death in infants.3,5,8–24 The relationship between maternal urinary tract infections and cognitive function of the infant has been explored, with little consensus on the association. Researchers for the National Collaborative Perinatal Project reported intelligence quotient scores were 2.38 points lower among white male offspring whose mothers had urinary tract infections during pregnancy, compared with unexposed infants, but no statistically significant variation in intelligent quotient scores was seen in black male or female infants.9,10

Mental retardation is one of the most common disabilities in childhood, with a prevalence rate of 2% or greater in most populations.25 Developmental delay is a broader label, often used during preschool years before a diagnosis of mental retardation is made. Based on data from the National Health Interview Survey, it has been estimated that 16.8% of children under 18 years old in the United States have at least one developmental disability.26

The notable problem with previous studies is the difficulty ascertaining the cause of mental retardation or developmental delay. Investigators have been unable to find causes in approximately 35–50% of individuals who had extensive examinations. The etiology of mental retardation is often described as multifactorial because most individuals have more than one possible cause. A multifactorial approach to etiology has been proposed, which includes biomedical, social, behavioral, and educational categories.27,28 The studies that investigated urinary tract infection as a cause of mental retardation or developmental delay have included many concurrent factors but not treatment of diagnosed urinary tract infections. Hence, it is not known whether the association of maternal urinary tract infection and adverse perinatal outcomes relates to the infection or the effectiveness of antimicrobial therapy.

This study compared frequency of mental retardation or developmental delay in infants of women who had urinary tract infections during pregnancy with its frequency in those who did not have urinary tract infections. We also explored the effect of presumed treatment of infection and its relationship to incidence of mental retardation or developmental delay. Our hypotheses were that a substantial proportion of women did not use prescribed medication for urinary tract infections during pregnancy, and that failure to do so is associated with increased frequency of mental retardation or developmental delay in their offspring. Linked Medicaid and vital records were used to answer those questions, a method encouraged in the literature.29


   Materials and Methods
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Abstract
 Materials and Methods
Results
 Discussion
 References
 
Data were collected from master files of the Office of Research and Statistics of the South Carolina Budget and Control Board, which link birth certificate data with medical information from Medicaid billings pertinent to mothers and infants. The file links birth outcome data from the Hospital Discharge Data Set (using Uniform Billing codes from 1992) with the birth certificate file and the Medicaid claims for prenatal and maternity care.

Mother-child pairs were matched and linked using the delivery file and the live birth certificate file. Through successive iterations, maternal deliveries were matched to live birth certificates based on agreement of hospital of delivery or birth, mother’s date of birth, infant’s date of birth, and (from 1994 onward) mother and infant names. Linked delivery-birth certificate files were matched to newborn files through a similar iterative matching algorithm. The three-way match was successful for 41,090 (86.9%) of the 47,246 reported live births (Figure 1Go). Medicaid-financed care for children is available after birth through a computerized file. South Carolina has expanded Medicaid coverage (up to 185% of poverty) for children until age 21 years. Thus we were able to search for mental retardation and developmental delay codes through 1998 because those files were linked and available for analysis. All matched records of children who had known causes of mental retardation were deleted. After those exclusions, there were 2875 cases of mental retardation (n = 617) or developmental delay (n = 2258) of unknown cause remaining for analysis. Diagnoses were identified using International Classification of Diseases, 9th Revision, Clinical Modification (ICD-9-CM) codes 315 (specific delays in development), 317 (mild mental retardation), 318 (other specified mental retardation), or 319 (unspecified mental retardation).



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  		Figure 1. UTI = urinary tract infection; MR = mental retardation; DD = developmental delay; 1 = difference: 9.2% UTI filled prescription and 6.8% no UTI, P < 0.001; 2 = difference: 9.2% UTI not filled prescription and 7.4% filled, P < 0.005; 3 = difference: 7.4% filled prescription and 6.8% no UTI, P < 0.05.

