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Irritable bowel syndrome: A behavioral model
Behar Prmcd
Ret. & Therap,. ,n Great
Vol.
0005.7967181/060475-0909102.00/0
19. pp. 475 LO 483. 19111
Pcrgamon
Bnlam
IRRITABLE BOWEL A BEHAVIORAL
Press Ltd
SYNDROME: MODEL
PAUL R. LATIMER Department of Psychiatry. Temple
University Medical School, Philadelphia, PA 19129. U.S.A. (Recked
3 March
3300 Henry
Avenue,
1981)
Summary-Current models for explaining irritable bowel syndrome (IBS), the most common gastrointestinal disorder, are critically reviewed and found wanting. Although inadequate to explain the complex clinical features of IBS. these models now determine treatment and research strategy. A behavioral model is offered as an alternative in the hope that it will’lead to effective treatment and a progressive research program. The central features of this model are: (a) that verbal, motoric and physiological behavior characteristitic of IBS are capable of independence or desynchrony; (b) that these aspects of behavior are quantitative variations of normal; and (c) that there is a genetic predisposition to neuroticism which. in turn, predisposes to IBS. Some of the model’s implications are discussed.
INTRODUCTION Irritable bowel syndrome (IBS) is a common and costly disorder (Almy, 1978) characterized by abdominal pain and a change in bowel habit (either constipation or diarrhea) in the absence of any abnormalities detected by the usual medical investigations for these symptoms. It has been said to account for 50-70% of all patients with digestive complaints (Fielding, 1977; Kirsner and Palmer. 1958) and the best available estimates indicate a prevalence in the general population of 10-357: (Apley and Naish, 1958; Ferguson et al., 1977; Leighton et al., 1963; Pringle et al., 1966; Traven, 1979; Thompson and Heaton, 1980). It is of uncertain etiology and pathophysiology and there is no treatment of demonstrated lasting efficacy. The two most widely held beliefs about patients with IBS are: (a) that they are characterized by some unique abnormality of gastrointestinal physiology; and (b) that they are psychologically disturbed. In support of the first hypothesis are studies reporting that patients with IBS have an abnormal electrical rhythm in the smooth muscle of the rectum and rectosigmoid colon @nape ef ul., 1976, 1977; Taylor et al., 1978) and rectal and colonic motor hyperactivity during baseline recording (Chaudhary and Truelove, 1961). following food intake (Connell er al., 1965), following the injection of neostigmine (Chaudhary and Truelove, 1961; Kopel er al., 1967; Wangel and Deller, 1964) and following rectal distension (Whitehead et al., 1980). Primary colonic hyperalgesia has also been suggested as an underlying biological determinant of the disorder (Ritchie, 1973). In support of the second hypothesis are studies reporting that patients with IBS are more anxious, depressed and neurotic than both normals and other medical patients (Esler and Goulston. 1973; Latimer er al., 1981; Palmer et al.. 1974; West, 1970; Whitehead et al., 1980; Wright and Das, 1969). On the basis of structured psychiatric interviews a high percentage of IBS patients can be assigned a psychiatric diagnosis-diagnoses of hysteria and depression are common (Latimer et al.. 1981; Liss et al., 1973; Young et al., 1976).
These findings
CURRENT MODELS OF form the basis for three current models
IBS of IBS:
(a) the digestive disease model; (b) the psychiatric disease model; (c) the psychophysiological model. Digestive
disease
model
The digestive disease model posits the primary problem in the gastrointestinal tract and any psychological problems are assumed to arise secondarily. Treatment is directed 475
PAUL R. LATIMER
476
at correcting the inferred lems for this model.
underlying
biological
dysfunction.
There
are three major
prob-
1. The evidence in support of a unique abnormality of intestinal physiology is inconclusive (Latimer, 1980. 1981). Elsewhere, I have argued that since environmental events, stress and psychological factors are known to be associated with changes in colonic physiology (Almy and Tulin. 1947; Grace et ~1.. 1949; Latimer. 1981). any study intended to show definitively that there is a colonic abnormality peculiar to IBS patients must use a control group consisting of patients who are equally psychologically disturbed but without bowel symptoms. In a study designed with this aim in mind we compared colonic motor and myoelectrical activity in three groups of subjects: patients with IBS; neurotic patients without IBS (but who were equally anxious, depressed and neurotic as the IBS patients); and normals. During rest the IBS patients were found to have a greater number and duration of colonic contractions than the normal subjects, but there were no significant differences between the neurotic and IBS patients on either colonic motor or myoelectrical measures (Latimer et al., 1981). The previously described abnormal myoelectrical rhythm (Snape er al., 1976; 1977; Taylor et al., 1978) was not seen in any group nor were the IBS patients found to have a lower threshold for pain in response to colonic distension (Latimer et al., 1979) as predicted by the primary colonic hyperalgesia hypothesis (Ritchie, 1973). 2. The psychological problems of IBS patients are greater than those found in patients with much more severe and disabling gastrointestinal disease and are therefore unlikely to be solely a reaction to the digestive symptoms (Esler and Goulston, 1973 : West, 1970). 3. A primary disorder of intestinal physiology does not readily explain the wide range of non-gastrointestinal symptoms found in IBS such as weakness. fatigue, lack of energy, muscular pains, headaches, insomnia, palpitations, nervousness. dizziness, excessive perspiration, frequency of micturition (in 63”,,), painful micturition (in 26%), dysmenorrhea (in 907;) and dyspareunia (in 33”;) (Fielding, 1977; Kirsner and Palmer, 1958). Psychiatric disease model According to the psychiatric disease model the primary problem is a psychiatric illness and any gastrointestinal problems are assumed to be secondary. Hislop (1971) has argued, for example, that all patients with IBS have an affective disorder. The major problems for this mode1 are: 1. All patients with IBS, even in clinic populations, do not receive a psychiatric diagnosis in carefully designed studies; among those who do, there are many different diagnoses (Liss et al., 1973; Young et al., 1976). 2. There are many equally disturbed individuals with any given psychiatric diagnosis who do not have IBS. Psychophysiological model The essential feature of the psychophysiological model is that IBS symptoms are supposed to be caused by physiological changes that normally accompany certain emotional states; in IBS patients these changes are presumed to be more intense and sustained. This model is consistent with all of the findings supporting the previous two models and it is more explicit about the relations between the psychological and gastrointestinal findings. Variations of this model have proposed that specific symptoms may result from specific unconscious conflicts, specific personality profiles. specific attitudes. constitutional vulnerability, individual response specificity or specific visceral conditioning. I have reviewed these theories elsewhere, as they relate to IBS (Latimer. 1979a). The major problem for this model in all its variations is that there has not been a convincing demonstration in IBS that the gastrointestinal physiological responses that normally
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bowel syndrome
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accompany emotional states are more intense and sustained than for subjects without IBS but who are experiencing similar emotions (Latimer et al., 1981). There is ample evidence that changing emotion can alter gastrointestinal physiological responses (Almy and Tulin, 1947; Grace er ul., 1949; Latimer, 1981) but why do some individuals get IBS while others do not? These models determine research and treatment strategies (Latimer, 1979b) and will continue to do so, despite their inadequacies, unless a heuristic alternative model is offered (Latimer, 1979~). Such a model must explain, at the least, all of the following facts : 1. Patients with IBS complain of a variety of symptoms including abdominal pain and alteration in bowel habits; 2. Symptoms are usually not confined to the gastrointestinal system; 3. These patients are, on average, more anxious depressed and neurotic than control subjects and most patients with IBS meet strict criteria for a psychiatric diagnosis; 4. They are a heterogeneous group with respect to psychiatric diagnoses; 5. No distinctive biological characteristics-physical, physiological, biochemical-have been demonstrated; 6. They closely resemble psychoneurotic patients in their psychological and physiological characteristics, sex distribution and nature of psychological problems; 7. They respond positively, albeit temporarily, to a variety of treatment procedures; and 8. The symptoms run in families. The remainder of this paper is devoted to the development of a behavioral which more adequately accounts for each of the above characteristics of IBS.
