SBBO may be asymptomatic or may present with chronic diarrhea associated with malabsorption of macronutrients. SBBO may thus lead to or aggravate protein-energy malnutrition.5,6 In children, SBBO has also been linked to recurrent abdominal pain that responded to antimicrobial treatment.41
Several disorders may predispose to the development of SBBO (Table 13.4). It is therefore crucial that in every child diagnosed with SBBO a careful work-up be performed, aimed at ruling out these underlying conditions.
We will focus here on SBBO associated with acute or persistent diarrhea and with environmental factors, given their high incidence and prevalence, particularly in young infants and in children living in unfavorable environments.
Table 13.4 Clinical conditions associated with small-bowel bacterial overgrowth
Anatomic abnormalities Congenital intestinal obstruction Acquired strictures and stenosis
(e.g. Crohn's disease) Intestinal fistula
Abnormalities of intestinal motility Pseudo-obstruction syndrome Scleroderma
Damage of the myenteric plexus
Post-surgery complications Stasis of the afferent loop Gastroenterostomy Enteroenterostomy
Without anatomic abnormalities Carbohydrate malabsorption Immunological deficiency Giardia infection Acute and persistent diarrhea Environmental enteropathy
Small-bowel bacterial overgrowth in acute and persistent diarrhea
In developing countries, these two conditions account for a major proportion of deaths in the early years of life, and it should be emphasized that mortality due to persistent infectious diarrhea is much greater than that due to its acute phase.44,45 SBBO does occur in children with acute diarrhea and is considered one of the factors leading to its perpetuation. In the 1970s, Fagundes-Neto et al46 and Albert et al47 showed a raised incidence of SBBO in children with acute diarrhea. A later study by Penny et al48 showed that SBBO was more frequent in children with persistent diarrhea (80%) than in acute diarrhea (40%). In a study carried out in Cuba, Cristia et al49 observed a similar frequency of SBBO in unweaned infants who had been hospitalized with acute and persistent diarrhea. From a functional point of view, Coello Ramirez and Lifschitz50 found a correlation between SBBO and malabsorption of carbohydrates.
Studies in Brazil31,32,42 and in other countries48 have shown an association between SBBO and severe acute diarrhea or persistent diarrhea caused by classic enteropathogenic Escherichia coli.
SBBO can thus be present in both acute and persistent diarrhea, aggravating the clinical manifestations of patients, and, in conjunction with other factors, prolonging its course. Being aware of this possibility is obviously necessary for proper and timely diagnostic and therapeutic interventions.
Small-bowel bacterial overgrowth in environmental enteropathy
In the 1960s, several studies in tropical countries showed that adults without clinical gastrointestinal manifestations presented histological changes in the small intestine and reduction of D-xylose absorption capacity, compared to healthy adults living in developed countries.51,52 With regard to morphology, the abnormalities observed in the small intestine were reduced height of the intestinal villi and increased lymphoplasmocytic infiltrate in the lamina propria. The disorder was initially named tropical enteropathy. However, the possibility of a spontaneous normalization of the defect in D-xylose absorption after a change of environment, as observed in Indians and Pakistanis who moved to New York,53 its close link with unfavorable environmental conditions, as well as the occurrence of this disorder in nontropical regions, led in the 1980s to a redefinition of this clinical condition as 'environmental enteropathy' by Fagundes-Neto et al.54,55 Environmental enteropathy can thus be defined as a set of unspecific morphological and functional abnormalities of the small intestine that are potentially reversible with a change in environmental conditions. From the clinical standpoint, it may be asymptomatic or associated with chronic diarrhea or with recurrent bouts of diarrhea. Stunted growth and protein-energy malnutrition often occur, as a result of the combination of malabsorption and inadequate nutrition, related to under privileged socioeconomic conditions. Environmental enteropathy may be associated with. SBBO. The high prevalence of SBBO in this disorder was confirmed by studies on slum-dwelling infants in the city of São Paulo,56,57 including 40 unweaned infants without diarrhea but presenting blunted D-xylose absorption and histological abnormalities of the small intestinal mucosa. SBBO was found in 61.2% of such infants. Study of the intestinal ultrastructure in these patients showed several abnormalities, such as decreased number and fusion of microvilli, cytoplasmic vacuolization and derangement of the mitochondria and endoplasmic reticu-lum. Taken together, these data56,57 showed that exposure to unsuitable environmental conditions can damage the intestinal digestive-absorptive functions.
Use of the hydrogen breath test with lactulose to characterize SBBO has enabled research into environmental enteropathy in larger numbers of children, leading to a social vision of the threat that SBBO represents to the infant population. Pereira et al58 studied 340 children under 5 years of age and found SBBO in 27.2% of this population in a town in Australia.
In Brazil, several studies have been performed using the hydrogen breath test with lactulose to characterize SBBO associated with environmental enteropathy. One such study59 involved 83 schoolchildren who lived in a rural area, an urban area and a slum (favela) area of a city in the interior of São Paulo State, south-east Brazil. SBBO was detected in 7.2% of the children investigated. In the same study, the proportion of SBBO in the slum-dwelling children (18.2%) was statistically higher than that of the non-slum-dwelling children, in whom SBBO was not identified. These data thus demonstrated an association between unsuitable environmental conditions and SBBO.39
Two studies performed in 5-10-year-old children are also of interest. The first60 was carried out in Indian children living in a reservation in Mato Grosso do Sul and found SBBO in 11.5% of the 252 children studied. The second61 compared 50 slum-dwelling children with 50 control children who lived in domiciles with adequate food and environmental conditions and came from families with a solid socioeconomic background. SBBO was investigated by means of the hydrogen breath test with lactulose (10g) on one day and then with glucose (50g) on the next. After excluding non-hydrogen-producing children, SBBO (increase of 20 ppm in hydrogen concentration in the first hour after ingestion of lactulose) was observed in 50.0% (23/46) of slum-dwelling children and in 2.2% (1/46) of control children. The hydrogen test with glucose did not enable characterization of greater frequency of SBBO in slum-dwelling children. Figure 13.3 displays the curves based on the average concentrations of hydrogen in exhaled air, showing that production of hydrogen in slum-dwelling children was greater than in the control group, indirectly indicating a greater quantity of lactulose-fermenting bacteria. On the other hand, the glucose test did not draw a distinction between the groups. The average (± SD) of the z-scores of weight for age (-0.45 ±0.95) and height for age (-0.66 ± 1.05) of the slum-dwelling children were lower than those of the control group (+0.39 ±0.97 and +0.18 ± 0.84, respectively); the difference was statistically significant and showed an association between SBBO and protein-energy malnutrition.61
The evidence presented shows that unfavorable environmental conditions with lack of basic sanitation or inadequate supply of treated water can prompt the consumption of contaminated water and food that cause episodes of acute infectious diarrhea. This chronic state of environmental aggression may then cause long-lasting abnormalities of intestinal function that by inducing environmental enteropathy, ends up by negatively impacting the health of a large portion of the world population.
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