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Original Articles: Gastroenterology

Validation of the Pediatric Rome II Criteria for Functional Gastrointestinal Disorders Using the Questionnaire on Pediatric Gastrointestinal Symptoms

Caplan, Arlene*; Walker, Lynn; Rasquin, Andrée*

Author Information
Journal of Pediatric Gastroenterology and Nutrition: September 2005 - Volume 41 - Issue 3 - p 305-316
doi: 10.1097/01.mpg.0000172749.71726.13
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Abstract

INTRODUCTION

The establishment of symptom-based diagnostic criteria for functional gastrointestinal disorders (FGIDs) in adults, known as the Rome Criteria, constituted a major breakthrough in diagnosis and treatment. The consensual definition of the criteria facilitated the selection of homogeneous groups of patients, thereby advancing considerable empirical research on these disorders in adults. Recently, the same consensual approach was used to define diagnostic criteria for functional disorders in children and adolescents. These were published in 1999 as the Pediatric Rome II Criteria (1) (Table 1), but they have not yet been validated. Although several studies on the prevalence of pediatric FGIDs have used these new criteria, the questionnaires used to arrive at Rome II diagnoses have similarly not been validated (2-8). The aim of this study was to examine the validity of the Pediatric Rome II criteria using a valid and reliable measure of gastrointestinal symptoms for the pediatric age group (9).

T1-7
TABLE 1:
Pediatric Rome II criteria

SUBJECTS AND METHODS

Subjects were 315 patients 4 to 18 years old, presenting to the Pediatric Gastroenterology Clinic of Hôpital Ste-Justine/University of Montreal for gastrointestinal symptoms unrelated to liver disease. At least one parent of every patient also participated. The sample was drawn from a larger group of 624 consecutive new patients and parents who participated in a study validating the Questionnaire on Pediatric Gastrointestinal Symptoms (QPGS) (9). Participants in this study had been classified as having a functional problem by 1 of 11 attending pediatric gastroenterologists.

Measures

The QPGS is a paper and pencil measure of gastrointestinal symptoms associated with FGIDs in children. It was designed as a research instrument to classify gastrointestinal and other symptoms into diagnostic groups defined by the Pediatric Rome II criteria. Content validity of the QPGS has been demonstrated, and responses to both parent and child versions of the questionnaire are stable over a 2 week period. Psychometric properties and test-retest reliability are reported in another publication (9). In the present study, parents completed Form A, and children 10 to 18 years old completed Form C.

QPGS Scoring for Diagnoses

Diagnoses were derived from computer algorithms reflecting the pediatric Rome II criteria. For each criterion on the QPGS, a response or range of responses reflecting the criterion was determined, and items were transformed into dichotomous variables (0/1: meets/does not meet the criterion). For each diagnosis, a separate algorithm was constructed. Patients meeting all necessary criteria were scored positive for the diagnosis.

The QPGS uses a temporal reference point of the past 3 months for the occurrence of most symptoms. Exceptions are symptoms reflecting the criteria for abdominal migraine and cyclic vomiting, for which the past year is used. The criteria for infants and toddlers were used to score functional constipation but were modified to refer to the past 3 months instead of 2 weeks. For scoring diagnoses of chronic abdominal pain-related disorders, frequency of pain/discomfort had to be “once a week” or more often. This cutoff was recommended by the Rome II Committee on diagnostic criteria of FGIDs in adults (10). For items associated with pain/discomfort, frequency was set at “sometimes” or more often.

Procedure

The study protocol was approved by the Scientific and Ethics Committees of Hôpital Ste-Justine Research Center. The procedure is detailed in the report on the validation of the QPGS (9) and was conducted over 17 months between January 2002 and May 2003. Patients and their parents gave informed consent and completed the QPGS before the child's clinical evaluation by 1 of 11 pediatric gastroenterologists. Clinical evaluations were conducted at the discretion of each gastroenterologist.

Children and parents completed questionnaires in separate clinic locations. A research assistant was present to assist if necessary. Completion of questionnaires took approximately 30 minutes. Physicians did not have access to patient or parent QPGS responses throughout the study.

