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Published online before print June 21, 2002, 10.1148/radiol.2242011245
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(Radiology 2002;224:333-337.)
© RSNA, 2002

Pediatric Imaging

Normal Appendix: Is There Any Significant Difference in the Maximal Mural Thickness at US between Pediatric and Adult Populations?1

Václav Simonovsky, MD, CSc

1 From the Ultrasound Unit, 3rd Polyclinic, Príbram, Czech Republic; and Clinic of Imaging Methods, Faculty Hospital Motol and 2nd Medical Faculty of Charles University, Prague, Czech Republic. Received July 23, 2001; revision requested August 24; revision received November 26; accepted January 22, 2002. Address correspondence to the author, U Slávie 34, 263 01 Dobrís, Czech Republic (e-mail: simonovsky@post.cz).


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
PURPOSE: To evaluate the normal maximal mural thickness (MMT) of the appendix in asymptomatic subjects and determine whether any significant difference in MMT exists between pediatric and adult populations.

MATERIALS AND METHODS: The MMT of 187 appendices in asymptomatic subjects was measured at sustained-compression ultrasonography (US). The measured MMTs were categorized into three groups according to patient age (39 young children [including infants] aged 1–6 years, 79 older children and adolescents aged 7–15 years, 69 adolescents and adults aged 16–82 years), and the relationships between categoric variables were analyzed by using analysis of variance and the parametric Scheffé test.

RESULTS: The mean MMTs in the young children, older children and adolescent, and adolescent and adult groups were 1.9 mm ± 0.4 (SD), 2.0 mm ± 0.5, and 2.1 mm ± 0.5, respectively. The corresponding ranges of normal MMT were 1.1–2.8, 1.0–2.8, and 1.2–3.0 mm, respectively. No significant difference in normal appendix MMT was observed between the young children group and the older children and adolescent group (P = .2) or between the older children and adolescent group and the adolescent and adult group (P = .639). The difference in MMT between the young children group and the adolescent and adult group was marginally significant (P = .042).

CONCLUSION: Although adoption of age-related MMT criteria does not seem warranted because it would necessitate measurement precision below 0.5 mm, which is not possible to achieve consistently in daily practice, data indicate that in children aged 6 years or younger, an appendiceal mural thickness of less than 3 mm should be regarded as normal.

© RSNA, 2002

Index terms: Appendicitis, 751.291 • Appendix, US, 751.12989 • Ultrasound (US), in infants and children, 751.12989


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Graded-compression ultrasonography (US) has been proved to be an effective aid in the diagnosis of acute appendicitis. Making an accurate diagnosis is difficult because both normal and abnormal appendices can be depicted on gray-scale US scans.

Measurement of the maximal outer diameter (MOD) is one of the most important morphologic criteria used to identify a normal or abnormal appendix (1–10). This measurement is subject to inherent inaccuracy, however, because noncompressible noninflammatory material in the lumen occasionally can easily cause the diameter to exceed any suggested upper limit of normal (9,11,12). Consequently, one may hypothesize that maximal mural thickness (MMT) as a criterion that can be easily and directly applied in the evaluation of both collapsed-lumen and lumen-distended appendices may be a more specific discriminating marker than MOD.

All measurement limits for a normal appendix, however, are derived exclusively from observations in symptomatic patients who are referred for acute right lower quadrant pain. Most published studies (1–6,8,10,13,14) lack the substantial number of visualized normal appendices that is needed to enable independent comparison with asymptomatic populations. To my knowledge, in no such study, including even those rare investigations that have involved a large number of normal appendices (7,9,11,12,15,16), had the range of dimensions measured in normal appendices been reported with data analyzed according to patient age to evaluate the possible influence of age increase on appendiceal mural thickness.