A BEHAVIORAL
The model
has three central
model
M0DE.L
features.
1. Desynchronl Behavior relevant to IBS at each of three levels-verbal, -is capable of independence or desynchrony.
motoric,
physiological
Unlike the diagnosis of medical disorders for which a biological marker has been established, the diagnosis of IBS is made entirely (apart from exclusionary criteria) on the basis of the patient’s reports; most diagnostic criteria require reports of both abdominal pain and change in bowel habit. No observations are usually made to confirm, for example, the frequency or nature of the bowel movements or the reported antecedents and consequences of the abdominal pain. There is usually no systematic investigation of physiological function, although it is commonly assumed that the reports of abdominal pain and constipation in patients with IBS are due to an increase in the frequency, amplitude and duration of colonic segmental contractions. That this assumption of a close relationship between symptom reports and gastrointestinal physiological activity may be unwarranted was suggested by the evidence reviewed above. Latimer et al. (1981) demonstrated that despite their reported bowel symptoms a group of IBS patients could not be distinguished in their colonic responses from a group of patients who were equally neurotic, anxious and depressed but who did not have IBS. These two groups of patients differed in their verbal behavior in the sense that one group had identified gastrointestinal symptoms as a problem requiring treatment and the other had not: the second group (psychiatric outpatients) had described their problems in psychological terms (e.g., anxiety. depression, marital problems). It is probably also true that these two groups differed in their non-verbal symptomatic behavior (e.g...use of laxatives, enemas. diet, toileting behavior. pain related behavior). This demonstrates that the report of gastrointestinal symptoms can be independent of any distinctive, identifiable. gastrointestinal. physiological correlate. A second. related. but as yet unanswered
478
PAUL R. LATIMER
question, is whether such reports in individual IBS patients correlate with changing gastrointestinai physiological responses (e.g., colonic contractions) though these may not be responses which are unique to IBS. The model predicts that such correlations are possible but by no means necessary and probably not the rule. This desynchrony hypothesis is, at once, the most distinctive feature of this model and. to most physicians. the most improbable. One of the most striking demonstrations that what a person says and does may be relatively independent of his physioIogica1 responses is the classic experiment of Schachter and Singer (1962). In this study. identical injections of epinephrine elicited different emotions depending on the social context in which the injections were administered. For the purposes of this argument, the key point is that quite different verbal and motor responses were eiicited in response to identical physiological stimuli. The practicaI implications of this notion have increasingly been the subject of serious investigation. A patient may report fear and yet show no signs of physiological arousal or even behavioral avoidance (Lang, 1968, Rachman, 1978); he may report sleep-onset insomnia and yet have a normal latency to EEG-determined sleep onset (Borkovec. 1979); and he may have ‘tension’ headaches whose occurrence and severity bear no relation to the EMG potentials measured in the apparently offending muscle (Martin, 1980). If individuals in the general population, at any given moment, either do or do not exhibit the behaviors characteristic of IBS at the verbal, motoric and physiological levels, then ail the possibilities illustrated in Table 1 come to mind. This assumes that some categorical criteria can be established for behavior at each level to classify it as either normal or abnormal, characteristic of IBS or not. In the general population the possibilities range from individuals with no characteristics of IBS at any level to those with characteristics at all three levels. Only those possibilities which include characteristic verbal behavior apply to clinical studies of IBS since their subjects are selected on the basis of their verbal behavior. 2. Diinensional us categorical view of IBS In IBS there are only quantitative changes in characteristic behavior, with a continuous variation from the extremes of ‘normal’ to ‘abnormal’. The matrix introduced in Table 1 made use of the usual categorical approach to IBS i.e., someone either has IBS or not. In this case they either have a behavioral abnormality characteristic of IBS at one of three levels or not. This is the usual medical approach to the study of diseases. Unfortunately, in this case there is no clear discontinuity between behavior universally agreed to be characteristic of IBS and behavior which is not. For certain purposes this problem is legitimately circumvented by establishing operational criteria to establish a discontinuity between those with the disorder and those Table 1. Tripartite behavioral assessment matrix Verbal
Behavior characteristic Physiological
of IBS Motoric
-
+ + + f e.g. Report of abdominal pain or change in bowel habit
+ 4
+ +
f -I-
+
f
e.g. Increase in colonic segmental contractions (duration, amplitude, frequency)
e.g. Taking medication for pain; restricted activity due to pain or fear of incontinence
(+) Indicates the presence and ( -) the absence of behavior characteristics of IBS.
