Mota, Denise M.*; Barros, Aluisio J.D.†; Santos, Iná†; Matijasevich, Alícia‡
Constipation is a frequent complaint in routine pediatric consultations and accounts for >20% of visits to pediatric gastroenterologists (1,2). Its prevalence varies from 0.3% to 8%, the variation being mainly due to using different definitions in describing the problem (Rome III (3,4), Paris consensus (5–7)). In Brazil, the prevalence rates of constipation are higher (17.5%–38.4%), but variable depending on the nature of population studied (8). The existing information on defining what constitutes proper bowel habits in children is limited (9,10). There are no cohort studies with longitudinal follow-up that characterize the age at which this problem begins to manifest itself.
The etiology of constipation is multifactorial and there is no unanimity of opinion on its relation to clinical course (11). Some authors consider that it is constitutional and disappears with age; others report that, even with treatment, 30% to 50% of children will have constipation until the age of 5, and some even during adulthood (12). Many families having adults with constipation believe that constipation is a family trait and not a serious problem. As a result, it is diagnosed late and often only after asking about the symptoms (12).
Functional constipation is defined as delayed or painful evacuation, which persists for ≥2 weeks to cause stress to the patient (2). In most cases, functional constipation is caused by painful defecation, creating a cycle. The child avoids evacuating because it is painful; the retained feces dries up and hardens causing discomfort and pain when defecating, thus perpetuating the cycle (13,14). Evacuation may be made painful by other factors such as dietary changes, intercurrent illnesses, stressful happenings, and inadequate sphincter control (difficulty in relaxing the external anal sphincter during defecation) (15).
The present study was aimed at evaluating the trajectory of bowel habits in the first 4 years of life in a birth cohort, estimating the prevalence of constipation and evacuation frequency, and describing stool characteristics.
The present study, based on a birth cohort, was started in 2004 in the city of Pelotas, Brazil. The mothers were interviewed during their hospitalization for childbirth, and their babies were measured (length and weight) and examined to assess gestational age.
The children were again sought when they turned 3, 12, 24, and 48 months; the mothers were interviewed and children's anthropometric measurements taken. Details of the methods followed for the study of Pelotas Birth Cohort Study 2004 are available in other publications (16,17).
In the present study, bowel habits of children were assessed, and the data used here relate to assessment of the segments of 12, 24, and 48 months. Children with a malfunctioning neurological system, or with cerebral palsy, and those forming part of multiple births, were excluded from the present study. During each visit, the mothers were asked to answer a questionnaire about their children's health, morbidity, feeding, sleep patterns, immunization, urinary and bowel habits, and their own health.
The following variables, related to the month preceding each interview, were used for assessing bowel habits: interval between evacuations, stool consistency (hard, soft, or firm), blood in stools, scybalous stools, pain or difficulty in evacuating, use of laxatives, and refusal to go to the bathroom.
When the child had daytime urinary control and refused to evacuate in the toilet or potty, it was considered a “refusal to go to the bathroom to evacuate.” Following modified Rome II criteria (3,4), functional constipation is defined as the presence of ≥2 of the following symptoms: hard stools, scybalous stools, evacuation with blood, difficulty in evacuating, interval between successive evacuations >72 hours, and the use of laxatives during the last 30 days. Rome III was not used because not all of the variables required had been collected. Toilet training was evaluated in terms of its commencement: before the age of 24 months, at the age of 24 months or later.
Introduction of cow's milk was considered in terms of “before the age of 1 month,” “between 1 and 2 months,” “between 3 and 5 months,” and “after 6 months.” Other variables used in the analysis were child's sex, maternal characteristics (education and age [in full years], parity, maternal paid work), and family socioeconomic level, based on the National Economic Indicator, with reference to quintiles for Pelotas (18).
The interviewers were specially trained for the purpose. To prevent possible fraud in the interviews and ensure quality control, 10% of the interviews were repeated at home through a reduced questionnaire and making use of telephone contact if the mothers had a landline or mobile telephone. Such repetition of the interviews satisfies the interviewer in confirming the content of the previous interview.
The analysis was performed using the program Stata 11 (StataCorp, College Station, TX). χ2 tests were used to compare prevalence rates according to categorical exposures and linear trend tests for ordinal exposures. Poisson regression was used to identify the risk factors for the occurrence of constipation at the age of 24 months and prognostic factors for its persistence up to the age of 48 months.
The study protocol was approved by the ethics and research board of the Medical School of the Federal University of Pelotas. Written consents were obtained from the participants in the study, after informing them of the objectives of the study and assuring them of confidentiality of the information.