The purpose of this study was to evaluate the normal MMT of the appendix in asymptomatic subjects and determine whether any significant difference in MMT exists between pediatric and adult populations.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
In a prospective study performed between 1996 and 1999, 411 randomly chosen patients (191 male patients, 220 female patients; age range, 1–82 years; mean age, 16.2 years) were examined at high-frequency transducer US. Most of these patients had been referred for routine abdominal US scanning for reasons other than abdominal pain, such as urogenital tract examination, hepatobiliary disease, screening for or control of congenital abnormality, annual follow-up for cured distant tumorous condition, assessment of nonsevere traumatic condition, and follow-up after trauma. The remaining individuals had undergone soft-tissue US examinations. The basic prerequisite for inclusion in this study was no history of right lower quadrant pain or discomfort for at least 3 months. The ethics committee affiliated with the Faculty Hospital Motol of 2nd Medical Faculty of Charles University, Prague, Czech Republic, approved the study, and informed consent was obtained from all enrolled patients.

The right side of the abdomen was imaged by using the graded-compression US technique described by Puylaert (17) and Jeffrey et al (18). Ten to 15 minutes was allowed to identify the appendix. All examinations were performed with US units (SSA-270A and SSA-340A, Toshiba Medical Systems, Woerden, the Netherlands; SD 800, Philips Medical Systems, Irvine, Calif) equipped with a 7.5-MHz linear-array or convex transducer.

Only the visualized appendices that clearly had a fully collapsible lumen were included in the study. Appendices with lumina that were at some point distended by noncompressible hyperechoic material that was presumed to be of fecal origin (12) were excluded from the study. This exclusion was intended to prevent even the theoretic threat of such material (especially in extreme cases) resulting in wall thinning caused by pressure on the wall and/or in the wrong definition of the mucosal surface (because of the hyperechogenicity of inspissated feces).

The entire lengths of the included appendices were carefully surveyed to determine the MOD. I then made three measurements at zoomed transverse US scanning during sustained appendiceal compression by using electronic calipers and averaged the obtained results. Appendiceal wall thickness was defined as the distance from the hyperechoic luminal interface (ie, collapsed mucosal surface) to the outer hyperechoic line (ie, serosa and subserosal fat)—that is, the distance halfway between the opposite serosal layers (because of the inclusion of only appendices with completely collapsed lumina). Because normal collapsed-lumen appendices are always compressible to some degree and thus exhibit an ovoid configuration on transverse US scans, the smallest anteroposterior outer diameter was selected at the measured point (Figs 1, 2). The exerted compression was considered to be adequate on the basis of visualization of a distinct change in appendiceal shape from round to ovoid. In addition, an anteroposterior diameter not greater than 4 mm in the normal ileal loops in the appendiceal surroundings was considered to be a corroborative marker of sufficient pressure (19). The transducer was handled in a gentle palpating manner to avoid causing the patient pain while the pressure was gradually increased.



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  		Figure 1. Transverse US scan of a normal collapsed-lumen appendix during compression shows characteristic ovoid configuration. Outer diameter is measured as the anteroposterior distance between the opposite hyperechoic serosal layers (ie, between the calipers, 3.5 mm). Appendiceal wall thickness is defined as the distance halfway of the measured distance. The thin central echogenic line corresponds to collapsed mucosal surfaces. Note that the hyperechoic line ventral to the proximal caliper is related to the ileum rather than to the appendix itself. MP = iliopsoas muscle, TI = terminal ileum. (Reprinted, with permission, from reference 12.)

 


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  		Figure 2. Left: Longitudinal US scan of a long segment of a normal collapsed-lumen appendix (between calipers) with a wall that has the typical multilayered structure. Right: Transverse US scan shows a pronounced ovoid configuration of this very easily compressible appendix. The anteroposterior distance between the opposite hyperechoic serosal layers defines the outer caliber (between the calipers, 2.3 mm). The thin central hyperechogenic line represents the collapsed lumen. TI = terminal ileum.