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479
bowel syndrome
without it. This pragmatic practice frequently becomes confused with the notion that patients so labelled as IBS are qualitatively distinct from those not so labelled, a point of view which has not, so far, been scientifically substantiated. The alternative to this categorical view of IBS, is that there are only quantitative differences in behavior between those labelled as IBS and the rest. This possibility leads to the replacement of the matrix in Table 1 with three partially independent dimensions (See Fig. 1). Every person in the general population could be described along each of these three dimensions according to the extent that they exhibited behavior on that dimension. The dimensions are probably only partially independent; their degree of correlation remains to be empirically demonstrated. This considerably expands the possibilities suggested by Table 1 but more closely approximates clinical reality and avoids the difficult problem of making the categorical distinctions. 3. Genetic predisposition There is a genetic predisposition to IBS.
to neuroticism
and neuroticism
predisposes
A familial tendency for IBS has been remarked upon by those interested in the condition for over 50 years (Ryle, 1928). Davidson and Wasserman (1966) studying the condition in children noted that 67”’ j0 of the parents and 50% of the siblings had a recurrent persistent functional bowel complaint. On the other hand, the number of relatives with functional complaints in families of patients with a variety of other specific gastrointestinal diseases was not as high. Similar findings have been reported by others (Stone and Barbero, 1970; Oster, 1972; Apley, 1975). Stone and Barber0 (1970) also reported a high incidence of early problems as reflected by abnormal pregnancy history, neonatal difficulty and infant colic. These facts are often cited as evidence for genetic contributions to the disorder although they are equally consistent with the importance of early environmental influence such as modelling by parents. In fact, Christensen and Mortensen (1975) found that children of persons with a history of IBS during childhood apparently did not suffer from abdominal pain more frequently than children of persons without IBS during childhood. Their data suggested that actual exposure to a parent with symptoms was more closely related to the occurrence of symptoms in children than was the history of a parents symptoms. This suggests the importance of vicarious learning. There is clearly insufficient data in this literature alone to clarify the relative importance of genes and environment. Given the overlap, documented above. between neuroticism and IBS it may be instructive to examine the evidence concerning genetic contributions to neuroticism. The best available data on this subject comes from an interesting animal model of neuroticism which may be particularly relevant to IBS: Maudsley Reactive and Nonreactive rats. In
Motaric
Verbal Physiological Fig. 1. Tripartite
behavioral assessment dimensions. physiological and motoric
A ihree-dimensional behavioral continua.
space defined
by verbal.
480
PAUL R. LATIMER
this model emotional defecation is used as an index of fear. This response was chosen partly because of easy measurement and partly because it is a matter of universal observation that strong emotion, especially fear, can cause involuntary excretion. Using a standard situation for the measurement of emotional defecation (the Open Field test), the response to stressful stimuli is measured as the number of fecal boluses dropped by the animal. An ambulation score is also calculated by recording the animals movements. In an elegant series of experiments designed to separate genetic and environmental effects, Broadhurst has convincingly demonstrated that there is strong genetic control over Open Field defecation. It has since been repeatedly demonstrated that although these strains were selectively bred entirely on the basis of defecation responses. they differ on a wide range of behavioral, psychophysiological, psychoendocrinological and psychopharmacological measures (Broadhurst, 1975; Broadhurst and Eysenck. 1965; Eysenck and Broadhurst, 1964). Broadhurst conceptualizes these two strains as having relatively stable differences for a generalized trait which he calls emotionality. Although. the use of a single hypothetical construct such as emotionality to account for all the observations has been seriously disputed (Archer. 1973. 1975) it is widely accepted that these experiments have successfully demonstrated the effects of genotype on a wide range of behaviors. As might be expected from the rigor of experimental design necessary to disentangle genetic and environmental effects on behavior in rats, the evidence involving humans is much weaker. Several reviews (Shields. 1973; Slater and Cowie. 1971: Vanderberg, 1967) of these studies (which usually involve the comparison of intrapair resemblances between monozygotic and dizygotic twins) have concluded that monozygotic twins are more similar in personality than are dizygotic twins and that this is, at least partially, genetic. Eysenck (1967) has been a strong advocate of the importance of a genetic contribution to the personality dimensions of extraversion and neuroticism; he uses ‘emotionality’ in rats as an animal model of ‘neuroticism’ in humans. This model seems particularly suitable for IBS. Patients with IBS are in several ways analogous to Maudsley Reactive rats. Some have an increased frequency of defecation particularly under stressful circumstances: they have high neuroticism scores together with generalized signs and symptoms of emotional arousal, and there is evidence that the condition runs in families. The theoretical importance of this comparison lies in the implicit suggestion that the change in bowel habits which is a cardinal feature of IBS may be an unlearned response to stressful circumstances. This has important imphcations for choosing appropriate therapeutic targets and goals.
DISCUSSION
If IBS patients come from the same ‘stock’ as other neurotic individuals many features of IBS become less perplexing. Anxiety, depression. neuroticism. heterogeneous psychiatric disorders, multiple somatic and psychological symptoms and positive response to various treatments are expected among such individuals. Likewise, it is generally accepted that neuroticism varies in the population in a dimensional way (Eysenck, 1967). The major question that remains is why some patients become identified as having IBS while others do not. The evidence reviewed above suggests that IBS is a behavioral problem in which the unadaptive behavior may consist of what the patient says, what he does, how he responds physiologically to certain circumstances. or a combination of these. The analogy with the Maudsley Reactive rats suggests that the unadaptive physiological responses and symptomatic change in bowel habits is an unlearned response to stressful circumstances. which IBS patients have in common with other equally neurotic individuals. They differ from other neurotics in their verbal and other overt symptomatic behavior. These differences may result from idiosyncratic learning experiences which may also be the basis for desynchrony. What are these additional learning experiences which determine symptom choice’? The answer to this question is not yet known, but there are several possibilities worth explor-
Irritable bowel syndrome