 
Case definitions for urinary tract infection exposure were either a Medicaid claim based on an ICD-9-CM diagnosis of urinary tract infection (ICD-9-CM code 599.0) or a claim for a urinalysis or urine culture, followed by a claim for an antibiotic within 14 days of testing. A group of 8578 infants was exposed to urinary tract infections (5320 had ICD-9-CM codes of 599.0 and 3258 had claims for urinalysis or urine culture, followed by claims for antibiotics). They were compared with the 32,237 infants who were not exposed to urinary tract infection or antibiotics.

Data were analyzed using {chi}2 tests and logistic regression modeling using SAS (SAS Institute, Cary, NC) for the UNIX operating system. {chi}2 tests were used to compare distribution of independent variables, whereas logistic regression models were used to measure associations between urinary tract infection exposure and mental retardation or developmental delay. We also compared the risk of mental retardation or developmental delay among exposed infants whose mothers had prescription claims with those whose mothers did not. Maternal age, gestational age at first prenatal visit, race, maternal alcohol use self-reported on the birth certificates, and gestational age at birth are associated with infant mental retardation and maternal urinary tract infection, thus, were considered potential confounders in the logistic models. Analysis of pharmacy claims data allowed us to assess antibiotics prescribed prenatally so this factor could be related to the mental retardation or developmental delay outcomes.


   Results
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Abstract
 Materials and Methods
 Results
Discussion
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The demographics of the mother-child pairs are shown in Table 1Go. The group of women with urinary tract infections without filled prescriptions had the highest proportion of black women, reported more alcohol use, had a higher proportion of infants less than 37 weeks’ gestation at birth, and had the highest fetal death rate. Women in the urinary tract infection group with filled prescriptions had the highest proportion of mothers with less than a high school education, and women without urinary tract infections had the highest proportion of older mothers. Those characteristics were considered potential confounders in the multivariable models and were used to adjust the relative risk (RR) calculations.


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  		Table 1. Maternal, Child, and Prenatal Care Characteristics
 
Among the 40,815 mother-infant pairs analyzed, 20.9% of mothers had urinary tract infections, with a 95% confidence interval (CI) of 20.5, 21.3. There were 2875 cases of mental retardation or developmental delay in infants, for a rate of 7.04% (95% CI 6.79, 7.29) for the entire group and composed of a mental retardation rate of 1.51% (95% CI 1.39, 1.63) and a developmental disability rate of 5.53% (95% CI 5.31, 5.75).

We identified 2013 women (23.5%) in the urinary tract infection group who had no pharmacy claims for medication for infections in the 2 weeks after diagnosis (Figure 1Go). Within that group, 185 infants (9.2%) had mental retardation or developmental delay. Women with filled antibiotic prescriptions had 488 infants with mental retardation or developmental delay (7.4%). When there was no report of maternal urinary tract infection, 2205 (6.8%) of infants had mental retardation or developmental delay. Differences among the groups were statistically significant. The urinary tract infection prescription-unfilled group’s percentage of infants with mental retardation or developmental delay was 35% higher than that of the unexposed group and 24% higher than that of the group that had urinary tract infections and had prescriptions filled.

To determine whether the association between exposure to urinary tract infection and mental retardation or developmental delay was influenced by other variables, logistic regression modeling was used (Table 2Go). The RR for mental retardation or developmental delay was 1.31 (95% CI 1.12, 1.54) when mothers had urinary tract infections and no pharmacy claims for antibiotics compared with women with no urinary tract infections. The risk was statistically significant in the first and third trimesters (first trimester 1.46 [95% CI 1.07, 1.99] and third trimester 1.41 [95% CI 1.11, 1.79]) but was not significant for the second trimester (1.14, [95% CI 0.95, 1.71]). The RR for mental retardation or developmental delay was 1.22 (95% CI 1.02, 1.46) in infants whose mothers did not have antibiotic claims compared with women with urinary tract infections and filled prescriptions. The RR of 1.37 (95% CI 1.03, 1.82) was statistically significant in the third trimester.