 
The data obtained from these measurements were classified, without regard to patient sex, into three age-based groups: young children, including infants (n = 39; age range, 1–6 years), older children and adolescents (n = 79; age range, 7–15 years), and adolescents and adults (n = 69; age range, 16–82 years). The relationships between the categoric variables were analyzed by using analysis of variance and the parametric Scheffé test (for multiple comparisons). A P value of less than .05 was considered to indicate a statistically significant difference.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
A collapsed-lumen appendix was visualized in 187 (84 male patients, 103 female patients; age range, 1–82 years; mean age, 16.3 years) (45.5%) of the 411 patients (Table). Appendices with a lumen that was distended to a varying degree by noninflammatory hyperechoic material that was presumed to be of fecal origin were observed in an additional 53 patients; however, according to the study protocol, these appendices were excluded.


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  		MMTs of 187 Normal Appendices Visualized at US

 
In all but three patients, the thin appendiceal wall displayed the typical multilayered structure of a bowel loop on the transverse US scan. The mean MMTs in the young children, older children and adolescent, and adolescent and adult groups were 1.9 mm ± 0.4 (SD), 2.0 mm ± 0.5, and 2.1 mm ± 0.5, respectively. The corresponding ranges of normal MMT were 1.1–2.8, 1.0–2.8, and 1.2–3.0 mm, respectively. One hundred two (54.5%) appendices had an MMT of 2.0 mm or less, and 162 (86.6%) had an MMT of 2.5 mm or less. No appendices with a wall thicker than 3 mm were seen in any group. The measured MMTs are presented in detail in the Table and are depicted in a scattergram in Figure 3. No statistically significant difference in normal appendix MMT was observed between the young children group and the older children and adolescent group (P = .2) or between the older children and adolescent group and the adolescent and adult group (P = .639). A marginally significant difference (P = .042) in MMT between the young children group and the adolescent and adult group was observed.



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  		Figure 3. Scattergram illustrates the MMTs in 187 visualized normal appendices plotted against the age of the patients.

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
Because both abnormal and normal appendices can be depicted on gray-scale US scans, the differentiation between them has become a challenging diagnostic problem; specificity of 68%–98% has been reported (1–3,5,6,10,11,13,20,21). One of the most commonly used criteria to preoperatively determine the status of a visualized appendix is the MOD, and the MOD limits suggested to be positive for appendicitis vary between 6 mm or greater and greater than 7 mm (1–10). The MOD is measured as the outer wall–to–outer wall diameter at the widest point of the appendix during transducer compression and is calculated as the sum of both (ventral and dorsal wall) mural thickness readings and the luminal thickness readings at that point. The advantage of such an approach is that it enables one to eliminate any discrepancies that result from trying to identify the mucosal surface within the appendix, and, most important, to include any noncompressible material secondary to acute appendicitis as pus in empyema. However, this determination implies that any noncompressible material will subsequently have a serious effect on MOD value; also noninflammatory contents, as to some degree inspissated feces (which may possibly be present at some point of appendiceal course) (11,12) or mucoid (in patients with cystic fibrosis) (9). As a result, there is the potential for inherent MOD measurement inaccuracies in the form of false-positive findings, because inspissated fecal material in particular can easily result in a diameter that grossly exceeds any adopted upper limit of normal at that place (11,12). In this regard, it is important to remember that this nonshadowing fecal material is not equivalent to loose feces, which can be easily compressed out of a normal patent lumen and are often associated with some amount of fluid that further facilitates their removal, or to the classic shadowing appendicolith, the presence of which strongly indicates possible appendicitis, regardless of the MOD, according to some investigators (1,20,22–24). Logically, noncompressible materials have the same devastating effect on the depiction of appendiceal compressibility that they have on MOD specificity; in this particular subset of normal appendices, this finding will constantly fail as a qualitative distinguishing feature of a normal appendix.

The inaccuracy of MOD measurement was confirmed recently in studies performed by Rettenbacher et al (15) and Lowe et al (10). Rettenbacher et al (15) measured MODs of 7 mm or greater in 9% (21 of 240) of the control subjects. On the basis of their overall data, they concluded that the 6-mm MOD criterion is surprisingly more useful for excluding rather than confirming acute appendicitis. However, despite their reports of grossly abnormal values for some of the normal appendices (up to 13 mm), no relevant explanation for the causes of these findings was given, although endoluminal inspissated feces might be the most probable explanation. Lowe et al (10) visualized six appendices that were false-positive for appendicitis; the MODs ranged from 6.2 to 8.0 mm. As in the Rettenbacher et al investigation, no morphological explanation for these false-positive findings was reported in the Lowe et al study.