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ing. First, there is the role of vicarious learning which has already been mentioned above. From parents or significant others with IBS, children may learn: (1) misconceptions about ‘normal’ bowel habits; (2) that symptoms of IBS are a socially acceptable sign of distress; (3) that symptoms of IBS are a socially acceptable way to avoid unpleasant responsibilities; (4) that symptoms of IBS are a socially acceptable way to eiicit a show of concern and affection from family, friends and health care providers. Patients with IBS have been reported to show a social-desirability response set (Latimer er al., 1981; Palmer er al., 1974). It may be, as it often appears clinically, that many of these patients recognize they have a problem and find it more acceptable socially to be identified as having a medical problem They therefore present themselves in a way that contributes to the primary physician usually not recognizing the psycho1ogi~al problem (Young et al., 1976). In addition to these factors. the patient’s degree of extraversion may also influence the tendency to report symptoms. The extraversion scores of patients with IBS have been found to fall midway between those of neurotic and normal subjects. (Esler and Goulston. 1973; Latimer er at., 1981; Palmer et al., 1974). It was shown, in a study by Bond (1971). that among patients in pain who had an elevated neuroticism score, those with higher extraversion scores were more likely to make complaints leading to nursing attention and prescription of analgesics. The role of health-care professionals may be very important in determining the healthcare trajectory of such patients. A patient reporting the presence of certain symptoms or experiences in an unbiased way may be influenced by the focus or interest of the physician he sees. Once medical intervention occurs, physician tendencies to identify behavior as illness may play a large part in determining outcome. A person with recurring constipation and abdominal pain may believe the problem is related to ongoing marital problems but may want to make sure there is nothing more serious. If the physician becomes concerned. orders many investigations, makes a diagnosis and prescribes treatment that produces a change. the patient may become convinced that there is an illness, may become increasingly alarmed when symptoms recur and may continue to seek treatment. Since the original stressful situation has not been altered, the effects of treatment will be temporary; both doctor and patient may begin to question the diagnosis. The patient, now convinced that there is an illness, may lose confidence in the doctor, who no longer seems sure about etiology or treatment. There can then follow a change of doctors, conflicting advice and progressive incapacitation. On the other hand, the same patient may be seen by a physician who finds out about the marital problems and reassures the patient that his or her symptoms are a variation of normal and of no ominous significance. Such a course of action may have an entirely different outcome. Whether or not the marital problems are successfully dealt with, the gastrointestinal symptoms take on a different significance. Although this behavioral model does not dictate the necessity for behavior therapy in every case of IBS, it does have implications for the target behaviors and therapeutic objectives in those cases where it is applied. Behavior therapists generally regard themselves as applying learning principles for the purpose of changing /earned unadaptive behavior (Wolpe. 1973). If the symptomatic change in bowel habits is an unlearned response to stressful circumstances. is it more appropriate to direct therapy at the altered bowel habits in an effort to uncouple this response from stressful stimuli or to teach patients that bowel symptoms are their normal response to stress and direct therapy at reducing stress? On a priori grounds it might be expected that the second approach would be most appropriate. These two approaches have quite different outcome implications. Following the first approach the goal is complete elimination of the symptoms; with the second, a change in bowel habit would be expected from time to time with changing life circumstances since
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the elimination of all stress is impracticle. It is noteworthy that the first approach with its goal of complete elimination of the symptoms is frequently what the patients themselves prefer. This approach has led to both behavioral (e.g., biofeedback of colonic contractions) and medical (e.g.. pharmacological) treatments for the disorder. Rather than implying that nothing can be done for such individuals, this analysis suggests that therapy must be directed at those aspects of behavior which are most susceptible to change. This model also has important implications for research on IBS. Unless behavior at the three levels is measured independently, there is no way of knowing how the populations selected by different investigators, on the basis of symptoms reports, compare with respect to relevant motor and physiological behavior. It is possible that a considerable amount of the variance among all the studies on IBS can be accounted for in this way. CONCLUSION
IBS has been the subject of a considerable body of literature, but there is little to suggest systematic progress in our understanding or management of the disorder. Although there is still a great deal to be learned about the physiology of the gut, its neural, hormonal and myogenic control systems and their interactions with. the environment, the impact of available knowledge may be unnecessarily muted by a reliance on inadequate models of the disorder. There is considerable evidence that IBS is essentially a behavioral disorder. It is hoped that the proposed behavioral model will lead to effective treatment and stimulate a progressive research program. REFERENCES ALMY T. P. (1978) Biological adaptation. digestive disorders and health services. Ps)&~omarics 19, 2C&207. ALMY T. P. and TULIN M. (1947) Alterations in colonic function in man under stress: experimental production of changes simulating the ‘irritable colon’. Gastrornreroloyv 8. 616-626. APLEY J. (1975) The Child wirh Abdominal Pains. Blackwell. Oxford. APLEY J. and NAISH N. (1958) Recurrent abdominal pains: a field survey of 1000 school children. Archs Dis. Childh.
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SHIELDSJ. (1973) Heredity and psychological abnormality. In ~u~dbffo~ of Ahnormul Ps,xhology (Edited by EYSENCKH. J.). Pitman Medical. London. SLATERE. and Crtwie I! (1971) 7% Genetics of Menral Disorders. Oxford Univ. Press. London. SNAPEW. J.. CARLSONA. M. and COHENS. (1976) Colonic myoelectric activity in the irritable bowel syndrome. Gastroenterology 70, 326330.
SNAPEW. J.. CARL~~NG. M.. MATARAZZOS. A. and COHENS. (1977) Evidence that abnormal myoelectric activity produces colonic motor dysfunction in the irritable bowel syndrome. Gustroenterology 72, 383-387.
STONER. 7. and BARBEROG. T. (1970) Recurrent abdominal pain in childhood. Pediurries 45, 732-738. TAYLORI.. DARBV C. and HAMMONDP. (1978) Comparison of rectosigmoid myoelectrical activity in the irritable colon syndrome during relapses and rem&ions. Gur 19, 9231929. THOMPSON W. G. and HEATONK. W. (1980) Functional bowel disorders in aooarentlv healthv_.neoole. I. . Gustroenreroloy~ 79, 283-288. TRAVENH. D. (1979) Personal communication. VANDERBERG S. G. (1967) Hereditary factors in normal personality traits (as measured by inventories). In Recent Acirunces in Bio/ogicul Psychiatry, Vol. IX (Edited by WORTISJ.). Plenum Press, New York. WANGELA. G. and DELLERD. J. (1964) Intestinal motility in man-III: mechanisms of constipation and diarrhea with particular reference to the irritable colon syndrome. Gastroenreroloav 48.69-84. WESTK. L. (1970) MMPI correlates of ulcerative colitis. J. &. Psvchol. 26, 214-219.-WHITEHEADW. E.. ENGEL B. T. and SCHUSTERM. M. (1980) Iriitable bowel svndrome: ohvsioloeical and psychological differences between diarrhea-predominant and constipation-piedominan; datienti. Digesr. Dis. Sri. 25, 404-413. WOLPEJ. (1973) The Pructicr qf Behavior Therapy. Pergamon Press. London. WRIGHT 3. T. and DAS A. K. (1969) Excretion of 4-hydroxy-3-methoxy mandelic acid in cases of ulcerative colitis and diarrhea of nervous origin. Gur IO, 628-630, YOL’NGS. J.. ALPERS D. H.. NORLANDC. C. and WOODRUFFR. A. (1976) Psychiatric illness and the irritable bowel syndrome. Gosrroenrerolog! 70, 162--166.
Ret. & Therap,. ,n Great
Vol.