Statistical Analyses

Convergent validity was assessed by examining the prevalence of Rome II diagnoses in all patients who had been previously classified by physicians as having a functional problem. To examine prevalence of each diagnosis, frequency distributions were computed, and overlaps between diagnoses, when not mutually exclusive, were calculated. For comparisons between age groups of children, chi-square tests were performed, with an alpha level of 0.05. For comparisons of prevalence rates derived by reports of parents and children from the same families, Cohen's kappa coefficients were used. Coefficients of 0.40 to 0.75 were considered fair to good (11).

Internal validity of the disorders defined by the pediatric Rome II criteria was assessed using factor analysis to examine interrelationships among criteria items. Factor analysis was previously used to validate the adult criteria (12,13); however, in those studies, all items included in the symptom checklists were answered by all patients. This approach was not possible in the present study because not all patients answered all QPGS items. Indeed, the QPGS was structured to help respondents focus on the location of symptoms, and therefore several items reoccur in the questionnaire. To minimize the length of completion time, respondents were not required to answer all QPGS items in a section if they responded negatively to the first question in that section. Thus, instead of entering all items into one factor analysis, internal validity in the present study was examined using separate factor analyses for each diagnosis, entering only those items pertaining to the diagnosis. Using this strategy, it was possible to examine clustering of symptoms/features believed to constitute each pediatric Rome II disorder. These analyses were performed for all diagnoses for which there were at least five criteria items.

To ensure sufficient statistical power for these analyses, a general subject-item ratio of 10 to 1 was considered a minimum requirement. Across all factor analyses, the maximum number of items entered was 9, yielding a minimum requirement of 90 patients. The analyses included all 315 patients, including those who had received Rome II diagnoses and those who had not. Instead of the Pearson product moment correlation matrix, the factor analyses used the tetrachoric correlation matrix, which is more appropriate for dichotomous variables. For all analyses, varimax rotation was applied to facilitate interpretation of the factor structure.

RESULTS

Sample Characteristics

Sociodemographic characteristics of study subjects (Table 2) have been described previously (9). Among the 315 subjects, there were 177 (56.2%) 4 to 9 year olds and 138 (43.8%) children/adolescents 10 to 18 years old. Only the 138 older patients gave self-reports.

T2A-7
TABLE 2A:
Sociodemographic information (n = 315 children and parents)
T2B-7
TABLE 2B:
Sociodemographic information (n = 315 children and parents)

Prevalence of FGIDs

Prevalence rates for all Rome II FGIDs derived from parent reports and child self-reports are shown in Table 3. In the younger group, the most prevalent disorders were irritable bowel syndrome (IBS, 22%) and functional constipation (19%). Among children with IBS, 26.4% reported pain in both the upper and lower abdomen. Functional abdominal pain syndrome (FAPS) and abdominal migraine were not diagnosed in younger children.

T3-7
TABLE 3:
Prevalence of Rome II diagnoses in children and adolescents 4 to 18 years classified as functional by pediatric gastroenterologists

Among 10 to 18 year olds, the most prevalent disorder was IBS, diagnosed in 23.9% and 35.5% by parent and child reports, respectively. Among IBS patients, pain/discomfort was in both the upper and lower abdomen for 36.4% according to parents and in 42.9% by child self-report. Although functional fecal retention was prevalent in 2.9% according to parents, it was prevalent in 17.4% by self-report. For both child age groups, the prevalence of FAPS was 0 when frequency of pain/discomfort was scored as “most of the time or always,” as specified by the Rome II criteria, instead of “sometimes.”

Parent-Reported Prevalence of FGIDs in 4 to 9 versus 10 to 18 Year Olds

Chi-square tests showed no statistical difference between younger and older children in parent-reported prevalence on most diagnoses. There was, however, a statistical difference between the two age groups in the prevalence of FAPS, with older children more likely to be diagnosed than younger children (2.9% vs. 0%, P = 0.036). More younger children were diagnosed with functional fecal retention on the basis of parent reports (9.0% vs. 2.9%, P = 0.035).

