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© 2008 American Society for Nutrition J. Nutr. 138:787-792, April 2008

Community and International Nutrition

Maternal Night Blindness during Pregnancy Is Associated with Low Birthweight, Morbidity, and Poor Growth in South India1,2

James M. Tielsch3,*, Lakshmi Rahmathullah4, Joanne Katz3, R. D. Thulasiraj4,5, Christian Coles3, S. Sheeladevi4,5 and Kartik Prakash5

3 Department of International Health, Bloomberg School of Public Health, Johns Hopkins University, Baltimore, MD 21205; 4 Aravind Centre for Women, Children and Community Health, Madurai, Tamilnadu, India 625020; and 5 Lions Aravind Center for Community Ophthalmology, Madurai, Tamilnadu, India 625020

* To whom correspondence should be addressed. E-mail: jtielsch{at}jhsph.edu.


   ABSTRACT
TOP
 ABSTRACT
Introduction
 Methods
 Results
 Discussion
 LITERATURE CITED
 
Maternal night blindness is common during pregnancy in many developing countries. Previous studies have demonstrated important consequences of maternal night blindness during pregnancy on the health of the mother and newborn infant. We compared birthweight, 6-mo infant mortality, morbidity, and growth among infants of women who did and did not report a history of night blindness from a community-based, randomized trial of newborn vitamin A supplementation in south India. Birthweight was measured within 72 h of delivery. Infants were followed until 6 mo of age for mortality and morbidity was assessed at household visits every 2 wk. Anthropometry was assessed at 6 mo of age. A total of 12,829 live-born infants were included, 680 of whom were infants of mothers with night blindness during the index pregnancy. Maternal night blindness was associated with an increased risk of low birthweight in a dose-dependent fashion based on birthweight cut-offs: <2500 g, adjusted relative risk (RR) = 1.13 (95% CI = 1.01, 1.26); <2000 g, adjusted RR = 1.70 (95% CI = 1.27, 2.26); <1500 g, adjusted RR = 3.38 (95% CI = 1.18, 6.33); with an increased risk of diarrhea (adjusted RR = 1.16, 95% CI = 1.03, 1.30), dysentery (adjusted RR = 1.25, 95% CI = 1.03, 1.53), acute respiratory illness (adjusted RR = 1.32, 95% CI = 1.21, 1.44), and poor growth at 6 mo; underweight (adjusted RR = 1.14, 95% CI = 1.02, 1.26), stunting (adjusted RR = 1.19, 95% CI = 1.05, 1.34). Maternal night blindness was not associated with 6-mo infant mortality or wasting at 6 mo. This study demonstrates that there are important consequences to the infant of maternal vitamin A deficiency during pregnancy.


   Introduction
TOP
 ABSTRACT
 Introduction
Methods
 Results
 Discussion
 LITERATURE CITED
 
Night blindness and other ocular signs of vitamin A deficiency have long been known to be associated with increased risk of morbidity and mortality in young children (1). In areas of the world where vitamin A deficiency is endemic, signs of this deficiency, as measured by the functional indicator night blindness or the physiological indicator low serum retinol level, also occur commonly in women of reproductive age, especially in the 3rd trimester of pregnancy when maternal stores are being transferred to the fetus (2–9). In many of these locations, the prevalence exceeds the current International Vitamin A Consultative Group criteria for the definition of a problem of public health significance (10).

Data from Nepal demonstrate that vitamin A deficiency in pregnancy has important health and survival consequences for the woman and her infant. Maternal night blindness was associated with a 3-fold excess risk of maternal death and maternal anemia, higher risks of protein-energy malnutrition, a variety of maternal morbidities, and a 63% excess risk of infant mortality in the first 6 mo of life (11–13).

To determine whether these serious adverse consequences of maternal vitamin A deficiency were confined to Nepal or more generalizable to the Indian Subcontinent as a whole, we examined the risk of low birthweight, early infant mortality and morbidity, and growth among infants born to mothers with and without night blindness during pregnancy in South India.


