Introduction

From the birth up to the adolescence, painful syndromes occur. These pain complaints affect a significant number of children, causing suffering to them and to their relatives, and still requiring social expenses. During the 1st year of age, colic predominates; in preschool children, the "growing pains" are the most frequent ones; between 4 and 12 years of age, abdominal pain is frequent; and among adolescents, cephalea is the most common complaint of pain (1).

New organic causes of recurrent abdominal pain have been identified. Information about the digestive tract motility in childhood start to disseminate. It is established that the pain has a nociceptive component (nervous structures that receive and transmit pain), and an emotional component (mental state), both influenced by genetics, individual experiences, and cultural environment. The knowledge of biopsychosocial influences on the child and on recurrent pain has increased (2). These acquisitions allow the arousal of new diagnostic and therapeutic approaches to recurrent abdominal pain in childhood. Recurrent abdominal pain is not only a symptom, but a distinct pediatric entity.

Definition and classification

Recurrent abdominal pain in children is defined as the occurrence of three or more episodes of pain in the abdomen within a period of 3 months or less. Such episodes are severe enough to interrupt routine activities. The patient remains asymptomatic between the pain crises (3,4).

Recurrent abdominal pain is the most common cause of recurrent pain among school children. It may have organic or functional origin. The latter is defined when no anatomical, infectious, noninfectious/inflammatory, or biochemical cause is established for the pain(5). Since the etiology and pathogenesis of functional recurrent abdominal pain are not established, and since there are no specific markers, it consists of an exclusive diagnosis, based on a detailed clinical history, on an detailed physical examination, and on few laboratory tests (6,7). Recurrent abdominal pain may be manifested as isolated paroxysms of periumbilical pain, as pain in the abdomen, pain with dyspepsia, and abdominal pain with dysfunction of the digestive tract. Signs and symptoms of dyspepsia include nausea, vomiting, regurgitation, pyrosis, early satiety, hiccups, and abdominal discomfort. The manifestations of dysfunction of the digestive tract include diarrhea, constipation, and the feeling of incomplete defecation. Out of the cases of recurrent abdominal pain, 75% are functional, with isolated paroxysms of pain around the umbilicus; 20% present manifestations of dyspepsia or dysfunction of the digestive tract. Only 5 to 10% of the children with recurrent abdominal pain present organic cause (6,8).

Epidemiology

Several studies show that recurrent abdominal pain affects 10 to 18% of children between 4 and 16 years of age. These variations are due to geographic and racial differences, as well as diagnostic criteria. Other 15% of school children and adolescents present episodes of abdominal pain for a period longer than 3 moths, but without the compromising of routine activities (6). Girls are more affected, in a proportion of 1.5:1 in relation to boys. It usually starts at 4 years of age, and presents a constant increase in the number of cases between 4 and 5 years, with a decrease after this age in boys, and a significant increase in the number of new cases among girls up to 10 years of age (3). Determining the beginning of recurrent abdominal pain is important for the prognosis. The early appearance of pain is associated with its bad evolution.

Etiology and pathophysiology of functional recurrent abdominal pain
In the etiology and pathophysiology of functional recurrent abdominal pain, factors such as genetic predisposition, autonomic nervous system, stress, and inflammatory process of the digestive tract should be considered. Since there are patients who present concomitant manifestations of dyspepsia and abnormal bowel movements, it seems that several painful manifestations are due to the same process. Controlled studies did not show any relationship between emotional alterations and recurrent pain (9,10). Psychic alterations are not primary causes of functional recurrent abdominal pain, but emotional processes obviously work as pain-intensifying factors.

