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AJR 2002; 178:445-450
© American Roentgen Ray Society


Sonographic Detection of Lymph Nodes in the Intussusception of Infants and Young Children

Clinical Evaluation and Hydrostatic Reduction

C. Koumanidou1, M. Vakaki1, G. Pitsoulakis1, K. Kakavakis1 and P. Mirilas2,3

1 Department of Radiology, "Agia Sofia" Children's Hospital, Thivon and Mikras Asias Sts., Goudi, 11527 Athens, Greece.
2 First Department of Pediatric Surgery, "Agia Sofia" Children's Hospital, 11527 Athens, Greece.
3 Department of Anatomy-Embryology, University of Crete Medical School, P.O. Box 1393, Herakleion, 711 10 Crete, Greece.

Received April 30, 2001; accepted after revision August 22, 2001.

 
Address correspondence to C. Koumanidou.


Abstract
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
 
OBJECTIVE. Our aim was to assess the sonographic appearance of enlarged lymph nodes in the intussusception in infants and young children and to investigate whether the enlarged lymph nodes affect the hydrostatic reduction rate of intussusception.

MATERIALS AND METHODS. This retrospective case control study included a total of 65 children with intussusception, consisting of two groups: a study group of 28 patients with lymph nodes detected in intussusception and a reference group of 37 patients of similar age without lymph nodes in intussusception. The selection criterion for the study group was the presence of a minimum of two lymph nodes, of which at least one had a long axis of 11 mm or greater. The intussusception patterns, target or doughnutlike, and the presence of trapped fluid in the intussusception were also evaluated. Clinical records were reviewed for associated disease. The reducibility of both study and reference groups was assessed and correlated with all the sonographic features mentioned.

RESULTS. Twenty-two of the 28 patients in the study group and none in the reference group had a recent or a current history of gastroenteritis. The overall hydrostatic reduction rate was 46.4% in patients with enlarged lymph nodes in the intussusception and 81.1% (p < 0.005) in patients without enlarged lymph nodes in the intussusception. Larger rather than numerous lymph nodes significantly affected the reducibility rate. Most of the reference group patients had a hydrostatic reduction at first attempt, whereas a second attempt at hydrostatic reduction was required in most of the study group patients.

CONCLUSION. Enlarged lymph nodes in the intussusception are mainly found in patients with a current or recent history of gastroenteritis and decrease the overall hydrostatic reduction rate.


Introduction
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
 
The role of sonography in the diagnosis of intussusception is well established, with a sensitivity of 98-100% and a specificity of 88-100% [1,2,3,4,5,6]. Conventional radiography is of limited value in the diagnosis of intussusception, and it is used only to examine the coexistence of complications such as pneumoperitoneum or intestinal obstruction. It has been postulated that sonography should be the initial imaging modality and that the barium enema should be performed only for therapeutic reasons [1, 2, 4, 7,8,9]. Investigators have mainly focused on sonographic signs indicative of reducibility in an attempt to reduce the risk of complications resulting from a vigorous hydrostatic reduction of gangrenous bowel.

Different predictors of reducibility in sonograms have been evaluated and have become subjects of discussion and controversy [2, 5, 10]. The target appearance of intussusception, consisting of multiple concentric rings surrounding an echogenic center, has been considered a sign of reducibility because this appearance is related to a lesser degree of vascular compromise [8]. In contrast, a thick hypoechoic rim (> 10 mm) in the doughnut appearance of the intussusception [1, 11], the presence of trapped intraperitoneal fluid in the intussusception [7], and the absence of blood flow in the intussusceptum [5, 12, 13] have all been related to irreducibility.