   Methods
TOP
 ABSTRACT
 Introduction
 Methods
Results
 Discussion
 LITERATURE CITED
 
The study population consisted of pregnant women and their newborn infants from 2 rural blocks in southern Tamilnadu, India who were enrolled in a population-based, randomized trial of newborn vitamin A dosing during the period 1998–2000 (14,15). The specifics of the design, recruitment, data collection, and follow-up have been published previously (14,15). In summary, trained village workers enrolled pregnant women in their villages after obtaining informed consent. Demographic and socioeconomic factors, including age, education, occupation of the head of the household, literacy, type of roof, land ownership, cattle ownership, and fuel used for cooking were obtained from the participants. Information on parental smoking, previous reproductive history, and details of the plan for delivery of the infant were also obtained. Fortnightly visits were made to each family to update any changes in the delivery plan.

After delivery, live-born infants were dosed with either vitamin A or placebo as per the randomization and their birthweight was measured using an electronic digital infant scale (Seca model 727). For this analysis, only weights measured within 72 h after delivery were included. A history of night blindness during the pregnancy was obtained using the approach recommended by the International Vitamin A Consultative Group (16). It began by asking the woman if she had experienced night blindness (using the appropriate local term) during this pregnancy. If she responded positively, we asked if she had problems seeing during the day as well. Only those with problems seeing only at night were considered night blind. All children were followed every 2 wk until 6 mo of age to collect vital status and morbidity details. At each visit, mothers were asked about the onset and length of specific signs and symptoms for each day of the preceding 2-wk period. The morbidities assessed included cough, fever, difficulty breathing, diarrhea, and dysentery. The definitions used in this analysis are as follows: diarrhea: ≥4 loose, watery stools on any day; chronic diarrhea: diarrhea with duration of >14 d; dysentery: blood or mucus in the stool on any day; acute respiratory illness (ARI)6-1: an episode of cough with fever on at least 1 d of the episode; ARI-2: an episode of difficulty breathing with fever on at least 1 d of the episode; and ARI-3: an episode of difficulty breathing with fever and cough on at least 1 d of the episode.

Episodes were defined as continuous days of signs/symptoms that met the above criteria. All episodes were separated by 3 or more symptom-free days. Immunizations received and any visits for health care for the child in the prior 2 wk were recorded.

All children were followed until 6 mo of age at which time they received a final morbidity assessment, anthropometric measurements, and a 100,000 IU dose of vitamin A (105 µmol retinol palmitate) and were discharged from the study. Subjects <6 mo old who were still being followed at the completion of the study at the end of March, 2001 were considered censored alive. The anthropometric assessment at the 6-mo visit consisted of measurements of weight, length, and mid-upper arm circumference (MUAC). Weight was measured using the same scale as was used for newborn weight. Length was measured 3 times to the nearest 0.1 cm using a wooden length board manufactured by Schorr and the median value was recorded. We measured MUAC 3 times on the left arm using a circumference tape and recorded the median value. Weight-for-age, length-for-age, and weight-for-length were calculated using the Anthro 2005 software (WHO) and were based on the WHO reference growth standards (17). Children falling more than 2 SD below the reference median were classified as underweight (weight-for-age), stunted (length-for-age), and wasted (weight-for-length).

    Statistical analysis. All analyses were conducted using either Stata version 9 or SAS version 9. The analysis compared birthweight, growth from birth to 6 mo of age, incidence of diarrhea, dysentery, and ARI, and survival of infants between those born to women with and without night blindness during the index pregnancy. We used statistical models including potentially confounding variables to estimate the association of maternal night blindness with birthweight, 6-mo infant mortality and morbidity, and attained growth at 6 mo of age. Linear regression models were used for continuous outcomes (birthweight, 6-mo weight, length, MUAC, weight-for-age, length-for-age, and weight-for-length), log binomial regression models were used for binary outcomes (percent low birthweight, mortality, underweight, stunting, and wasting), and log linear Poisson models were used for morbidity incidence. The criterion used for significance was a type I error of 5%.

This study received ethical approval from the ethical committee of the Aravind Eye and Children's' Hospitals, Madurai, Tamilnadu, the Department of Health, Tamilnadu State Government, and the Committee on Human Research of the Johns Hopkins Bloomberg School of Public Health, Baltimore, Maryland.


   Results
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 ABSTRACT
 Introduction
 Methods
 Results
Discussion
 LITERATURE CITED
 
A total of 14,035 pregnant women agreed to participate at the time of recruitment, 13,173 of whom delivered 12,936 live-born children (Fig. 1). A total of 687 women reported being night blind at some time during their index pregnancy, a prevalence of 5.22% (95% CI: 4.84, 5.60); 2 women who delivered could not have night blindness assessed as they were blind from other causes. Among those who delivered at least 1 live-born infant, 680 reported having been night blind at some time during that pregnancy, a prevalence of 5.16% (95% CI: 4.78, 5.54). Women who reported being night blind were older, from lower castes, had higher parity, were less likely to be literate, and had poorer housing (Table 1).


