Prevalence of non-communicable diseases in Brazilian children: follow-up at school age of two Brazilian birth cohorts of the 1990's

The study was based on two birth cohorts, one initiated in Ribeirão Preto in 1994 and the other in São Luís in 1997-98, and on follow-up studies conducted in RP in 2004/05, when the children were 9-11 years old and in SL, in 2005/06, when the children were 7-9 years old. Ribeirão Preto is a city in the state of São Paulo, located in the Southeast, a rich and industrialized region. It had a population of 461,427 inhabitants in 1994[9]. Its Municipal Human Development Index was 0.855 in 2000[6]. São Luís is the capital of Maranhão state, located in the Northeast, one of the poorest regions of the country. It had a population of 781,068 inhabitants in 1997 [10]. Its Municipal Human Development Index was 0.778 in 2000[6].

A total of 2923 infants born at 10 maternity hospitals of the city over a four-month period (April-August 1994) were included in the first stage of the Ribeirão Preto cohort study, representing 99% of all live births. Losses represented less than 5% of all births. Excluding twins, the final sample consisted of 2858 births to residents of the city [9].

The first phase of the São Luís cohort study was conducted from March 1997 to February 1998, using systematic sampling stratified by the number of births at 10 public and private maternity hospitals in the city. In each hospital one out of seven children was randomly selected, including 2541 hospital births (live births, stillbirths and singletons or multiple births of mothers living in the city). The sample was representative of births in the city because hospital births accounted for 96.3% of the total. After exclusion of multiple births (n = 50) and stillbirths (n = 48), the final sample consisted of 2443 births. Losses due to refusal or inability to locate the mother occurred in 5.8% of cases [10].

In the two cohorts, anthropometric data and information on pregnancy, childbirth and postpartum were collected at birth through a standardized questionnaire answered by the child's mother.

Five birth weight groups were considered for the follow-up study: very low birth weight (VLBW <1500 g), low birth weight (LBW - 1500 to <2500 g), insufficient birth weight (2500 to <3000 g), normal birth weight (3000 to <4250 g), and children whose birth weight was at least two standard deviations above the population mean, who were classified as high birth weight (HBW ≥ 4250 g). The students in these weight groups with a smaller number of infants (VLBW, LBW and HBW) were oversampled in order to increase the study power.

Children were traced at schools, or using the addresses supplied by the mother at birth and by media advertising. All parents or guardians of children in the groups of VLBW, LBW and HBW and a fraction of one out of three children in the groups of normal and insufficient birth weight were eligible and were invited to participate by telephone or mail. In Ribeirão Preto, after excluding deaths in the first year of life (n = 48), 1150 children were eligible for follow-up. The follow-up rate was 68.7% (169 LBW, 28 HBW and 593 normal and insufficient birth weight). A total of 790 children participated in the follow-up (Figure 1). In São Luís, excluding 65 deaths in the first year, 2378 children were alive at one year of age. Thus, 673 of 926 eligible children participated in the follow-up study (72.7% of the original target group, 81 being LBW, 19 HBW and 573 being of normal and insufficient birth weight) (Figure 2). Follow-up losses occurred due to migration, impossibility to locate the children, children not enrolled in school, and school or parental refusal.

Since mortality was very high among children weighing less than 1500 g and ≥ 4250 g, a non-random additional sample was recruited, for a total of 132 children in SL and 79 in RP. Only children whose birth weights and gestational ages could be confirmed by inspecting hospital records or child health cards were included. Thus, the total sample included 1674 children, 869 from RP (Figure 1) and 805 from SL (Figure 2). The additional sample will only be included in selected studies to test hypotheses concerning groups of very low and high birth weight.

A sample of 673 children (SL) and 790 (RP) has a 90% power to detect a minimum difference of 10% in the prevalence of the different conditions studied (estimated at about 50%, which is the prevalence that yields the maximum sample size) between the exposed and unexposed groups, with a 5% probability of type I error.