In this article, we present a new sonographic sign of intussusception predicting irreducibility. Enlarged mesenteric lymph nodes are found during abdominal sonography in infants and children with acute gastroenteritis and acute abdominal pain [14]. Additionally, we observed that in most infants and children with a current or recent history of gastroenteritis who developed intussusception, a number of lymph nodes were identified in the intussusception and a lower hydrostatic reduction rate was seen in such cases. We therefore conducted a retrospective case control study involving two groups of children affected by intussusception—those with sonographically detected lymph nodes in the intussusception and those without lymph nodes—to assess this finding and to correlate it with the hydrostatic reduction rate.


Materials and Methods
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
 
This retrospective case control study was carried out over a 28-month period, from October 1998 to February 2001. Sixty-five patients, with an age range from 5 to 28 months (mean age, 20 months), were enrolled in the study. The study included the following two groups: a study group of 28 patients (10 girls and 18 boys; age range, 5-26 months; mean age, 19.1 months) with lymph nodes detected in the intussusception and a reference group of 37 patients (19 girls and 18 boys; age range, 6-28 months; mean age, 20.5 months) without lymph nodes in the intussusception. The study and reference groups included patients of similar age who were not age-matched. Abdominal radiographs with the patient in erect or supine positions were obtained in all patients to exclude the presence of free peritoneal air or small-bowel obstruction.

Sonograms using broadband 5- to 8-MHz micro-convex and 5- to 12-MHz linear array transducers (HDI 5000; Advanced Technology Laboratories, Bothell, WA) and a 7-MHz linear array transducer (LOGIC 400; General Electric Yokagawa Medical Systems, Tokyo, Japan) were obtained in all patients. The entire abdomen was examined in the transverse and longitudinal planes. Sonographically, the presence or absence of the following characteristics was noted: the demonstration of the intussusception as a targetlike mass consisting of multiple concentric rings surrounding an echogenic center; the appearance of a doughnutlike mass corresponding to the intussusception in transverse planes, consisting of a hypoechoic peripheral rim and a hyperechoic center; and the detection of trapped fluid, such as a crescent hypoechoic area, in a target or doughnutlike mass.

All sonographic patterns of intussusception were examined particularly for the presence of enlarged lymph nodes. The number and long-axis measurement of lymph nodes were evaluated.

Selection Criteria
The study group included cases with a minimum of two lymph nodes in the intussusception, of which at least one lymph node had a long axis of 11 mm or greater. The reference group included patients with no lymph nodes in the intussusception. Patients with a single large lymph node or multiple nodes less than 11 mm were excluded from this study. We selected only patients who had a minimum of two lymph nodes because, according to our experience, one lymph node was found occasionally and did not correlate with the patient's gastroenteritis history or reduction outcome. Furthermore, we evaluated these lymph nodes only when the long axis of at least one of them measured equal to or more than 11 mm, because mesenteric lymph nodes less than 11 mm were not considered pathologically enlarged because they had been observed in asymptomatic children [14]. Considering that these mesenteric lymph nodes could enter in the intussusception, we regarded 11 mm as the lower limit of their longest axis. Only patients with a prompt blood flow in the intussusceptum were selected for both the study and reference groups.

A barium enema was performed in all children within an hour after the sonographic diagnosis of intussusception. The "rule of three" (three hydrostatic reduction attempts, each 3 min in duration and with a barium column height of 3 ft [1.35 m]) was strictly followed during the reduction procedure. Radiologists who attempted the hydrostatic reductions did not perform the sonographic examinations, and they were unaware of the sonographic presence of enlarged lymph nodes in the intussusception and the patient's history of gastroenteritis, which eliminated the potential selection bias. A postevacuation radiograph was obtained to document successful reduction when it was necessary. All patients in whom the hydrostatic reduction failed underwent surgery with manual management of the intussusception or segmental bowel resection.

Clinical records were reviewed for associated disease and presenting symptoms and their duration. The findings of the physical examination by a pediatric surgeon were recorded. Imaging studies, hydrostatic reduction results, and operative records were also reviewed. Sonographic data were also correlated to pathology reports in all operated children in whom enterectomy was performed.