In the families of children with functional recurrent abdominal pain, the report of pain complaints, such as peptic ulcer, irritable bowel, and migraine, are frequent; this suggests genetic predisposition to pain and functional compromising in these patients. The presence of cephalea, paleness, and dizziness in these children reveals the autonomic nervous system involvement in the process. Stressful, physical, and psychosocial factors usually cause the pain crises. The extrinsic nerves of the bowels, and/or the central nervous system probably have their roles in the threshold of the pain perception. A discrete and unspecific inflammatory process is found in all the digestive tract of children with functional recurrent abdominal pain, which is a cause or a consequence of the altered intestinal motility. This inflammation affects endocrine and neural functions that influence immunologic processes. The immunocompetent cells that are located in the intestine secrete cytokines and inflammatory mediators that act in the enteric neurons. The intestinal and central nervous systems modulate the immunologic response through neurotransmitters and neuropeptides that affect the lymphocyte function. These inter-relations have implications in the functional recurrent abdominal pain (6,11).

The pathogenesis mostly accepted in the present days for functional recurrent abdominal pain consists of alterations in the gastrointestinal motility and/or visceral hypersensitivity. The specific pattern of intestinal motor alterations during functional recurrent abdominal pain has not been determined yet. Studies in heterogeneous groups of adults with functional recurrent abdominal pain show an increased intensity of intestinal muscular contraction and increased transit. Few controlled studies in children show increased intestinal transit, exacerbated colonic motor response to pharmacological stimulation, and great-amplitude duodenal contraction (6,12,13).

The increase in the visceral pain sensitivity in children with functional recurrent abdominal pain is suggested by studies carried out in adults with irritable bowel who show a decrease in the pain threshold in all segments of the digestive tract (14-16). The improvement of recurrent pain with the withdrawal of the diet of gas production operators (lactose, fructose, sorbitol), which provoke the distension of the digestive tract, or of the diet of fatty acids, which modify the enteric motility, point out to alterations in the visceral sensitivity or in the intestinal motility, which are present in the functional recurrent abdominal pain (6,17,18).

A recent study with children presenting functional recurrent abdominal pain showed a decrease in the pain threshold induced by pressure in all the body surface; this study suggests the compromising of the central nervous system at these patients' pain perception. The decreased pain threshold would predispose or would start the pain crises (19).

Factors that intensify functional recurrent abdominal pain

Children with functional recurrent abdominal pain usually present a bad adaptation to the painful process. These factors that intensify the crises are of environmental, behavioral, and emotional origin, and make the children feel more pain, or predisposing them to new episodes of pain.

Environmental factors
Patients with functional recurrent abdominal pain do not know about the etiology and prognosis of the pain crises. They maintain expectations that the pain will improve. They are unable to avoid new episodes of pain, and they do not dominate the techniques that could make the pain milder. As a consequence, an increase in the emotional stress occurs, predisposing to a higher pain perception. Little knowledge about pain makes the parents attribute the cause of the crises to certain external factors, such as foods, environmental conditions, and routine activities of the child's life. The anxiety of the child when facing these false causative factors provokes the onset or the aggravation of the pain. The patient starts to present a phobic behavior, with restrict social and school activities, and his/her life becomes different from other children's. These stress creates or intensifies the
episodes of pain (20).

Behavioral factors
What children know about pain comes from their own experience, from the knowledge received from their parents, relatives and from the society in general. They learn how to communicate the crises with words and behavioral changes, and acquire techniques to relieve the painful process. Usually, the parents do not know how to deal with the pain, and respond ambiguously to the crises. Sometimes, they have great physical and emotional care. In other episodes, they suggest that the patient is the only responsible for the pain handling. The child understands that the painful manifestations should be communicated with exaggerated attitudes, in order to receive a better parental support. This behavior maintains the pain. The parents also encourage the child not to go to school after crises, resting instead, to avoid physically stressful activities, to skip social compromises, to avoid doing unpleasant activities. They dismiss the child of familial responsibilities. So, there are secondary benefits that start or prolong the painful process. The child becomes frustrated, isolated, and anxious. He/she acquires passive attitudes towards the pain, and this passivity intensifies the painful perception. All these learning processes are going to maintain and intensify the functional recurrent abdominal pain (20).

Emotional factors
The recurrent pain is aversive, causing prolonged stress in the patient and his/her family. The child becomes anxious, frustrated, angry, sad, and depressed. These emotions intensify the stress that starts or maintains the pain, creating a vicious circle: pain - emotional stress - pain (20).