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  		Table 2. Adjusted Relative Risk (and 95% Confidence Interval) for Mental Retardation After Urinary Tract Infection During Pregnancy
 
In these results, our assumption was that all the women without antibiotic claims did not take the medicine. However, that is not realistic, so we modeled the effect of assuming that 10–40% (in increments of 5%) of women who did not have antibiotic claims actually took antibiotics (paid by another source or given as samples). We also assumed that all the women with antibiotic claims took the medicine, so we modeled the effect of assuming that 10–40% of those women did not take antibiotics, again in increments of 5%. That approach allowed us to control for the biases in the study that arose from what we really cared about, namely, use of antibiotic, not its purchase. The results in Table 3Go show that the 9.2% rate of mental retardation or developmental delay for women who did not take medication was still statistically significant (P < .05) with the assumption changed to allow for 10–35% of the women with prescription claims filled not taking their medicine and up to 40% of women who did not have antibiotic claims taking medicine. That range of assumptions (generating 49 pairwise comparisons) resulted in mental retardation or developmental delay rates between 8.41% and 9.45% for the remaining women who did not take their medicine. Thus, our estimate of a mental retardation or developmental delay rate of 9.2% of infants of women who did not take their antibiotics is a reasonable approximation of the rate.


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  		Table 3. Mental Retardation and Developmental Disability Rate for Mothers With Urinary Tract Infections and No Antibiotic Claim*
 

   Discussion
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Abstract
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 Results
 Discussion
References
 
We found statistical evidence that failure to take antibiotics to treat urinary tract infections is associated with mental retardation or developmental delay. Because diagnosis and treatment codes were available, we were able to exclude infants with diagnoses of known causes of mental retardation, an advancement over use of historical datasets, such as the National Collaborative Perinatal Project, because fewer causes of mental retardation were known during the 1970s. The rate of mental retardation or developmental disability was within the range reported by other studies.25,26

In this population of Medicaid-funded women, we found that over 23% with urinary tract infections did not have antibiotic claims from their pharmacies which was associated with higher rates of mental retardation or developmental delay in their infants. Antibiotic treatment was determined from pharmacy coding, so it cannot be said with certainty why that percentage is so high. Possible causes include use of sample drugs, underprescribing by providers, noncompliance with prescription filling by patients, failure of pharmacies to submit claims because of paperwork difficulties, or obtaining the prescription without using the Medicaid card because South Carolina Medicaid only covers three prescriptions per month. We believe the last group would be small because most pregnant women are on few prescription drugs other than prenatal vitamins. The consequence of assuming that some women in the untreated group were treated would lead to an underestimate of the real effect of urinary tract infections on mental retardation or developmental delay. Bias in the urinary tract infection group results from the fact that some of the women who had urinary tract infections and a filled prescription did not take their medication. That would lead to an overestimate of the effect, although it is unlikely that over 35% of women who had prescriptions filled did not take their medication (Table 3Go).

The population used for this analysis was a low socioeconomic group, so findings might not be generalizable to all women. An association is recognized between poverty and mental retardation or developmental delay in infants; however, in this study the exposed and comparison groups were covered by Medicaid, effectively controlling for an independent effect of poverty on the outcome. Diagnosis data on infant outcomes are currently available only for children up to 3 years old, and mental retardation or developmental delay might be diagnosed after the age of 3 years, so the numbers of affected infants or children might be underestimated. That limitation could strengthen our findings if more diagnoses of mental retardation or developmental delay were made in the exposed group. Using secondary data analysis meant there was no method for analyzing unrecorded variables, such as maternal signs and symptoms of infection or whether bacteriuria was detected by routine screening. Possibly only febrile cases of bacteruria or specific bacteria were associated with adverse outcomes, but that could not be confirmed because the organism identified by culture was not part of the diagnostic coding.