0005.7967181/060475-0909102.00/0
19. pp. 475 LO 483. 19111
Pcrgamon
Bnlam
IRRITABLE BOWEL A BEHAVIORAL
Press Ltd
SYNDROME: MODEL
PAUL R. LATIMER Department of Psychiatry. Temple
University Medical School, Philadelphia, PA 19129. U.S.A. (Recked
3 March
3300 Henry
Avenue,
1981)
Summary-Current models for explaining irritable bowel syndrome (IBS), the most common gastrointestinal disorder, are critically reviewed and found wanting. Although inadequate to explain the complex clinical features of IBS. these models now determine treatment and research strategy. A behavioral model is offered as an alternative in the hope that it will’lead to effective treatment and a progressive research program. The central features of this model are: (a) that verbal, motoric and physiological behavior characteristitic of IBS are capable of independence or desynchrony; (b) that these aspects of behavior are quantitative variations of normal; and (c) that there is a genetic predisposition to neuroticism which. in turn, predisposes to IBS. Some of the model’s implications are discussed.
INTRODUCTION Irritable bowel syndrome (IBS) is a common and costly disorder (Almy, 1978) characterized by abdominal pain and a change in bowel habit (either constipation or diarrhea) in the absence of any abnormalities detected by the usual medical investigations for these symptoms. It has been said to account for 50-70% of all patients with digestive complaints (Fielding, 1977; Kirsner and Palmer. 1958) and the best available estimates indicate a prevalence in the general population of 10-357: (Apley and Naish, 1958; Ferguson et al., 1977; Leighton et al., 1963; Pringle et al., 1966; Traven, 1979; Thompson and Heaton, 1980). It is of uncertain etiology and pathophysiology and there is no treatment of demonstrated lasting efficacy. The two most widely held beliefs about patients with IBS are: (a) that they are characterized by some unique abnormality of gastrointestinal physiology; and (b) that they are psychologically disturbed. In support of the first hypothesis are studies reporting that patients with IBS have an abnormal electrical rhythm in the smooth muscle of the rectum and rectosigmoid colon @nape ef ul., 1976, 1977; Taylor et al., 1978) and rectal and colonic motor hyperactivity during baseline recording (Chaudhary and Truelove, 1961). following food intake (Connell er al., 1965), following the injection of neostigmine (Chaudhary and Truelove, 1961; Kopel er al., 1967; Wangel and Deller, 1964) and following rectal distension (Whitehead et al., 1980). Primary colonic hyperalgesia has also been suggested as an underlying biological determinant of the disorder (Ritchie, 1973). In support of the second hypothesis are studies reporting that patients with IBS are more anxious, depressed and neurotic than both normals and other medical patients (Esler and Goulston. 1973; Latimer er al., 1981; Palmer et al.. 1974; West, 1970; Whitehead et al., 1980; Wright and Das, 1969). On the basis of structured psychiatric interviews a high percentage of IBS patients can be assigned a psychiatric diagnosis-diagnoses of hysteria and depression are common (Latimer et al.. 1981; Liss et al., 1973; Young et al., 1976).
These findings
CURRENT MODELS OF form the basis for three current models
IBS of IBS:
(a) the digestive disease model; (b) the psychiatric disease model; (c) the psychophysiological model. Digestive
disease
model
The digestive disease model posits the primary problem in the gastrointestinal tract and any psychological problems are assumed to arise secondarily. Treatment is directed 475
PAUL R. LATIMER
476
at correcting the inferred lems for this model.
underlying
biological
dysfunction.
There
are three major
prob-
1. The evidence in support of a unique abnormality of intestinal physiology is inconclusive (Latimer, 1980. 1981). Elsewhere, I have argued that since environmental events, stress and psychological factors are known to be associated with changes in colonic physiology (Almy and Tulin. 1947; Grace et ~1.. 1949; Latimer. 1981). any study intended to show definitively that there is a colonic abnormality peculiar to IBS patients must use a control group consisting of patients who are equally psychologically disturbed but without bowel symptoms. In a study designed with this aim in mind we compared colonic motor and myoelectrical activity in three groups of subjects: patients with IBS; neurotic patients without IBS (but who were equally anxious, depressed and neurotic as the IBS patients); and normals. During rest the IBS patients were found to have a greater number and duration of colonic contractions than the normal subjects, but there were no significant differences between the neurotic and IBS patients on either colonic motor or myoelectrical measures (Latimer et al., 1981). The previously described abnormal myoelectrical rhythm (Snape er al., 1976; 1977; Taylor et al., 1978) was not seen in any group nor were the IBS patients found to have a lower threshold for pain in response to colonic distension (Latimer et al., 1979) as predicted by the primary colonic hyperalgesia hypothesis (Ritchie, 1973). 2. The psychological problems of IBS patients are greater than those found in patients with much more severe and disabling gastrointestinal disease and are therefore unlikely to be solely a reaction to the digestive symptoms (Esler and Goulston, 1973 : West, 1970). 3. A primary disorder of intestinal physiology does not readily explain the wide range of non-gastrointestinal symptoms found in IBS such as weakness. fatigue, lack of energy, muscular pains, headaches, insomnia, palpitations, nervousness. dizziness, excessive perspiration, frequency of micturition (in 63”,,), painful micturition (in 26%), dysmenorrhea (in 907;) and dyspareunia (in 33”;) (Fielding, 1977; Kirsner and Palmer, 1958). Psychiatric disease model According to the psychiatric disease model the primary problem is a psychiatric illness and any gastrointestinal problems are assumed to be secondary. Hislop (1971) has argued, for example, that all patients with IBS have an affective disorder. The major problems for this mode1 are: 1. All patients with IBS, even in clinic populations, do not receive a psychiatric diagnosis in carefully designed studies; among those who do, there are many different diagnoses (Liss et al., 1973; Young et al., 1976). 2. There are many equally disturbed individuals with any given psychiatric diagnosis who do not have IBS. Psychophysiological model The essential feature of the psychophysiological model is that IBS symptoms are supposed to be caused by physiological changes that normally accompany certain emotional states; in IBS patients these changes are presumed to be more intense and sustained. This model is consistent with all of the findings supporting the previous two models and it is more explicit about the relations between the psychological and gastrointestinal findings. Variations of this model have proposed that specific symptoms may result from specific unconscious conflicts, specific personality profiles. specific attitudes. constitutional vulnerability, individual response specificity or specific visceral conditioning. I have reviewed these theories elsewhere, as they relate to IBS (Latimer. 1979a). The major problem for this model in all its variations is that there has not been a convincing demonstration in IBS that the gastrointestinal physiological responses that normally
Irritable
bowel syndrome
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accompany emotional states are more intense and sustained than for subjects without IBS but who are experiencing similar emotions (Latimer et al., 1981). There is ample evidence that changing emotion can alter gastrointestinal physiological responses (Almy and Tulin, 1947; Grace er ul., 1949; Latimer, 1981) but why do some individuals get IBS while others do not? These models determine research and treatment strategies (Latimer, 1979b) and will continue to do so, despite their inadequacies, unless a heuristic alternative model is offered (Latimer, 1979~). Such a model must explain, at the least, all of the following facts : 1. Patients with IBS complain of a variety of symptoms including abdominal pain and alteration in bowel habits; 2. Symptoms are usually not confined to the gastrointestinal system; 3. These patients are, on average, more anxious depressed and neurotic than control subjects and most patients with IBS meet strict criteria for a psychiatric diagnosis; 4. They are a heterogeneous group with respect to psychiatric diagnoses; 5. No distinctive biological characteristics-physical, physiological, biochemical-have been demonstrated; 6. They closely resemble psychoneurotic patients in their psychological and physiological characteristics, sex distribution and nature of psychological problems; 7. They respond positively, albeit temporarily, to a variety of treatment procedures; and 8. The symptoms run in families. The remainder of this paper is devoted to the development of a behavioral which more adequately accounts for each of the above characteristics of IBS.