The child with functional recurrent abdominal pain presents great expectations about him/herself in several aspects (school, family, and sports). He/she desires high patterns of performance, even already having an adequate performance. Consequently, he/she gets frequently frustrated, and this increases the risk for developing somatic manifestations of stress (20).

To sum up, children with functional recurrent abdominal pain do not present accuracy in understanding the disease, but maintain a limited control over it; they do not know the results of treatment and prognosis; they present behavioral disorders and an elevated level of anxiety and fear. These stressful factors predispose to a change in the pain perception, making life become limited of low-quality, and causing familial suffering.

Functional recurrent abdominal pain with isolated paroxysms of periumbilical pain

In this type of functional recurrent abdominal pain, the episodes of pain last for less than 1 hour in 50% of the children, and for less than 3 hours in 40% of them. Time is longer in the remaining cases. Pain varies in severity and frequency in the same patient. The child indicates the umbilical region as the place where the pain is more intense. There is no report of pain irradiation. Relationships between the pain episodes and time, food, activities and intestinal habits are rare. The paroxysms do not occur during sleep, but they may prevent a child from sleeping. During the most intense crises, associated signs and symptoms may occur: cephalea, paleness, nausea, vertigo, prostration and mild fever (37.2 ºC to 37.7 ºC). Motor signs for the relief of the pain are also observed, such as bending the body over the abdomen, or compress it with the hands (4,21,23).

Between the crises, the child does not present complaints or alterations on physical examination. In the retrospective history, reports of colic, gastroesophageal reflux, anorexia, changes in milk formulas, fear, sleep disorders, nocturnal enuresis, and difficulty in school are common. In the familial history, reports of psychophysiological symptoms and functional diseases, such as spastic bowel, irritable bowel, mucosal or spastic colitis, as well as marital problems, quarrels among brothers, recent diseases in relatives or other conflicts are also frequent. When examining the patients' personality, we find hyperactive, overdemaning patients, as well as those with intolerance to frustration. They are "good children" in terms of attitudes, behavior and maturity. They undertake more responsibility in relation to the age group. They are aggressive with the adult's lack of sensibility towards their disease, hardly tolerate criticism, and feel constant fear (4,9,24-27).

The causes of functional recurrent abdominal pain with isolated paroxysms of periumbilical pain are listed in Table 1. A positive diagnosis of functional presentation is carried out when the following findings are present:
a) Onset of pain between 4 and 16 years of age;
b) Frequency of the process with at least three episodes of pain in a period not inferior to 3 months;
c) Periumbilical pain crises without irradiation;
d) Normal physical examination, including rectal touch;
e) Factors that reinforce the painful behavior present in the environment;
f) Normal laboratory exams: hemogram, erythrocyte sedimentation rate, urine routine and culture, parasitological examination of feces, presence of blood in feces, abdominal simple radiography, and ultrasound.

Table 1 -
Causes of recurrent abdominal pain with isolated paroxysms of periumbilical pain

The hemogram orientates about the presence of infections and hemolytic anemias. An altered erythrocyte sedimentation rate points to inflammatory diseases. Urine exams suggest infections or calculi. Parasitological examination of feces should be performed due to the high prevalence of parasites in our setting. The presence of blood in the feces points to intestinal inflammatory diseases. Abdominal X ray and ultrasound show the presence of renal and biliary calculi, anatomical malformations, and mainly occult constipation. A diagnostic approach of functional recurrent abdominal pain with isolated paroxysms of periumbilical pain is shown in Figure 1.

There are alert signs and symptoms that suggest the organic origin of isolated paroxysms of abdominal pain, such as loss of weight, impaired growth, pain distal from the umbilical region, pain that awakes the child during the night, extraintestinal manifestations (fever, skin eruptions, articular pain, recurrent aphthae, and dysuria), presence of blood in feces, chronic diarrhea, anemia, elevated erythrocyte sedimentation rate, and familial history suggestive of ulcerous or inflammatory disease at the digestive tract (3,4). The presence of these alterations, associated with other more specific ones of organic causes, orient to the specific prognosis (Table 1).