The cohort for perinatal study consisted initially of 4231 children (0.8% losses and refusals). During the first 4 years of life, there were 94 deaths, 6.8% of losses, and 1.2% of refusals, and a total of 3799 children were evaluated at the age of 48 months (92% of the original cohort, excluding deaths). For this analysis, 7 children with meningomyelocele and 1 with cerebral palsy were excluded, besides 40 pairs of twins.
Table 1 shows that 14.7% of the children were premature and 10% low birth weight. Constipation was observed in 27.3% of the children at 24 months, in 30.8% at 48 months, and 13.6% of the children were constipated both at 24 and 48 months. Table 1 also describes the characteristics of the cohort of children at 4 years of age. The most common groups are the children of mothers ages between 20 and 29 years (49.4%), with 5 to 11 years of schooling (74.9%) and belonging to the first 2 reference quintiles of economic status (44.1%). About half of the children (49.5%) started receiving toilet training before the age of 2. Cow's-milk feeding was introduced before the first month of life in 15.2% of the children, and in the case of children between 1 and 2, 3 and 5, and 6 months of age or older in 34.6%, 13.7%, and 22.1%, respectively.
Child's sex, maternal age, education, and socioeconomic status show a direct association with the prevalence of constipation at 48 months. The age at which toilet training began was associated with prevalence of constipation at 24 months, but not at 48 months. Among the children who had started toilet training before 24 months, 29.2% had constipation at 24 months and 31.7% at 48 months, compared with 25.4% (P = 0.010) and 30.3% (P = 0.356), respectively, of those who began toilet training after 24 months. Evaluation of children, who were always constipated (at 24 and 48 months), shows that the prevalence was higher among those with training before 24 months (15.4% vs 12.0%, P = 0.004).
Table 2 describes the prevalence of constipation, stool characteristics, and symptoms related to bowel habits of constipated children, according to age and sex. The most prevalent symptoms at 24 and 48 months were scybalous stools and the need for straining at stool (difficulty to evacuate). The presence of feces in clothing was the most prevalent symptom at 24 months, which was reported by more than half the mothers of constipated children. Children who had been constipated since the age of 24 months used laxatives 4 times more when compared with those who were constipated only at 24 or 48 months. They usually used lactulose, tamarine herbal, mineral oil, or oral magnesium sulfate (data not shown).
Among the children with constipation at 24 months, 49.9% remained constipated up to 48 months. Among the nonconstipated children at 24 months, 23.6% were constipated for 48 months (P < 0.001), and the incidence during that period was different between the sexes (20.2% among boys, against 27.3% among girls, P < 0.001). The frequency of evacuations, with interval >72 hours, was 2.5% at 24 and 5.5% at 48 months of age. More than one-fourth of the children at 24 months (28.1%) with this trait maintained this habit even at 48 months. Among those who did not have such a long interval at 24 months, the prevalence was 4.9%. In terms of sex, boys maintained their habit in 35.9% of the children and girls in 22.0% (P = 0.148). Regarding the bowel habits studied, they were more frequently reported among girls at 48 months, with no difference between sexes at 24 months. The most common combinations of symptoms at 24 months, among both girls and boys, were evacuation difficulty and scybalous stools. The corresponding combinations, most prevalent at 48 months, were hard and scybalous stools (data not shown).
Table 3 describes the characteristics of the children who refused to evacuate, and those who did not. At 24 months, 48.3% of the children who did not wear diapers but controlled urine during the day (N = 1610) refused to use the toilet (or potty). At 48 months, this prevalence (N = 3651) decreased drastically (2.9%). Refusal to go to the bathroom was more prevalent among boys than girls at 24 months (56.0% vs 41.2%, P < 0.001), as well as at 48 months (4.2% vs 1.4%, P < 0.001). Refusal to use the toilet or potty at 24 months was not related to bowel symptoms. At the age of 48 months, refusal was associated with hard stools, evacuation difficulty, use of laxatives, and interval between successive evacuations >72 hours (Table 3).
Among the children who were off diapers before 24 months, 1.9% refused to go to the bathroom at 48 months and 3.9% in those who were off diapers at 24 months or later (P = 0.001). Among the children who were already off diapers at the age of 24 months, constipation at 24 months was more frequent than among those who were still on diapers (32.0% vs 25.8%, P < 0.001). At 48 months, this difference disappeared (29.1% vs 31.3%, P = 0.209). At 24 months, the presence of scybalous stools (52.5% vs 46.1%, P = 0.001), hard stools (24.8% vs 15.6%, P < 0.001), and interval >72 hours between evacuations (3.4% vs 2.2%, P = 0.039) were more common among children who were off diapers at 24 months (data not shown). All of these differences disappeared at 48 months.