Because of MOD measurement limitations, one can hypothesize that MMT as a criterion that can be easily applied in the evaluation of both collapsed-lumen and lumen-distended appendices may be a more specific discriminating marker of appendix normality or abnormality. As such, MMT may be a useful adjunctive measurement, especially in the examination of patients in whom presumed noninflammatory endoluminal material is visualized. The MMT limits proposed to be positive for appendicitis in the literature (2,11–13,18,20) are greater than 2 mm and greater than 3 mm; the latter limit is used more commonly because of its considerably higher specificity. However, even this limit lacks 100% sensitivity: There have been verified cases of appendicitis in which the outer luminal diameter was 6 mm or less, which may be considered as equivalent to an MMT of 3 mm or less in collapsed-lumen appendices (1,12,14–16,25). In most of these reports, however, the quantity of data is not sufficient to determine whether the cases were more frequent in a particular age group or were evenly distributed regardless of age.

All MMT and MOD limits of normal are derived exclusively from examinations performed in symptomatic patients who are referred for US because of acute right lower quadrant pain. However, there are several ways to introduce potential inaccuracies into the measurement criteria of normality that are derived from such studies. First, although the results of some studies (7,11,12,16) show that a normal appendix can be depicted at US more often than has been reported, the descriptions of encountered normal appendices in these studies are limited to the statements of not meeting the selected criterion of pathology used in these studies. However, there is no reliable way to confirm that all of the clinically normal appendices (ie, those not addressed surgically) visualized in symptomatic patients would be normal at histopathologic analysis if surgery were performed. Some of these cases might represent unrecognized self-limiting acute appendicitis. The concept of spontaneously resolving appendicitis, although disputed in the past, is currently supported by an abundance of evidence (1,3,5,6,8–12,16,26). Second, in a symptomatic patient the presence of small (but nevertheless measurable with use of a precision scale of 0.1 mm) acute and/or residual appendiceal inflammatory wall changes is always possible, even when acute appendicitis is not present at the time of examination. The presumed mechanism of such appendiceal wall thickening (in itself not related to acute appendicitis) is sympathetic mural edema, which is a manifestation of secondary reactive changes that develop in the vicinity of the original problem (16,22). With regard to the residual appendiceal wall thickening, one can expect this to result from previous episodes of spontaneously resolved appendicitis (discussed earlier herein) or from an aborted episode of chronic appendicitis (1,3,5,8–12,16,25,26). A final potential drawback that is inherent of these MMT and MOD limits is that they are derived mostly from studies performed in unselected groups comprised mostly of adults, with no emphasis on the values obtained in children.

Thus, there is completely missing the comparative view from the other side of the employed threshold—that is, an investigation of the margins of normality upon observations in a completely asymptomatic population and with emphasis on analysis of data obtained in individuals of various ages. In addition, although it is generally accepted that appendiceal morphologic criteria can be used independently of age, to my knowledge, before this investigation, no study to compare findings in adult and pediatric populations had been performed. The available related data, with the exception of those obtained by Hahn et al (9) and Rettenbacher et al (15), are lacking.

Hahn et al (9) reported a mean normal MOD of 3.9 mm ± 1.2 in a series of 54 asymptomatic subjects aged 1–19 years. The mean MMT in their young subjects (1.9 mm ± 0.6, derived from MOD) was similar to that in the present study, in which the obtained values (1.9 mm ± 0.4, 2.0 mm ± 0.5, and 2.1 mm ± 0.5) were classified into three age-based groups. Rettenbacher et al (15) reported a mean MOD of 4.7 mm ± 1.51 in 240 adult control subjects. However, because the range of MODs in these cases varied considerably (2–13 mm) and no relevant explanation for the cause of the abnormally wide appendices was given (15), no direct comparison with the findings in the present study can be drawn.