A BEHAVIORAL
The model
has three central
model
M0DE.L
features.
1. Desynchronl Behavior relevant to IBS at each of three levels-verbal, -is capable of independence or desynchrony.
motoric,
physiological
Unlike the diagnosis of medical disorders for which a biological marker has been established, the diagnosis of IBS is made entirely (apart from exclusionary criteria) on the basis of the patient’s reports; most diagnostic criteria require reports of both abdominal pain and change in bowel habit. No observations are usually made to confirm, for example, the frequency or nature of the bowel movements or the reported antecedents and consequences of the abdominal pain. There is usually no systematic investigation of physiological function, although it is commonly assumed that the reports of abdominal pain and constipation in patients with IBS are due to an increase in the frequency, amplitude and duration of colonic segmental contractions. That this assumption of a close relationship between symptom reports and gastrointestinal physiological activity may be unwarranted was suggested by the evidence reviewed above. Latimer et al. (1981) demonstrated that despite their reported bowel symptoms a group of IBS patients could not be distinguished in their colonic responses from a group of patients who were equally neurotic, anxious and depressed but who did not have IBS. These two groups of patients differed in their verbal behavior in the sense that one group had identified gastrointestinal symptoms as a problem requiring treatment and the other had not: the second group (psychiatric outpatients) had described their problems in psychological terms (e.g., anxiety. depression, marital problems). It is probably also true that these two groups differed in their non-verbal symptomatic behavior (e.g...use of laxatives, enemas. diet, toileting behavior. pain related behavior). This demonstrates that the report of gastrointestinal symptoms can be independent of any distinctive, identifiable. gastrointestinal. physiological correlate. A second. related. but as yet unanswered
478
PAUL R. LATIMER
question, is whether such reports in individual IBS patients correlate with changing gastrointestinai physiological responses (e.g., colonic contractions) though these may not be responses which are unique to IBS. The model predicts that such correlations are possible but by no means necessary and probably not the rule. This desynchrony hypothesis is, at once, the most distinctive feature of this model and. to most physicians. the most improbable. One of the most striking demonstrations that what a person says and does may be relatively independent of his physioIogica1 responses is the classic experiment of Schachter and Singer (1962). In this study. identical injections of epinephrine elicited different emotions depending on the social context in which the injections were administered. For the purposes of this argument, the key point is that quite different verbal and motor responses were eiicited in response to identical physiological stimuli. The practicaI implications of this notion have increasingly been the subject of serious investigation. A patient may report fear and yet show no signs of physiological arousal or even behavioral avoidance (Lang, 1968, Rachman, 1978); he may report sleep-onset insomnia and yet have a normal latency to EEG-determined sleep onset (Borkovec. 1979); and he may have ‘tension’ headaches whose occurrence and severity bear no relation to the EMG potentials measured in the apparently offending muscle (Martin, 1980). If individuals in the general population, at any given moment, either do or do not exhibit the behaviors characteristic of IBS at the verbal, motoric and physiological levels, then ail the possibilities illustrated in Table 1 come to mind. This assumes that some categorical criteria can be established for behavior at each level to classify it as either normal or abnormal, characteristic of IBS or not. In the general population the possibilities range from individuals with no characteristics of IBS at any level to those with characteristics at all three levels. Only those possibilities which include characteristic verbal behavior apply to clinical studies of IBS since their subjects are selected on the basis of their verbal behavior. 2. Diinensional us categorical view of IBS In IBS there are only quantitative changes in characteristic behavior, with a continuous variation from the extremes of ‘normal’ to ‘abnormal’. The matrix introduced in Table 1 made use of the usual categorical approach to IBS i.e., someone either has IBS or not. In this case they either have a behavioral abnormality characteristic of IBS at one of three levels or not. This is the usual medical approach to the study of diseases. Unfortunately, in this case there is no clear discontinuity between behavior universally agreed to be characteristic of IBS and behavior which is not. For certain purposes this problem is legitimately circumvented by establishing operational criteria to establish a discontinuity between those with the disorder and those Table 1. Tripartite behavioral assessment matrix Verbal
Behavior characteristic Physiological
of IBS Motoric
-
+ + + f e.g. Report of abdominal pain or change in bowel habit
+ 4
+ +
f -I-
+
f
e.g. Increase in colonic segmental contractions (duration, amplitude, frequency)
e.g. Taking medication for pain; restricted activity due to pain or fear of incontinence
(+) Indicates the presence and ( -) the absence of behavior characteristics of IBS.
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479
bowel syndrome
without it. This pragmatic practice frequently becomes confused with the notion that patients so labelled as IBS are qualitatively distinct from those not so labelled, a point of view which has not, so far, been scientifically substantiated. The alternative to this categorical view of IBS, is that there are only quantitative differences in behavior between those labelled as IBS and the rest. This possibility leads to the replacement of the matrix in Table 1 with three partially independent dimensions (See Fig. 1). Every person in the general population could be described along each of these three dimensions according to the extent that they exhibited behavior on that dimension. The dimensions are probably only partially independent; their degree of correlation remains to be empirically demonstrated. This considerably expands the possibilities suggested by Table 1 but more closely approximates clinical reality and avoids the difficult problem of making the categorical distinctions. 3. Genetic predisposition There is a genetic predisposition to IBS.