Concordance Between Parent and Child-Reported Prevalence of Diagnoses in 10 to 18 Year Olds

Concordance between parent and child-reported prevalence varied for the 11 diagnoses, with kappa coefficients high for aerophagia (K = 0.80) and fair for cyclic vomiting syndrome (K = 0.42). IBS and ulcer-like dyspepsia showed concordance coefficients close to acceptable, with kappas of 0.39 and 0.38, respectively. There was low agreement for functional constipation (K = 0.24), functional abdominal pain (K = 0.23), and dysmotility-like dyspepsia (K = 0.13). There was no agreement between parents and children for the diagnoses of abdominal migraine, functional fecal retention, and functional nonretentive fecal soiling (K = −.01 to .02).

Overlap Among Diagnoses

According to Pediatric Rome II criteria, certain disorders by definition are mutually exclusive (Table 1). Because prevalence rates for diagnoses in 10 to 18 year olds were higher by self-report than parent report, the calculation of overlap for that age group was performed based on child self-report. Overlap among diagnoses for the two age groups is shown in Figure 1. Among younger children, the majority of overlaps with other diagnoses were observed for functional fecal retention, IBS, and functional dyspepsia (FD, unspecified type). In the older group, the majority of overlap was accounted for by functional fecal retention with IBS and functional constipation.

F1-7
FIG. 1:
overlap between diagnoses in patients 4 to 9 years (n = 177) and 10 to 18 years (n = 138).

Factor Analyses

Results of factor analyses applied to the five diagnoses for which there were sufficient criterion items are presented in Table 4.

T4-7
TABLE 4:
Factor analysis of Questionnaire on Pediatric Gastrointestinal Symptoms (QPGS) items reflecting pediatric Rome II criteria for functional dyspepsia, irritable bowel syndrome, functional abdominal pain syndrome, and abdominal migraine

FD, ulcer-like.

For ulcer-like dyspepsia, a one-factor solution was produced for both younger and older children, accounting for 50% and 41%, respectively, of explained variance. Factor loadings for individual items ranged between 0.53 and 0.80 for the two groups.

FD, dysmotility-like.

For dysmotility-like dyspepsia, a one-factor solution was found for younger patients, explaining 48% of the variance. Factor loadings ranged from 0.47 to 0.79 in that group. For the older group, two factors accounted for 47% of the variance. The first factor represents pain/discomfort not associated with changes in bowel habits or relief with defecation. The second factor represents symptoms of discomfort.

IBS.

For IBS, a two-factor solution was found for both age groups, explaining 40% and 26% of the variance in younger and older patients, respectively. In younger patients, the first factor includes changes in stool consistency and frequency, whereas the second represents abdominal pain/discomfort. For older children, the factor structure is less well defined. The first factor includes items pertaining to changes in stool consistency/frequency with a slightly lower factor loading for abdominal pain/discomfort. The second factor explains only an additional 3% of variance. For both age groups, relief of pain/discomfort after bowel movements did not load on either factor.

Factor analyses were performed separately for IBS associated with pain/discomfort in the upper and lower abdomen. The two-factor solution for IBS in the upper abdomen for children 4 to 9 years old was similar to that for IBS overall but also included the item pertaining to relief of pain/discomfort with defecation (factor loading = 0.52).

FAPS.

Factor analysis of criteria items for FAPS yielded two factors in both age groups, explaining 44% and 38% of variance in younger and older children, respectively. In the younger group, Factor 1 comprises items reflecting an absence of changes/improvement associated with bowel movement and eating, whereas Factor 2 includes items reflecting pain/discomfort, interference with daily functioning, and a lack of improvement after eating. The factor structure was similar for older children. The item pertaining to pain/discomfort worsening after eating (negatively weighted) did not load on either factor among older patients.

Abdominal migraine.

All items for abdominal migraine showed loadings greater than 0.40. For younger children, two factors emerged, explaining 40% of variance. Symptoms of headache and ocular sensitivity to light clustered to form one factor, whereas other neurologic symptoms and intense pain episodes clustered on the second. Responses of older patients clustered together to form a single factor, with factor loadings between 0.51 and 0.74, accounting for 36% of explained variance.

Analyses of Patients with Abdominal Pain

Pain characteristics.

The majority of the 315 children classified by physicians as having a functional problem reported experiencing abdominal pain/discomfort at some time (88% of younger and 95% of older children). Percent of those who reported pain/discomfort in the upper abdomen was 65.7% and 77.8% in the lower abdomen. Frequency and onset, both included in Rome II criteria for abdominal pain-related disorders, as well as duration and intensity of pain/discomfort are shown in Table 5.