A standardized questionnaire was applied to parents or guardians of children from the two cohorts, containing demographic questions and questions regarding general and oral health of the children. The questionnaire included variables concerning bruxism, nonnutritive sucking habits, recurrent abdominal pain and daily time spent in some sedentary activities. Cognitive function, mental health problems and childhood depression were also evaluated. Anthropometric examination was performed, and weight and height were measured. The questionnaire administered by the International Study of Asthma and Allergies in Childhood (ISAAC), translated and validated to assess asthma symptoms, was applied [14]. The assessment of asthma, bronchial hyperresponsiveness (methacholine challenge test) and skin tests for allergens was performed in a non-random subsample drawn by convenience. For each child of low birth weight two children of normal birth weight were included. The subsample included 328 children in RP and 330 in SL, corresponding to 41.5% and 49.0% of the original samples, respectively.

We used the Raven Colored Progressive Matrices Test, standardized for Brazilian children, which assesses general aspects of nonverbal intelligence, based on the multifactorial theory of Spearman [15]. It consists of five sets of 12 problems to infer the relationship between matrices. The sum of correct responses provides the overall score. It does not require reading and writing skills. The most satisfactory method of interpreting the overall score is by calculating the person's percentile by comparing his/her score to that attained by people of the same age and by identifying his/her relative position. This method makes no a priori assumption that the development of intellectual capacity is necessarily uniform or symmetrically distributed in childhood [15]. We calculated the prevalence of cognitive function below average or considered poor (≤ 25 percentile).

This is a maturity assessment that takes into account evolutionary and emotional indicators present in graphic production. It is also an indicator of cognitive development. It has been standardized by Wechsler in Brazil [16] and involves a simple activity - the drawing of a person using pencil and eraser. The standardized scores are converted to percentiles. We calculated the prevalence of below average, borderline or poor (below the 25th percentile) HFD.

The Strengths and Difficulties Questionnaire (SDQ) was proposed by Goodman in 1997 [17] for screening behavioral problems of children and adolescents between 4 and 15 years of age. It can be answered by parents/guardians, teachers or the adolescents themselves. In the present study a version of the questionnaire answered by parents was used. The questionnaire, aimed at identifying mental health problems, is composed of four subscales: emotional symptoms, conduct problems, hyperactivity/attention deficit, and peer problems. Scores are assigned to each of these scales (0, 1 or 2 as false, true or somewhat true). Then, a total score ranging from 0 to 40 is assigned at the end. According to the score, each scale is classified as normal, borderline or abnormal [17]. The presence of mental health problems was identified when the total score was greater than 16, which is considered abnormal [17]. The questionnaire was adapted and validated for Brazil [18].

It was measured by the Children's Depression Inventory (CDI). It is a screening instrument based on self-report prepared by Kovacs in 1981 which includes 27 items with three response options to be answered from 7 years of age onwards. The child selects the answer that best describes how he/she feels. It was adapted and validated by Gouveia et al. for Brazilian school children [19]. To each item 0, 1 or 2 responses are assigned, according to the order of the answers - 1st, 2nd or 3rd, respectively. Then the items are summed to obtain the total score. The score from which the child was considered to be "depressed" was less than 17 points, according to a Brazilian study [19].

Parents were asked whether the child used a bottle, pacifier or sucked its finger ever in life. Finger sucking and pacifier use were considered non-nutritive sucking habits. Bruxism corresponded to the habit of grinding or clenching the teeth and was considered to be present if observed during sleep or when the child was awake; current bruxism was identified when parents or guardians reported that the habit had persisted until the day the interview took place.

Primary headache was considered to be present when the mother reported that her child presented ≥ 2 episodes of headache in the two preceding weeks, without any associated organic symptoms, no matter how long or intense they were or where in the head they were located. This criterion was established according to the International Classification of Headache Disorders guidelines [20].

Recurrent abdominal pain was considered to be the occurrence of pain or discomfort in the stomach in the last three months, strong enough to disrupt the child's daily activities such as playing, going to school or sleeping [21].

The presence of symptoms of current asthma was investigated by adapting the questionnaire used in the asthma module of the ISAAC study [22]. The airway responsiveness was measured by the methacholine challenge test (bronchoconstrictor stimulus). The child inhaled methacholine at increasing concentrations, which started at 0.03 mg/ml and were successively doubled up to 16 mg/ml. The test was terminated when there was a decrease of 20% or more in forced expiratory volume in one second (FEV1) or when the last concentration of the protocol was reached. PC20, which is the concentration of methacholine causing a 20% fall in FEV1, was calculated. If PC 20 ≤ 2 mg/ml, the test was considered positive. Responsiveness was considered borderline if PC20 >2 to 16 mg/ml and normal if PC20 >16 mg/ml. For the examination the persons responsible for the children were instructed not to give the child tea, coffee, chocolate or soft drinks within 6 hours before the exam. To avoid false-positive results, the test was rescheduled if the child had had airway infection in the previous four weeks.