The treatment of functional recurrent abdominal pain should emphasize emotional factors through talks to the family, using a positive approach while the problem is exposed. As the transition from the organic to the functional focus occurs, the patient will feel relieved of pain, and will not need further cognitive-behavioral interventions. The first and most important step is the obtainment of a detailed history. In order to achieve this objective, it is necessary to let the family and the child talk; their bodies, their gestures, their voices have to be observed. Group and individual interviews with the parents and the child are essential components of this process. Details about the pain, about the familial, social, and school environment, and about familial and personal antecedents are important in order to compose the diagnosis. The pediatrician should try to identify why the seek for medical care happened at that exact moment of such a chronic process as recurrent abdominal pain, why the parents, and eventually the child, elected that specific episode of pain to set an appointment. Still, the pediatrician should value each episode of pain as being acute, considering that a child with recurrent abdominal pain is not free from developing an acute disease, such as appendicitis, for example. The treatment of functional recurrent abdominal pain, which starts at the first appointment, aims to:

a) clarify to the parents the authenticity of the pain. It is not a case of simulation or imagination, but real pain.

b) Introduce the concept of functional disease.

c) Explain the possible role of alteration in the digestive tract motility and of the visceral sensitivity in the genesis of the pain.

d) Orient about the relation between central nervous system, motility, and intestinal sensitivity. The painful behavior should be explained by the perspective of a social learnship.

e) Show the benignity of functional recurrent abdominal pain.

f) Tranquilize relatives and the child about the possibility of serious organic diseases.

g) Introduce the concept of causative factors in the onset of crises in functional diseases.

h) Diagnose the possible factors of the child's behavior that cause or aggravate the pain status.

i) Condemn secondary benefits of the recurrent pain, such as gifts, privileges, and more familial attention.

j) Advice the parents so that they ignore the nonverbal painful behavior, and direct the child to some other activity when there is a verbal communication of the pain. If the child agrees, he/she should receive compliments, and possible new complaints should be ignored. The parental care will be firm and discrete. The pain crises should not subvert the familial dynamics.

k) The patient's life should be normal. The activities should only be interrupted at the moment of the crisis. This is valid both in the familial and in the social and school environment. After the crisis, life has to go on. Behavioral effort will be made during the days without pain. They will be registered, for example, in a calendar, and for a given number of days in the week without painful behavior, a reward can be given to the child. This procedure will be periodically reviewed during the entire treatment, aiming at increasing the number of days free from pain for new rewards. The use of a scale to evaluate the intensity of the pain, such as the color scale, allows the patient to verify his/her progresses objectively.

l) Teach the patient techniques that decrease the intensity of the pain during the crises, deviating the attention from the pain perception. Examples are whistling, singing, jumping, running, clicking fingers, counting or making mathematical calculations mentally. Relaxation techniques should be also taught aiming at decreasing the pain, such as sitting, writing, walking, and lying in a pleasant position. If the crises do not improve, the self reinforcement, with positive self-verbalization, may be used. If the pain still persists, imaginative strategies should be used: for example, the pain is being destroyed by a hero, or the patient imagines he/she is in pleasant situations.

m) Clarify what the alert signs are, showing the importance of the immediate communication with the doctor when such signs are observed (27,28).

These procedures aim at decreasing both the parents' and the patient's anxiety, and mainly at condemning behaviors and situations that cause, maintain or intensify the pain perception (27,28). A study using these procedures showed that 87% of the children were free from the pain within 3 months. In a control group, where the conventional treatment was performed, only 37.5% of the patients remained asymptomatic (29).

The child should attend periodical appointments, mainly during the first 6 months, so that the concepts of functional recurrent abdominal pain, as well as the ways to handle the pain, are reinforced and clarified. In these appointments, it is possible to verify if the secondary benefits, causative factors, alert signs and symptoms, as well as other findings that suggest organic disease are still present. So, it consists of an active observation of the patient, his/her family and setting.