T5-7
TABLE 5:
Characteristics of abdominal pain/discomfort

Between 79% and 85% of patients in both age groups reported pain/discomfort at least once a week. Duration of pain/discomfort was at least 3 months in 76% to 91% of children. Pain/discomfort was transient (less than 1 hour duration) in 27% to 39% of patients and lasted at least most of the day in up to 36%. Intensity was moderate in 35% to 49% of patients and severe or very severe in 38% to 45%.

Prevalence of Criteria Symptoms in Children with Abdominal Pain but without Rome II Diagnoses

Among the 315 patients classified by physicians as having a functional problem, there were 111 (35%) who did not meet Rome II criteria for any of the 11 pediatric diagnoses. Of these, 97 (87%) had had abdominal pain/discomfort during the previous 3 months. Table 6 shows the proportion of these 97 patients meeting the criteria for each item.

T6A-7
TABLE 6:
Patients with abdominal pain/discomfort but without Rome II diagnoses (n=97): Percentage scoring positive for Questionnaire on Pediatric Gastointestinal Symptoms (QPGS) criteria items
T6B-7
TABLE 6:
(continued) Patients with abdominal pain/discomfort but without Rome II diagnoses (n=97): Percentage scoring positive for Questionnaire on Pediatric Gastointestinal Symptoms (QPGS) criteria items

For dyspepsia, IBS, and FAPS, approximately half of patients (41-63%) met the first required criterion of having pain/discomfort at least once a week during the past 3 months. Fewer older patients reported pain/discomfort of more than 3 months duration. Other than pain/discomfort, dyspeptic symptoms were somewhat more prevalent in older children, but the majority of patients in both age groups met remaining criteria concerning absence of change in bowel habits and relief by defecation. For IBS, the percentage of patients in both groups meeting remaining symptom criteria was low, ranging from 0% to 42%. For FAPS, criteria symptoms pertaining to the absence of changes in consistency and frequency of bowel movements were present in most patients. However, absence of improvement after bowel movements occurred less frequently (52% of older patients). In addition, pain/discomfort in relation to eating was absent in most children of both age groups, with the exception of pain/discomfort worsening after eating, which was reported for 54% of younger patients. The two criteria for FAPS concerning interference with school and social/family activities were met by fewer children than the other criteria. For abdominal migraine, approximately one third of patients met the initial criterion item (3 or more episodes of intense pain), but few had the other required symptoms. For the remaining disorders, the proportion of children in both age groups reporting criteria symptoms was generally low.

Effect of Onset on Prevalence Rates for Chronic Abdominal Pain-Related Diagnoses

As with the Rome II criteria, a minimum 3 month period was required before most diagnoses could be made. For IBS, dyspepsia, and FAPS, lowering the cut-off for symptom onset to 2 months or more did not substantially alter the pattern of parent-reported prevalence rates. Diagnoses increased by 2.8% and 5.1% for younger and older patients, respectively. According to self-reports, prevalence of diagnoses increased by 8.0%. Most of the observed increases were accounted for by IBS (5.8%).

DISCUSSION

This study represents the first attempt to validate the Pediatric Rome II criteria. The validation was performed on a clinical sample of pediatric patients referred to a tertiary care center, and therefore results should be interpreted in that context. Indeed, this population is characterized by more severe and prolonged symptoms and an average of more than three previous medical consultations (9).

Results of this study support the validity of some of the pediatric Rome II criteria for FGIDs. The clustering of symptoms specified by the criteria was generally confirmed, and the prevalence of most disorders was consistent with previous research. This study also examined for the first time concordance between diagnoses derived from parent and child reports. Although prevalence rates derived from child self-reports may be more reliable than those of their parents (9), they may in fact be underestimates because children tend to rate onset of symptoms as shorter than do parents. However, when a 2 month criterion cut-off for onset rather than 3 month was used, the increase in prevalence was modest. This suggests that in this population, other criteria are at least as important as symptom onset in determining diagnoses.