In addition to serving as supplementary data to those previously published, the results of the present study show that MMT differences among the studied age groups are not statistically significant, except when the findings in young children are correlated with those in adolescents and adults (P = .042). Consequently, from a practical standpoint, it follows that when such marginal statistical significance combined with the mean MMT difference detected between these boundary age groups (0.2 mm) is considered, one may conclude that adopting clear-cut defined age-related MMT thresholds does not seem to be warranted because it would necessitate measurement precision that is considerably below 0.5 mm, which is hard to achieve consistently in daily clinical practice. Despite this, the data obtained in healthy populations suggest that in children aged 6 years or younger, as opposed to older children and adults, the appendiceal mural thickness should be regarded as normal only when it is less than 3 mm.

Although MMT evaluation can be considered a valuable index of the status of the visualized appendix in patients suspected of having appendicitis, it should be emphasized that the highest diagnostic accuracy can be accomplished only by regarding several US criteria simultaneously. Therefore, in addition to appendix measurements, evaluation of numerous additional criteria, such as presence or absence of periappendiceal inflamed fat (4,11,22,24), tenderness at the site of the appendix (5,7,11,22,24), and hyperemia at power or color Doppler US (14,16,25), should be a routine part of the examination of the appendix.

In this study, every attempt was taken to make the patient cohort as homogeneous as possible. In addition to excluding those patients who could have introduced acute and/or residual wall thickening into the analysis (although I recently documented that I observed no significant difference in mural thickness between normal appendices with collapsed lumens and those with lumens distended by noncompressible noninflammatory fecal material [12]), to prevent even the theoretic threat of such material (especially in extreme cases) resulting in wall thinning caused by pressure on the wall and/or the wrong definition of the mucosal surface (because of the hyperechogenicity of inspissated feces), I included only appendices with a clearly collapsed lumen in this study.

Even with these precautions, however, the study had inherent limitations. First, the mural dimensions were measured on a scale of 0.1-mm measurement accuracy. In theory, the axial resolution limit at US equals a half pulse length; thus, with a 7.5-MHz frequency (wavelength of 0.205 mm), the axial resolution limit is about 0.1 mm (27,28). However, due to technology limits, an axial resolution of about 0.2 mm may be expected in actual clinical practice. In addition, three different US scanners from two manufacturers were used, and the identical measurement precision of these scanners to the scale of that used cannot be warranted. Second, because mural thickness may vary slightly within the length of even a normal appendix, despite the effort exerted to determine a maximal thickness point, in all cases a definitive measurement can only be attempted.

Third, measurements of the appendix generally are hindered by the difficulty in ensuring an adequate control of a sufficient degree of compression and the necessity to use a different degree of compression in heavier versus thinner patients. Fourth, despite questioning the patient or individuals accompanying him or her about whether he or she had experienced right lower quadrant pain or discomfort during the last 3 months, recently healed appendicitis in an asymptomatic individual cannot always be reliably excluded. Finally, none of the patients, who were asymptomatic with regard to the purposes of this study, underwent surgery for acquisition of histopathologic proof of a normal appendix. In addition, there was no clinical follow-up to determine whether right lower quadrant problems developed any time after the US examinations.

In conclusion, the data obtained in an asymptomatic population confirmed the initial expectation that there is an age-related difference in mean MMT; however, this finding was not shown to be significant, except when the results obtained in young children were correlated with those obtained in adolescents and adults (P = .042). Although adopting clear-cut defined age-related MMT thresholds was not found to be warranted, the data suggest that in children aged 6 years or younger, the appendiceal mural thickness should be regarded as normal only when it is less than 3 mm.


   ACKNOWLEDGMENTS
 
I thank Marie Hladíková, magister, of the Department of Medical Informatics at the 2nd Medical Faculty of Charles University, Prague, Czech Republic, for statistical analysis.


   FOOTNOTES
 
Abbreviations: MMT = maximal mural thickness, MOD = maximal outer diameter

Author contribution: Guarantor of integrity of entire study, V.S.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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