The psychiatric treatment is only indicated when the child internalizes the painful behavior in an extreme way (depression, anxiety, and low self-esteem, or when conversion symptoms are verified), when he/she is not able to take a normal life even after the harmful factors are no longer present, or when the family is not able to handle the painful process (6).

The continuous use of drugs (anticholinergic, antispasmodic, anticonvulsant) in the treatment of functional recurrent abdominal pain has not proven benefic; on the contrary, it has shown to maintain the painful process. The use of drugs in children with functional recurrent abdominal pain intensify the hypochondriac state and the drug dependence (6).

One only randomized, double-blind, placebo-controlled study showed a reduction of 50% in the pain crises after the inclusion of fibers in these children's diet (30). These results were not published. Sometimes, the decrease of sugars (lactose, fructose, sorbitol, and amide) in the diet shows some improvement in the crises (6,17,18). The fermentation of carbohydrates probably produces the gas that distends the hypersensitive intestine, causing pain or increasing the osmolality of the alimentary bolus that would alter the intestinal motility.

Functional recurrent abdominal pain with dyspepsia

The manifestation of dyspepsia is defined as a recurrent or persistent pain, or as a discomfort that happens at the superior part of the abdomen, and is caused by functional or organic diseases (reflux, peptic disease, Crohn's disease). The functional diseases present manifestations similar to the peptic ulcer or to the intestinal motility alterations. In the ulcerous pattern, the epigastric pain predominates; it precedes alimentation and is alleviated by foods and antacids. In motility alterations, pain is not the main symptom. Regurgitation, vomits, nausea, early satiety, and abdominal discomfort occur. However, there are considerable variations and overlapping of signs and symptoms among the groups (6).

The functional recurrent abdominal pain with dyspepsia is influenced by the same environmental and behavioral factors as the isolated paroxysms of periumbilical pain. Thee are no signs or symptoms that may distinguish between organic and functional dyspepsia. The diagnosis should be done only when there is a characteristic history of recurrent pain with normal physical examination (except for some pain at the palpation of the superior part of the abdomen), and unaltered complementary examinations: hemogram, erythrocyte sedimentation rate, serum amylase and lipase, aminotransferases, H. pylori, parasitological examination of feces, radiological contrast studies of the esophagus, stomach, duodenum, and intestine, abdominal ultrasound, and upper gastrointestinal endoscopy (6).

The alert signs and symptoms for the organic causes are epigastric pain, which expands to the back, blood in feces or in vomits, loss of weight, fever, persistent vomits, diarrhea, dysphagia, hepatomegaly, splenomegaly, abdominal mass or massiveness, and articular edema (Table 2).

Table 2 -
Causes of recurrent abdominal pain with dyspepsia

The treatment of functional recurrent abdominal pain with dyspepsia is based on the orientation of the patient and parents about the authenticity of the pain, concepts of functional pain, factors that maintain, intensify, and improve the painful process, and prognosis of the disease. This approach is discussed in the functional recurrent abdominal pain with isolated paroxysms of periumbilical pain.

Adults with functional dyspepsias are sometimes treated with drugs. Those that present ulcerous pattern receive histamine-2 receptor antagonists, and are recommended not to smoke, not to use caffeine, nonsteroidal anti-inflammatory drugs, and acetylsalicylic acid. Those that present signs and symptoms suggestive of altered motility are treated with prokinetics (cisapride or metoclopramide). There are no data that prove the benefit of these interventions in children with functional recurrent abdominal pain and dyspepsia. The use of drugs reinforces the painful behavior (6).

Functional recurrent abdominal pain with digestive tract dysfunction

Recurrent abdominal pain with intestinal dysfunction is characterized by pain usually at the inferior part of the abdomen, which is intensified or alleviated with intestinal movements. With defecation, there is the relief of pain, or its association with changes in the frequency or consistency of the feces, feeling of incomplete defecation, evacuative urgency or effort, passage of mucus, discomfort, and abdominal distension (31-33).