Biases related to not knowing whether women took medication were explored using various assumptions (Table 3Go). If we assume, for example, that 35% of women who did not have antibiotic claims actually took medicine and 15% of women who had antibiotic claims did not take their medicine, the estimate for mental retardation or developmental delay is 9.07% for those who did not take any medication. Compared with the treated rate of 7.4% mental retardation or developmental delay, that rate is different at a significance level of P = .002. If there really is no difference between women who took antibiotics for their urinary tract infections and those who did not have an infection, the probability of finding a difference between the group without medication and the group with medication would be even stronger. When we simulated the breakdown of assumptions using 6.8% mental retardation or developmental delay (the rate for the control group) instead of 7.4% for the treated group, the estimates for the no-medication group were higher and more statistically significant. That gave us confidence that our predicted rates of mental retardation or developmental delay for women who did not take medication were accurate.

Limitations of this analysis resulted from working with a reimbursement data set. There was ascertainment bias because mean gestational age at entry to Medicaid was 3.1 months (standard deviation [SD] 0.01). Urinary tract infections before entry could not be accounted for in the analysis, and that biased the study to the null hypothesis (no difference between cases and controls). A second bias related to detection of the exposure results from our reliance on computerized data for diagnosis and treatment. The rate of urinary tract infection in that Medicaid group was substantially higher (20.9%) than that in earlier literature. Coding variation is substantial among providers, with any positive urine culture (even in asymptomatic patients) often coded as urinary tract infection. It is possible there was underidentification and overidentification of exposure. Some diagnoses might not be coded (underidentification), and some antibiotic treatments after a urine culture could be for other infections (overidentification). However, we do not believe there was differential or reporting biases of the exposed related to the outcome because the data were collected prospectively.

Women in the group with urinary tract infections without filled prescriptions had ICD-9-CM diagnoses for urinary tract infections and an increased RR for mental retardation or developmental delay compared with women without infections. Thus, the comparison was not affected by classification errors. The group with urinary tract infection and filled prescriptions included ICD-9-CM–diagnosed women and those who had urine cultures followed by antibiotics within 14 days. When we compared that group to the group without urinary tract infection, there was no statistically significant difference in the mental retardation or developmental delay outcome. If we assume there was misclassification in the urinary tract infection group with filled prescriptions because some of the women with urine cultures followed by antibiotics within 14 days did not have urinary tract infections, we could underestimate the association of the exposure and adverse outcome.

The biologic plausibility of cognitive deficits in infants of mothers with urinary tract infections during pregnancy is supported by basic embryology and findings from the National Collaborative Perinatal Project. Subnormal intellectual development can result from insults during the eighth to 16th week and during the later stages of gyri development, myelination, and glial cell formation, when disturbances in the organization of the cells in the central nervous system can result in mental retardation.12,30 It is noteworthy that our data showed a fetal death rate of 5.2% in the group with urinary tract infection without filled prescription compared with no deaths in the group with urinary tract infection with filled prescription and a rate of 2.0% in the no-infection group (Table 1Go), which is consistent with results of Leviton and Gilles.30

Further studies are needed to assess the influence of type of organism, severity of infection, and various treatment regimens on outcomes of mental retardation or developmental delay. Animal models might be helpful for looking at causative pathophysiology and anatomy in that relationship. Expansion of those analyses into broader populations of women representing a larger geographical area and wider income distribution would make our findings more generalizable.


   Footnotes
 
The findings, conclusions, and opinions contained in this manuscript are those of the authors and do not necessarily reflect the findings, conclusions, and opinions of the South Carolina Department of Health and Human Services.

PII S0029-7844(00)00823-1

Received November 2, 1999. Received in revised form January 18, 2000. Accepted February 1, 2000.


   References
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 Results
 Discussion
 References
 
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