Toilet training before 24 months of age was the only variable that was associated with the risk of constipation at 24 months after adjusting for other characteristics of mother and child. The prevalence ratio adjusted was 1.16 (confidence interval 95% 1.04–1.29, P = 0.008) (Table 4). The introduction of cow's milk before 1 year of age was associated with constipation at 24 months, and children who received cow's milk in the first month of life had a 24% greater risk than those who started after this age. To identify the prognostic factors that expose the children to the risk of constipation from 24 to 48 months, only those children who were constipated at 24 months of age were considered for analysis. Among these, after adjusting for the other characteristics of mother and child, only the socioeconomic status continued to remain associated (Table 4). Children from the richest quintile had 36% higher risk than those from the poorest quintile, considering the latter as the reference group (prevalence ratio 1.36; confidence interval 95% 1.11–1.66, P = 0.006).
In their first year of life, children constantly change, and it is at this stage that habits are learned and consolidated according to each culture. The normal frequency of evacuations has an inverse relation with age, stabilizing at approximately 4 years of age. Consultations with pediatricians and pediatric gastroenterologists are more frequent during this period when parents are more aware of bowel habits. The lack of standardization in the definition of constipation makes comparison of results difficult, and they are often conflicting. Chung et al (19) found that bowel habits in 31.3% of 5- to 13-year-old children, selected from schools, are inadequate. The most frequent among these were constipation (6.7% characterized by the frequency of evacuations and 11.8% using the Bristol scale) (20,21), pain in evacuation (15.8%), and fecal incontinence (7.8%) (19). In the present study, in which only the frequency of evacuations was used for the diagnosis of constipation, the prevalence was 5.5% at 4 years. Fecal incontinence was uncommon at 4 years of age as compared with that at 2 years of age, which is the learning phase of the child. This is thus an acceptable symptom within normal limits.
Wald et al (10) used a scoring system with 5 symptoms (<3 evacuations per week, bulky stools, maneuvering to hold for >25% of the time, fecal incontinence, straining at evacuation for >25% of the time) and reported that 10% of 5- to 8-year-old children, selected from pediatric services, had ≥2 of these intestinal symptoms.
In the present study, it was found that almost half of the children who were off diapers refused to use the toilet or potty at age 2 years, a habit that virtually disappeared at 48 months. This behavior is part of the child's normal development between 2 and 3 years of age, but inappropriate at age 4. It is important that the child is not punished or pressured during the phase of refusal (22–25). At 4 years of age, when this behavior was much less prevalent, refusal was associated with symptoms of constipation and changes in stool characteristics. Constipated children experience painful evacuations that lead to stool-holding maneuvers (avoidance of evacuation), thus perpetuating the cycle of uncomfortable bowel movements (7).
Toilet training is an important step in child development and the training must be proper and complete to avoid problems arising from inadequate training (26). A detailed description of the acquisition of sphincter control in the Pelotas 2004 cohort can be found in other publications (27,28). In the present analysis, toilet training started before the age of 24 months was associated with higher prevalence and greater risk of constipation, as well as changes in stool characteristics, which perpetuated up to the age of 4 years in about half of the children who were constipated at 24 months. Mothers should be advised regarding appropriate bowel habits, taking into account not only the interval between evacuations but also the characteristics of the feces, especially the scybalous stools, which is common in the present study.
The introduction of cow's milk before 6 months of age has been considered a risk factor for various morbidities during the first year of life, especially due to iron-deficiency anemia, constipation, and food allergies, which show increased prevalence (29). In the present study, children who did not use cow's milk before 1 year of age had a lower risk of constipation. These findings reinforce the guidelines and directives of the Brazilian Society of Pediatrics, which recommends only breast-feeding until 6 months of age and the avoidance of cow's milk during the first year of life (30).
The failure of parents and doctors in recognizing constipation can lead to chronic symptoms, defeating the very purpose of treatment (31). Identification of symptoms is important in routine diagnosis, as in the case of urinary symptoms (27).