Figure 1
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  		FIGURE 1  Flow chart of study participation.

 

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  		TABLE 1 Selected characteristics of night blind and non-night blind women

 
    Infant birthweight. Infants who died prior to our study team's arrival at the place of birth, who were born outside the study area, or whose parents refused could not have their birthweight measured and were excluded, as were those whose weights were measured >72 h after delivery (Fig. 1). Infants born to women who had night blindness during pregnancy had significantly lower birthweight than those born to normal women and the strength of association increased with increasingly restrictive definitions of low birthweight (Table 2). The relative risk (RR) of low birthweight increased from 1.18 when the traditional cut-off of <2500 g was used to 1.75 when the cut-off was <2000 g and 3.76 when the cut-off was <1500 g. Although adjustment for confounders modestly reduced the size of these associations, maternal night blindness remained significantly associated with low birthweight based on any definition.


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  		TABLE 2 Association of night blindness during pregnancy and infant birthweight among live-born infants1

 
    Infant survival. Mortality during the first 6 mo of life was associated with a number of risk factors that are typically associated with an increased risk of mortality. These included maternal literacy, maternal age, parity, socioeconomic status, and a history of previous child death in the household (data not shown). However, maternal night blindness during pregnancy was not associated with an increased risk of mortality in their infants in either the crude or adjusted analysis (Table 3). Stratifying the analysis by the initial treatment group in the trial did not yield an interaction between maternal night blindness and treatment on mortality.


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  		TABLE 3 Crude and adjusted associations of night blindness during pregnancy and 6-mo infant mortality among live-born infants

 
    Morbidity. Maternal night blindness in pregnancy was associated with an excess risk of diarrhea, dysentery, and acute respiratory infections in infants (Table 4). There was a 16% excess risk for diarrhea, a 25% excess risk for dysentery, and an ~30% excess risk for respiratory infection among infants of night blind women after adjusting for potentially confounding factors. The strength of association for respiratory infection did not change with increasing specificity in the definition of ARI. All RR estimates were significantly different from 1.00 at the 5% level.


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  		TABLE 4 Association of night blindness during pregnancy and incidence of morbidity among live-born infants

 
    Growth. Maternal night blindness was associated with poorer attained growth of infants at 6 mo of age (Table 5). After adjustment, infants of night blind women were lighter (difference = 99.0 g), shorter (difference = 0.30 cm), and had modestly higher rates of underweight (RR = 1.14), stunting (RR = 1.19), and wasting (RR = 1.11) than did infants of normal women (Table 5). All differences were significant with the exception of wasting.


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  		TABLE 5 Association of night blindness during pregnancy and attained infant growth at 6 mo

 

   Discussion
TOP
 ABSTRACT
 Introduction
 Methods
 Results
 Discussion
LITERATURE CITED
 
Night blindness during pregnancy is a highly prevalent condition, especially in South Asia where rates vary between 5 and 50% (2–8). In this study, the rate was 5.22%. The correlation of maternal night blindness in pregnancy with poor vitamin A status is supported by studies showing high proportions of women reporting this symptom with low serum retinol levels (18,19). In addition, night blindness is thought of as a sign that occurs only when significant deficiency exists; thus, the true prevalence of vitamin A deficiency among women in this population is likely to be considerably higher than our prevalence of night blindness (16). Although there is a modest amount of literature on the prevalence and risk factors for maternal night blindness, there are few reports describing the health consequences of this condition to either the woman or her infant. Previous perceptions of this condition as an unimportant nuisance have been shown to be inaccurate. As with other indicators of vitamin A deficiency in children and women, there are substantial health consequences associated with this indicator. In our study, maternal night blindness was associated with an increased risk of low birthweight, higher incidence of common childhood morbidities, and poorer attained growth at 6 mo of age. Despite these associations, there was no association with mortality, which is in agreement with a previous study from a mountainous area in Nepal with extremely high rates of maternal night blindness (52%) that showed no significant association between maternal night blindness and 3-mo infant mortality (OR = 1.18; 95% CI 0.94, 1.48) (7). It is in contrast, however, to a more recent report from southern Nepal where infants of mothers who were night blind during pregnancy had a 63% excess risk of 6-mo infant mortality (13). This association of night blindness with infant mortality was significantly reduced if the mother received either β-carotene or vitamin A as supplements during the index pregnancy (13). The discrepancy in the results of these 3 studies may be due to chance or a differential ability within study to control for potentially important confounding variables. In our study, we had only 27 and 71% power to detect RR of 1.25 and 1.50, respectively.