to neuroticism
and neuroticism
predisposes
A familial tendency for IBS has been remarked upon by those interested in the condition for over 50 years (Ryle, 1928). Davidson and Wasserman (1966) studying the condition in children noted that 67”’ j0 of the parents and 50% of the siblings had a recurrent persistent functional bowel complaint. On the other hand, the number of relatives with functional complaints in families of patients with a variety of other specific gastrointestinal diseases was not as high. Similar findings have been reported by others (Stone and Barbero, 1970; Oster, 1972; Apley, 1975). Stone and Barber0 (1970) also reported a high incidence of early problems as reflected by abnormal pregnancy history, neonatal difficulty and infant colic. These facts are often cited as evidence for genetic contributions to the disorder although they are equally consistent with the importance of early environmental influence such as modelling by parents. In fact, Christensen and Mortensen (1975) found that children of persons with a history of IBS during childhood apparently did not suffer from abdominal pain more frequently than children of persons without IBS during childhood. Their data suggested that actual exposure to a parent with symptoms was more closely related to the occurrence of symptoms in children than was the history of a parents symptoms. This suggests the importance of vicarious learning. There is clearly insufficient data in this literature alone to clarify the relative importance of genes and environment. Given the overlap, documented above. between neuroticism and IBS it may be instructive to examine the evidence concerning genetic contributions to neuroticism. The best available data on this subject comes from an interesting animal model of neuroticism which may be particularly relevant to IBS: Maudsley Reactive and Nonreactive rats. In
Motaric
Verbal Physiological Fig. 1. Tripartite
behavioral assessment dimensions. physiological and motoric
A ihree-dimensional behavioral continua.
space defined
by verbal.
480
PAUL R. LATIMER
this model emotional defecation is used as an index of fear. This response was chosen partly because of easy measurement and partly because it is a matter of universal observation that strong emotion, especially fear, can cause involuntary excretion. Using a standard situation for the measurement of emotional defecation (the Open Field test), the response to stressful stimuli is measured as the number of fecal boluses dropped by the animal. An ambulation score is also calculated by recording the animals movements. In an elegant series of experiments designed to separate genetic and environmental effects, Broadhurst has convincingly demonstrated that there is strong genetic control over Open Field defecation. It has since been repeatedly demonstrated that although these strains were selectively bred entirely on the basis of defecation responses. they differ on a wide range of behavioral, psychophysiological, psychoendocrinological and psychopharmacological measures (Broadhurst, 1975; Broadhurst and Eysenck. 1965; Eysenck and Broadhurst, 1964). Broadhurst conceptualizes these two strains as having relatively stable differences for a generalized trait which he calls emotionality. Although. the use of a single hypothetical construct such as emotionality to account for all the observations has been seriously disputed (Archer. 1973. 1975) it is widely accepted that these experiments have successfully demonstrated the effects of genotype on a wide range of behaviors. As might be expected from the rigor of experimental design necessary to disentangle genetic and environmental effects on behavior in rats, the evidence involving humans is much weaker. Several reviews (Shields. 1973; Slater and Cowie. 1971: Vanderberg, 1967) of these studies (which usually involve the comparison of intrapair resemblances between monozygotic and dizygotic twins) have concluded that monozygotic twins are more similar in personality than are dizygotic twins and that this is, at least partially, genetic. Eysenck (1967) has been a strong advocate of the importance of a genetic contribution to the personality dimensions of extraversion and neuroticism; he uses ‘emotionality’ in rats as an animal model of ‘neuroticism’ in humans. This model seems particularly suitable for IBS. Patients with IBS are in several ways analogous to Maudsley Reactive rats. Some have an increased frequency of defecation particularly under stressful circumstances: they have high neuroticism scores together with generalized signs and symptoms of emotional arousal, and there is evidence that the condition runs in families. The theoretical importance of this comparison lies in the implicit suggestion that the change in bowel habits which is a cardinal feature of IBS may be an unlearned response to stressful circumstances. This has important imphcations for choosing appropriate therapeutic targets and goals.
DISCUSSION
If IBS patients come from the same ‘stock’ as other neurotic individuals many features of IBS become less perplexing. Anxiety, depression. neuroticism. heterogeneous psychiatric disorders, multiple somatic and psychological symptoms and positive response to various treatments are expected among such individuals. Likewise, it is generally accepted that neuroticism varies in the population in a dimensional way (Eysenck, 1967). The major question that remains is why some patients become identified as having IBS while others do not. The evidence reviewed above suggests that IBS is a behavioral problem in which the unadaptive behavior may consist of what the patient says, what he does, how he responds physiologically to certain circumstances. or a combination of these. The analogy with the Maudsley Reactive rats suggests that the unadaptive physiological responses and symptomatic change in bowel habits is an unlearned response to stressful circumstances. which IBS patients have in common with other equally neurotic individuals. They differ from other neurotics in their verbal and other overt symptomatic behavior. These differences may result from idiosyncratic learning experiences which may also be the basis for desynchrony. What are these additional learning experiences which determine symptom choice’? The answer to this question is not yet known, but there are several possibilities worth explor-
Irritable bowel syndrome
481
ing. First, there is the role of vicarious learning which has already been mentioned above. From parents or significant others with IBS, children may learn: (1) misconceptions about ‘normal’ bowel habits; (2) that symptoms of IBS are a socially acceptable sign of distress; (3) that symptoms of IBS are a socially acceptable way to avoid unpleasant responsibilities; (4) that symptoms of IBS are a socially acceptable way to eiicit a show of concern and affection from family, friends and health care providers. Patients with IBS have been reported to show a social-desirability response set (Latimer er al., 1981; Palmer er al., 1974). It may be, as it often appears clinically, that many of these patients recognize they have a problem and find it more acceptable socially to be identified as having a medical problem They therefore present themselves in a way that contributes to the primary physician usually not recognizing the psycho1ogi~al problem (Young et al., 1976). In addition to these factors. the patient’s degree of extraversion may also influence the tendency to report symptoms. The extraversion scores of patients with IBS have been found to fall midway between those of neurotic and normal subjects. (Esler and Goulston. 