1. Abi-Hanna A, Lake AM. Constipation and encopresis in childhood. Pediatr Rev
2. Baker SS, Liptak GS, Colletti RB, et al. Constipation in infants and children: evaluation and treatment. A medical position statement of the North American Society for Pediatric Gastroenterology and Nutrition. J Pediatr Gastroenterol Nutr
3. Caplan A, Walker L, Rasquin A. Validation of the pediatric Rome II criteria for functional gastrointestinal disorders using the questionnaire on pediatric gastrointestinal symptoms. J Pediatr Gastroenterol Nutr
4. Caplan A, Walker L, Rasquin A. Development and preliminary validation of the questionnaire on pediatric gastrointestinal symptoms to assess functional gastrointestinal disorders in children and adolescents. J Pediatr Gastroenterol Nutr
5. Benninga M, Candy D, Catto-Smith AG, et al. The Paris Consensus on Childhood Constipation Terminology (PACCT) Group. J Pediatr Gastroenterol Nutr
6. Bigélli RHM, Fernandes MIM. Constipação intestinal na criança. Medicina Ribeirão Preto
7. Catto-Smith AG. 5. Constipation and toileting issues in children. Med J Aust
8. Motta ME, Silva GA. Chronic functional constipation in children: diagnosis and prevalence in a low-income community. J Pediatr (Rio J)
9. Corazziari E, Staiano A, Miele E, et al. Bowel frequency and defecatory patterns in children: a prospective nationwide survey. Clin Gastroenterol Hepatol
10. Wald ER, Dio Lorenzo C, Cipriani L, et al. Bowel habits and toilet training in a diverse population of children. J Pediatr Gastroenterol Nutr
11. Di Lorenzo C, Benninga MA. Pathophysiology of pediatric fecal incontinence. Gastroenterology
2004; 126 (1 suppl 1):S33–S40.
12. Vives AC, Allue IP. Estudio caso-control de los factores de riesgo asociados al estrenimiento. Estudio FREI. An Pediatr (Barc)
13. Borowitz SM, Cox DJ, Tam A, et al. Precipitants of constipation during early childhood. J Am Board Fam Pract
14. Constipation Guideline Committee of the North American Society for Pediatric Gastroenterology, Hepatology and Nutrition. Evaluation and treatment of constipation in infants and children: recommendations of the North American Society for Pediatric Gastroenterology, Hepatology and Nutrition. J Pediatr Gastroenterol Nutr
15. van der Plas RN, Benninga MA, Taminiau JA, et al. Treatment of defaecation problems in children: the role of education, demystification and toilet training. Eur J Pediatr
16. Barros AJ, da Silva dos Santos I, Victoria CG, et al. The 2004 Pelotas birth cohort: methods and description. Rev Saude Publica
17. Santos IS, Barros AJ, Matijasevich A. Cohort profile: the 2004 Pelotas (Brazil) birth cohort study. Int J
18. Barros AJ, Victora CG. A nationwide wealth score based on the 2000 Brazilian demographic census. Rev Saude Publica
19. Chung JM, Lee SD, Kang DI. An epidemiologic study of voiding and bowel habits in Korean children: a nationwide multicenter study. Urology
20. Minguez Perez M, Benages Martinez A. The Bristol scale—a useful system to assess stool form? Rev Esp Enferm Dig
21. Pares D, Comas M, Dorcaratto D, et al. Adaptation and validation of the Bristol scale stool form translated into the Spanish language among health professionals and patients. Rev Esp Enferm Dig
22. Issenman RM, Filmer RB, Gorski PA. A review of bowel and bladder control development in children: how gastrointestinal and urologic conditions relate to problems in toilet training. Pediatrics
23. Blum NJ, Taubman B, Nemeth N. During toilet training, constipation occurs before stool toileting refusal. Pediatrics
24. Taubman B. Toilet training and toileting refusal for stool only: a prospective study. Pediatrics
25. Schmitt BD. Seven deadly sins of childhood: advising parents about difficult developmental phases. Child Abuse Negl
26. Mota DM, Barros AJ. Toilet training: methods, parental expectations and associated dysfunctions. J Pediatr (Rio J)
27. Mota DM, Barros AJ. Toilet training: situation at 2 years of age in a birth cohort. J Pediatr (Rio J)
28. Mota DM, Barros AJ, Matijasevich A, et al. Longitudinal study of sphincter control in a cohort of Brazilian children. J Pediatr (Rio J)
30. Ministério da Saúde. Newborn Health Care: A Guide of Health Professionals, Vol 4. Care of the Late-Preterm Infant [English title]. http://bvsms.saude.gov.br/bvs/publicacoes
. Published 2011. Accessed March 19, 2012.
31. Loening-Baucke V. Functional fecal retention with encopresis in childhood. J Pediatr Gastroenterol Nutr