The most frequent cause of recurrent abdominal pain with dysfunction of the digestive tract is the functional irritable bowel syndrome, which corresponds to the irritable bowel in the adult. It affects mainly teenagers, and is manifested in two different ways, with the predominance of diarrhea or constipation and with variable defecation patterns. The diagnosis is done through typical history (recurrent abdominal pain with intestinal dysfunction pattern), normal physical examination, including rectal touch and laboratory tests without alterations: hemogram, erythrocyte sedimentation rate, assay for the detection of parasites, eggs, cysts, and occult blood in the feces (31-33).

The alert signs and symptoms suggestive of organic diseases are pain or diarrhea that interrupt the sleep, presence of blood in the feces, delayed growth, fever, skin eruptions, articular pain or edema, fistula, perianal fissures or ulcers. The causes of recurrent abdominal pain with digestive tract dysfunction are listed in Table 3.

Table 3 -
Causes of recurrent abdominal pain with altered intestinal pattern

The treatment of functional irritable bowel syndrome follows the same orientations as the functional recurrent abdominal pain with isolated paroxysms of periumbilical pain. Orientation should be given to the parents and the patient about the authenticity of the pain, the concept of functional pain, the factors that maintain, intensify, and attenuate the pain crisis, and orientation about the prognosis. However, patients in which diarrhea predominates benefit from the use of antidiarrheal agents. Children that present a tendency to constipation improve with the use of prokinetics and fibers. The excessive use of carbohydrates should be avoided due to the production of gases, and there should be orientation about how to eat slowly, avoiding aerophagia. In some children, the use of simeticone is recommended (31-33).

Prognosis of functional recurrent abdominal pain

Some retrospective studies and few prospective ones have assessed the evolution of functional recurrent abdominal pain in childhood. Two months after the diagnosis, 30 to 50% of the affected children no longer complain of recurrent abdominal pain. This occurs when the parents and the patient accept the association between stress and pain. Some (25%) continue to present painful symptoms for 5 years. From 30 to 50% of these children will have abdominal pain still in adulthood, but in 70% of the cases, the pain does not interfere with the activities. One-third of the children with functional recurrent abdominal pain will develop other pains in adulthood: cephalea, backache, and menstrual pain. Thirty percent of the adults with irritable bowel syndrome reported its beginning in childhood. The possibility of the children to develop organic diseases, such as Chron's disease, is below 2% (6,34,35).

The best prognosis for functional recurrent abdominal pain occurs: in families without pain complaints; in girls; when the beginning of the pain crises occurs after 6 years of age; when the treatment is started within 6 months after the beginning of the painful process. The worst diagnosis is observed: in families with painful manifestations; in boys; when the beginning of the pain occurs before 6 years of age; when the seek for treatment occurs late.

Conclusions

The ambiguity of attitudes that these pain crises provoke in most doctors and families frequently induces to a overabundance of examinations. The impropriety of such conduct is far known. In the review of medical records of children hospitalized for the assessment of deficient growth, those with organic problems had the diagnosis strongly suggested by history and by physical examination. No exam had a positive value without a specific indication of the clinical evaluation (36). When many exams are performed without following any criterion, besides the discomfort and the costs generated, there are other reasons that should lead us to be prudent in cases of children with recurrent pain. There is the possibility of finding some false positive exams, and of the patient being diagnosed and frequently treated for a disease that actually does not exist. The failure in acknowledging this was already playfully called Ulisses' syndrome, in allusion to the Greek mythological hero: the unnecessary and uncritical use of laboratory examinations, leading to long investigation journeys, and making the child and his/her family go through an unnecessary, expensive, and sometimes dangerous expedition, whose end is the starting point (37). Achieving an equilibrium, knowing the measurement of things, not loosing time, neither abolishing stages of the investigation and treatment processes of recurrent abdominal pain should be the pediatrician's objective when facing a child and his/her family with this problem. The pediatrician should not be as a secure refuge, but as a compass, knowing that the prognosis of functional recurrent abdominal pain is good, that only 1/4 of the patients continue to present painful symptoms after 5 years counting from the beginning of the pains. Late organic complications in this group of children are rare. These attitudes help the pediatrician navigate in these calm but unclear waters (38-40).