Asthma was considered to be present when subjective (symptoms of current asthma, or wheezing in the last 12 months) and objective criteria (presence of bronchial hyperresponsiveness) were present simultaneously or, by other definition, when subjective symptoms were reported alone.

Skin tests for allergy were applied by the puncture technique by trained personnel. We used the following allergens: 3 dust mites (Dermatophagoides pteronyssimus, Dermatophagoides farinae and Blomia tropicalis), cat, dog, two types of cockroaches (Periplaneta americana and Blatella German), pollen and four fungi (Alternaria alternata, Cladosporium herbarum, Aspergillus fumigatus and Penicillium notatum). The result was considered positive when the wheal size was over 3 × 3 mm with hyperemia.

Height and weight were measured, with the children barefoot and wearing light clothing, using standard techniques [23]. The instruments used were a precision scale calibrated periodically for measuring weight and an anthropometer for measuring standing height. For the assessment of nutritional status two references were used. The criteria proposed by the International Obesity Task Force (IOTF), based on data from six countries, including Brazil, used cutoffs of BMI for each age and sex, corresponding to cutoff points for overweight and obesity in adults [24]. For low weight the cutoff point <17 kg/m² was considered [25]. According to the American reference, children were considered underweight if BMI for age and gender was ≤ 5th percentile, overweight if BMI >P85 and ≤ P95 and obese when BMI > 95th percentile [26].

Blood pressure was measured three times with a digital sphygmomanometer, with cuffs adjusted for arm circumference. The measurements were performed by the same person, at 15-minute intervals with the participant resting in the sitting position, with his left arm at heart level. We calculated the average of the last two measurements. Hypertension was defined as systolic blood pressure and/or diastolic blood pressure equal to or greater than the 95th percentile for age, sex and height [27].

To assess the time spent in sedentary activities, the children reported the average daily time spent watching television, playing videogames or using the computer. Average daily time spent in some sedentary activities was divided into the following categories: 0 hours, up to 4 hours, more than 4 to 8 hours and over 8 hours.

The other variables considered were gender (male and female), child's skin color as reported by the mother/guardian (white, black, brown/mulatto and yellow/indigenous), monthly family income (<1, 1 to <4, 4 < 10 and 10 or more minimum wages), occupation of household head (non-manual, skilled manual and semi-skilled, unskilled/unemployed), maternal schooling in years (0-4, 5-8 and 9 or more years), maternal and paternal schooling in years (0-4, 5-8 and 9 or more years),performance of domestic chores by the child, and child labor (if the child perfomed some paid work outside the home, yes/no). For some variables, missing values were also presented.

Due to the complex sampling design, children with birth weights <1500 g, 1500 g to 2499 g and ≥4250 g were overrepresented in the sample. Therefore, the prevalence estimates and their standard errors were weighted using the svy set of commands in Stata. The weighting took into account the different probabilities of selection of each of the five groups of birth weight and preterm birth. Stratification of the sample by birth weight was also taken into account. We used the chi-square test for comparison of proportions between the two cohorts and to assess differences in the percentage of follow-up according to maternal age, schooling and marital status, parity, and child's sex.

The reasons for the study and its methodological procedures were explained to the parents or guardians. After accepting the participation of their children in the research, they signed the consent form according to the guidelines and standards regulating research involving human subjects of the National Health Council, resolution 196/1996. Study participants were guaranteed the right to interrupt the study at any time, access to the results, confidentiality of the results, guidance and referral to specialized evaluation when necessary. The project was approved by the Research Ethics Committee of the University Hospital, Federal University of Maranhão (protocol number 3104-476/2005) and the Research Ethics Committee of the University Hospital, Faculty of Medicine of Ribeirão Preto, University of São Paulo (protocol number 6828/2004).