Factor analysis and other cluster analytic strategies have been used in the validation of the Rome criteria for adults, using validated bowel symptom questionnaires (12-15). Its application in this study was different from that used to empirically derive symptom clusters from a broad range of gastrointestinal symptom. This study sought to validate previously established symptom groupings proposed by the Pediatric Rome II criteria. Its aim was not to empirically derive symptom clusters, but rather to confirm their presence in a clinical pediatric population. Results of the factor analyses showed that for abdominal pain-related disorders (IBS, FD, FAPS, abdominal migraine), symptom groupings proposed by Rome II were valid. Indeed, there were very few criteria items that did not appear in the factor solutions and the clustering of symptoms when more than one factor emerged was coherent.

The 10% to 15% prevalence rates found for FD are consistent with 15.9% found in a recent study based on parent-reported symptoms (2). These rates are vastly different from the 49.4% reported previously using Rome I diagnostic criteria in a more selected sample in which physicians obtained information from parents (16). Concordance between parents and children was particularly low for dysmotility-like FD. This was probably because parent-child agreement on subjective symptoms is lower than for more observable features (9). Results of the factor analyses for both ulcer-like and dysmotility-like FD strongly support the validity of these diagnoses, as defined by Rome II. One-factor solutions for both subtypes indicate that symptoms of FD constitute a coherent syndrome.

The prevalence of IBS in our study children was slightly lower than the 45% reported in a study from a tertiary care center using the parent report form of the QPGS (2). This is not surprising because children and adolescents were presenting specifically with abdominal pain and not for gastrointestinal symptoms at large. Using Rome I criteria, other researchers have found a prevalence of IBS between 25% and 68%, depending on the diagnostic measure (17,18). The increase in IBS with age in our study has been reported previously. In a community study, high school students were more than twice as likely to receive an IBS diagnosis as were middle school students, according to Rome I criteria for adults (19). In a study of Italian children up to 12 years old in a primary care setting, IBS prevalence using the Rome II criteria was much lower (.2%) (3).

Parent-child concordance for IBS was close to the lower acceptable limit, likely because of parental ignorance of the bowel habits of 10 to 18 year olds. Lack of parental awareness may also explain the higher prevalence of IBS reported by children themselves. The factor analyses for IBS confirmed the clustering of two of the three symptom clusters specified by the Rome II criteria for this disorder. The two factors reflect pain- and defecation-related symptoms. The third criterion, relief with defecation, was not confirmed by the factor analyses. Although IBS was the most prevalent diagnosis found in this study, the fact that patients had to be positive for all symptoms rather than report their absence to meet Rome II criteria may in part explain the lower factor loadings found for IBS than FD.

Results of this study indicate that FAPS is a rarely occurring disorder, occurring in 2.9% of all children. Indeed, the Rome II criteria for FAPS were meant to describe a very limited group of patients with constant pain that could not be modified by any aspect of gastrointestinal functioning. This syndrome is believed to reflect central pain and should not be confused with recurrent abdominal pain, a more commonly occurring and less severe phenomenon (20). In fact, many patients in this study did report severe or very severe pain, and approximately one third of the sample had pain that lasted most of the day or longer. The numerous items that had to be positive for a diagnosis of FAPS reflect the stringency of the Rome II criteria for this disorder. In the recent study conducted in an abdominal pain clinic, FAPS was reported in 7.5% of 4 to 17 year olds (2). In another report of 40 children with incapacitating abdominal pain, FAPS was diagnosed in 38% (8). The low prevalence for FAPS found in the present study reflects the fact that patients were sampled from a general gastroenterology clinic, where FAPS has been encountered over the years but is not expected to be as prevalent as in specialized pain clinics. In addition, because Rome II criteria stipulate that pain/discomfort in the upper abdomen unrelated to defecation constitutes FD, some severe cases of dyspepsia may in fact represent FAPS.

Results of factor analyses for FAPS produced very similar internal structures in both age groups, consisting of two symptom clusters. One factor represented pain, not improved after eating, and interfering with daily functioning. The other factor comprised items related to pain not associated with defecation. The two symptom clusters are consistent with the underlying conceptualization of FAPS, namely, that pain is caused by a centralized mechanism and is independent of gastrointestinal functioning associated with eating and defecation (21). Two items related to the absence of relationship between pain and eating were not strongly interrelated with other symptoms, namely, worsening after eating and pain when hungry/before eating. These questions should be omitted from the diagnostic criteria for FAPS.