1973; Latimer er at., 1981; Palmer et al., 1974). It was shown, in a study by Bond (1971). that among patients in pain who had an elevated neuroticism score, those with higher extraversion scores were more likely to make complaints leading to nursing attention and prescription of analgesics. The role of health-care professionals may be very important in determining the healthcare trajectory of such patients. A patient reporting the presence of certain symptoms or experiences in an unbiased way may be influenced by the focus or interest of the physician he sees. Once medical intervention occurs, physician tendencies to identify behavior as illness may play a large part in determining outcome. A person with recurring constipation and abdominal pain may believe the problem is related to ongoing marital problems but may want to make sure there is nothing more serious. If the physician becomes concerned. orders many investigations, makes a diagnosis and prescribes treatment that produces a change. the patient may become convinced that there is an illness, may become increasingly alarmed when symptoms recur and may continue to seek treatment. Since the original stressful situation has not been altered, the effects of treatment will be temporary; both doctor and patient may begin to question the diagnosis. The patient, now convinced that there is an illness, may lose confidence in the doctor, who no longer seems sure about etiology or treatment. There can then follow a change of doctors, conflicting advice and progressive incapacitation. On the other hand, the same patient may be seen by a physician who finds out about the marital problems and reassures the patient that his or her symptoms are a variation of normal and of no ominous significance. Such a course of action may have an entirely different outcome. Whether or not the marital problems are successfully dealt with, the gastrointestinal symptoms take on a different significance. Although this behavioral model does not dictate the necessity for behavior therapy in every case of IBS, it does have implications for the target behaviors and therapeutic objectives in those cases where it is applied. Behavior therapists generally regard themselves as applying learning principles for the purpose of changing /earned unadaptive behavior (Wolpe. 1973). If the symptomatic change in bowel habits is an unlearned response to stressful circumstances. is it more appropriate to direct therapy at the altered bowel habits in an effort to uncouple this response from stressful stimuli or to teach patients that bowel symptoms are their normal response to stress and direct therapy at reducing stress? On a priori grounds it might be expected that the second approach would be most appropriate. These two approaches have quite different outcome implications. Following the first approach the goal is complete elimination of the symptoms; with the second, a change in bowel habit would be expected from time to time with changing life circumstances since
PAUL R. LATIMER
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the elimination of all stress is impracticle. It is noteworthy that the first approach with its goal of complete elimination of the symptoms is frequently what the patients themselves prefer. This approach has led to both behavioral (e.g., biofeedback of colonic contractions) and medical (e.g.. pharmacological) treatments for the disorder. Rather than implying that nothing can be done for such individuals, this analysis suggests that therapy must be directed at those aspects of behavior which are most susceptible to change. This model also has important implications for research on IBS. Unless behavior at the three levels is measured independently, there is no way of knowing how the populations selected by different investigators, on the basis of symptoms reports, compare with respect to relevant motor and physiological behavior. It is possible that a considerable amount of the variance among all the studies on IBS can be accounted for in this way. CONCLUSION
IBS has been the subject of a considerable body of literature, but there is little to suggest systematic progress in our understanding or management of the disorder. Although there is still a great deal to be learned about the physiology of the gut, its neural, hormonal and myogenic control systems and their interactions with. the environment, the impact of available knowledge may be unnecessarily muted by a reliance on inadequate models of the disorder. There is considerable evidence that IBS is essentially a behavioral disorder. It is hoped that the proposed behavioral model will lead to effective treatment and stimulate a progressive research program. REFERENCES ALMY T. P. (1978) Biological adaptation. digestive disorders and health services. Ps)&~omarics 19, 2C&207. ALMY T. P. and TULIN M. (1947) Alterations in colonic function in man under stress: experimental production of changes simulating the ‘irritable colon’. Gastrornreroloyv 8. 616-626. APLEY J. (1975) The Child wirh Abdominal Pains. Blackwell. Oxford. APLEY J. and NAISH N. (1958) Recurrent abdominal pains: a field survey of 1000 school children. Archs Dis. Childh.
33,
165-167.
ARCHER J. (1973) Tests for emotionality in rats and mice: a review. Anim. Behac. 21, 205-235. ARCHER J. (1975) The Maudsley Reactive and Nonreactive strains of rats: the need for an objective evaluation of differences. Behac. Gener. 5, 411413. BOND M. R. (1971) The relation of pain to the Eysenck Personality Inventory. Cornell Medical Index and Whitely Index of Hypochondriasis. Br. J. Psychiar. 119, 671-678. BORKOVEC T. D. (1979) Pseudo (experiental)-insomnia and idiopathic (objective) msomnia: theoretical and therapeutic issues. Adc. Behar. Res. Ther. 2. 27-55. BROADHURST P. L. (1975) The Maudsley Reactive and Nonreactive strains of rats: a survey. Eehar. Gener. 5. 299-3
19.
BROADHURST P. L. and EYSENCK H. J. (1965) Emotionality in the rat: a problem of response specificity. In Srephanos (Edited by BANKS C. and BROADHURST P. L.). Univ. of London Press. London. CHAUDHARY N. A. and TRUELOM S. C. (1961) Human colonic motility: a comparattve study of normal subjects. patients with ulcerative colitis and patients with irritable colon syndrome. Gastroenrerology 40, 1-36. CHRISTENSEN M. F. and MORTENSEN 0. (1975) Long term prognosis in children with recurrent abdominal pain. Archs Dis. Childh. 50, 110-l 14. CONNELL A. M.. JONES F. A. and ROWLANDS E. N. (1965) Motility of the pelvic colon, Part IV. Abdominal pain associated with colonic hyperactivity after meals. Gur 6, 105-l 12. DAVIDSON M. and WASSERMAN R. (1966) The irritable colon of childhood (chronic non-specific diarrhea syndrome). J. Pediar. 69, 1027-1038. ESLER M. D. and GOULSTON K. J. (1973) Levels of anxiety in colonic disorders. New Enyl. J. Med. 288. 1620. EYSENCK H. J. (1967) The Bioloyicul Busis of Personalir!. Thomas. Springfield. Illinois. EYSENCK H. J. and BROADHURST P. L. (1964) Experiments with animals: introduction. In kperimenrs in Morirarion (Edited by EYSENCK H. J.). Pergamon Press, Oxford. FERGUSON A.. SIRCUS W. and EASTWO~D M. A. (1977) Frequency of ‘functional’ gastrointestinal disorders. Lancer ii, 613-614. FIELDING J. F. (1977) A year in out-patients with the irritable bowel syndrome. Ir. J. met/. SC!. 146, 1622166. GRACE W. J.. WOLF S. and WOLFF H. G. (1949) Life situations. emotions and colonic function. Gasrroenreroloy) 14, 93-108.
HISLOP I. G. (1971) Psychological sigmficance of the irritable colon syndrome. Gut 12. 452457 KIRSNER J. B. and PALMER W. L. (1958) The irritable colon. Gusrrornrerologv 34, 491-501. KOPEL F. B.. KIM 1. C. and BARBERO A. J. (1967) Comparison of rectostgmoid motility in normal children. children with recurrent abdominal pain. and children wtth ulcerative colitis, Pediarrics 39. 539-545. LANG P. J. (1968) Fear reduction and fear behavior: problems in treating a construct. In Research in Psychorhurapy. Vol. 111 (Edited by SHLEIN T. M.). p. 90. American Psychological Association Washmgton. DC. LATIMER P. R. (1979a) Psychophysiologic disorders: a critical appraisal of concept and theory illustrated with reference to the irritable bowel syndrome. Psycho/. Med. 9, 71-80.
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