The association of maternal night blindness with lower birthweight and higher risk of low birthweight found in our study is supported by the only other study to examine this association (7). In the mountains of Nepal, there was a 73-g lower birthweight estimated for infants born to night blind women compared with mothers without night blindness. This compares to the unadjusted difference of 77 g found in our study. Adjustment for confounding factors reduced the difference in Nepal to 52 g and to 33 g in our study. The adjusted incidence of low birthweight (<2500 g) was ~10% higher in Nepal, similar to the RR of 1.13 found in our study. The association was stronger with more restrictive definitions of low birthweight in both studies. Similarly, fetal vitamin A status, as measured by cord serum levels, has been associated with birthweight and length (20–22), but cord blood levels vary with gestational age, suggesting that confounding may explain these results (23). Given that the majority of low birthweight in south Asia is related to intrauterine growth restriction, and the limited accuracy of our measure of gestational age in this study, we assume that the association observed with maternal night blindness relates to intrauterine growth restriction instead of prematurity. Maternal vitamin A deficiency was also associated with lower birth weight and early infant growth among HIV-infected mothers (24), supporting our observation of poorer attained growth at 6 mo of age among infants born to night blind women. The increased risk of morbidity observed in our study could explain this association with poorer growth. In contrast to these associations, randomized trials of supplementation of pregnant women with vitamin A in southern Nepal and Indonesia have shown no differences in birthweight, growth, or morbidity in the first few months of life (23,25) and trials in HIV-infected women in Malawi and Tanzania have had mixed results (26,27). However, these randomized trials were conducted on entire populations of women, not just those who were vitamin A deficient during their pregnancy, and the overall lack of impact on birthweight, growth, and morbidity may mask important effects in a deficient subgroup of women and their infants. Also, vitamin A deficiency is rarely an isolated nutritional deficiency and commonly occurs together with other deficiencies associated with diets low in fortified or animal source foods. Given the complex associations of nutritional factors with risk of mortality, the contrast between the observational data and the lack of impact in the supplementation trials may indicate that maternal night blindness is an indicator of broad nutritional deficits.

Like all observational studies, this study has limitations in the causal inferences that can be drawn between maternal night blindness and the adverse consequences to newborn infants. The use of a clinical indicator of vitamin A deficiency underestimated the true prevalence of poor vitamin A status in our study population (18,19). This misclassification would likely bias our findings toward the null, making our estimates of association conservative.

Although we have adjusted for a variety of confounding factors, the presence of residual confounding due to unmeasured factors associated with both maternal vitamin A deficiency and adverse newborn health cannot be disregarded. However, even if maternal night blindness is merely a marker for a constellation of factors that result in excess risk to the woman and her newborn infant, the ease of measurement of this parameter makes it a feasible marker for high risk populations and/or targeted intervention to improve reproductive and early infant outcomes. Given the likelihood that women who have night blindness in pregnancy suffer multiple nutritional deficiencies, interventions targeted to these high risk women should be comprehensive in their approach.


   FOOTNOTES
 
1 Supported by Cooperative Agreement No. HRN-A-00-97-00015-00 between the Johns Hopkins Bloomberg School of Public Health and the Office of Health and Nutrition, U.S. Agency for International Development, Washington DC, a grant from the Bill and Melinda Gates Foundation, Seattle, Washington, and commodity support from Task Force Sight and Life, Roche, Ltd., Basel, Switzerland. Back

2 Author disclosures: J. M. Tielsch, J. Katz, and C. Coles are members of the Sight and Life Institute at the Johns Hopkins Bloomberg School of Public Health, which is a recipient of a grant from Roche, Ltd. (now DSM, Inc.); L. Rahmathullah, R. D. Thulasiraj, S. Sheeladevi, and K. Prakash, no conflicts of interest. Back

6 Abbreviations used: ARI, acute respiratory illness; MUAC, mid-upper arm circumference; RR, relative risk. Back

Manuscript received 12 September 2007. Initial review completed 17 October 2007. Revision accepted 18 January 2008.


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 Introduction
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 Discussion
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