In this study, abdominal migraine was prevalent in 2.2% of patients, slightly less than the 4.7% prevalence recently reported in a comparable study (2). Previous epidemiologic studies have found this disorder to be prevalent in 1.7% to 4.1% of children (22,23). The factor analyses for abdominal migraine supported the internal validity of this disorder as defined by Rome II. Among younger children, there were two symptom clusters, whereas in older children, all symptoms clustered together and formed a unitary concept. Although these analyses could not verify the absence of stomach pain between episodes of acute pain and family history of migraine, the other criteria for abdominal migraine were validated.

The only previous report concerning aerophagia pertains to institutionalized handicapped children, a population at high risk for the disorder, where 8.8% of children received the diagnosis (24). The prevalence rate of aerophagia found in this study was 1.3%, and parent-child concordance for this diagnosis was high.

The prevalence of cyclic vomiting syndrome found in this study (2.2-6.2%) was comparable with the 2.3% prevalence rate previously reported for Western Australian children and 1.9% reported for Scottish children, both in community-based studies (25,26). The higher prevalence rate found for younger children in the present study accords with the finding that this disorder is more common in children between 2 and 7 years old (27).

In this study, prevalence of functional constipation was found to be 19.2% in children 4 to 9 and 15.2% in the 10- to 18-year-old group. Previous studies have reported that constipation occurs anywhere from 0.3% to 8.0% in the general pediatric population and that it constitutes 25% of consultations in pediatric gastroenterology (28,29). The fact that parents often could not reliably report on their children's defecation habits is likely an important reason for the low concordance between diagnoses derived from parents' versus children's reports. This problem was also noted in a recent study where parents had difficulty specifically reporting on the form and consistency of their children's stools and stool-withholding behavior (5).

Posturing is the central feature of functional fecal retention, which was diagnosed in 9.0% of younger children and 17.4% of older ones in this study. The unusually high prevalence found based on reports of children and adolescents 10 to 18 years strongly suggests that questionnaire items tapping functional fecal retention were not well understood by this age group and should be rephrased to obtain a more valid estimate of the disorder (9). The large overlap found between functional fecal retention and several other diagnoses also supports this contention. Its overlap with functional constipation in particular raises the question as to whether separate diagnoses are warranted. Functional nonretentive fecal soiling is a more rare disorder, showing a prevalence of less than 1% in this study population. Previous research has documented its prevalence to be as high as 21% in specialized clinics for defecation disorders (5). In those settings, comparisons between Rome II and other diagnostic criteria have indicated that the Pediatric Rome II criteria for defecation disorders are exceedingly restrictive (4,5).

The results of this study can be interpreted from different points of view. On one hand, more than half of children presenting with gastrointestinal symptoms unrelated to organic disease meet pediatric Rome II criteria for FGIDs. However, it is also true that up to 45% are not diagnosed. It is possible that their symptoms are not well enough defined to constitute a syndrome. On the other hand, because most of these children complain of abdominal pain, they might fit into a less strict diagnostic category than FAPS, IBS, or FD. Such a diagnosis may in fact describe a very large group of children that experiences abdominal pain that is occasionally related to eating and defecation but which is not FAPS, IBS, or FD.

In addition to shedding light on the prevalence of FGIDs in a clinical pediatric population, this validation study constitutes preliminary support for the conceptual underpinnings of many of the Rome II criteria defined by pediatric gastroenterologists. Its findings provide important information that can be used to elucidate the characteristics of FGIDs in children and adolescents and to refine both the criteria and methodology used to elicit information from parents and children. It is hoped that the Pediatric Rome II criteria will advance the understanding of the pathophysiology of childhood FGIDs and lead to the development of treatment approaches in pediatrics, as they have already done in the adult domain.

Acknowledgment

The authors gratefully acknowledge the staff of the Division of Gastroenterology, Hepatology, and Nutrition at Hôpital Ste-Justine and Philippe Lambrette for their assistance in the execution of this study. Special thanks to Marc Dumont for his assistance with statistical analyses.

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    Keywords:

    Functional gastrointestinal disorders in pediatrics; Pediatric Rome II criteria; Functional abdominal pain in pediatrics; Irritable bowel syndrome in pediatrics; Functional dyspepsia in pediatrics

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