Statistics
The chi-square test was applied to correlate the presence of lymph nodes in the intussusception, sonographic appearance, and hydrostatic reduction outcome. A power of 0.8 was chosen to avoid false-positive results and consequently a p value of less than 0.05 was considered significant. Taking into account the failed reductions with the cases and the lymph nodes present in the intussusception as the risk factor, we estimated an odds ratio for this case control study. The chi-square test was also applied to noncontinuous variables to assess the statistical significance of the presence or absence of the sonographic features of the intussusception pattern. A Yates correction was applied to the chi-square test when appropriate. When the expected number of each cell was less than five, exact binomial probabilities were computed using the Fisher's exact test in place of the chi-square test. To test the correlation of the largest lymph node length with the reduction outcome in the study group, we used an unpaired t test.


Results
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
 
The study group included 28 patients with intussusception in whom lymph nodes were sonographically detected in the intussusception. Twenty-two of the patients had a current (n = 8) or recent (i.e., 5-8 days after the clinical cure of the disease) history of gastroenteritis (n = 14), and six patients had no history of gastroenteritis or symptoms directly suggesting intussusception. All patients with gastroenteritis presented with fever, vomiting, and diarrhea, which indicated a low clinical suspicion of intussusception.

The reference group included 37 patients with intussusception but without lymph nodes: 19 patients with a high clinical suspicion of intussusception (abdominal pain, currant jelly stool, and palpable abdominal mass) and 18 patients with atypical symptoms of diarrhea or restless behavior. Ten of the 18 patients had atypical symptoms of diarrhea but neither fever nor vomiting; C-reactive protein and WBC were found within the normal range in these patients. The remaining eight patients had restless behavior. Except for children with current gastroenteritis, the duration of symptoms was less than 24 hr in both the study and reference groups.

Supine radiographs showed a large amount of air in an otherwise normal bowel (adynamic ileus) in the eight patients with current gastroenteritis. In the 14 patients with a recent history of gastroenteritis, nonspecific signs were found on conventional abdominal radiography, except for four patients in whom the findings were indicative of intussusception. From the 43 patients without a history of gastroenteritis, only eight had radiologic features specific to intussusception, such as the presence of a soft-tissue mass or meniscus sign in the right quadrant.

Lymph nodes sonographically detected were contiguous. They were all detected at the base of the intussusception (proximally in the longitudinal section), with a large amount of hyperechoic mesentery. We did not find the lymph nodes in the intussusception apex (distally in longitudinal section) in which the mesentery was minimal. Nodes were noted in all sonographic intussusception patterns in the study group.

On transverse sonographic scans, the intussusception pattern appeared as a targetlike mass consisting of multiple hypoechoic concentric rings surrounding an echogenic center in six patients from the study group (Figs. 1 and 2) and in six patients from the reference group (Fig. 3); as a doughnutlike mass consisting of a hypoechoic external ring and an echogenic center in 17 patients from the study group (Fig. 4) and in 25 patients from the reference group (Fig. 5); and as a hypoechoic crescent area representing trapped fluid in the intussusception with a target or doughnutlike appearance in five patients from the study group (Fig. 6) and in six patients from the reference group. Operative records noted that fluid was observed coming out of the base of the intussusception in patients with trapped fluid.



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Fig. 1. 8-month-old male infant with intussusception and recent history of gastroenteritis; hydrostatic reduction failed. Transverse sonogram of right mid abdomen is presented. Intussusception is shown as targetlike mass, consisting of multiple concentric rings. Five lymph nodes are revealed in hyperechoic mesentery. Long axis measures 11 mm in two lymph nodes (arrows), whereas three measure less than 9 mm (arrowheads). Trapped fluid was not detected.

 


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Fig. 2. 20-month-old boy with intussusception and recent history of gastroenteritis; hydrostatic reduction was successful. Transverse sonogram of right upper abdomen shows targetlike mass, representing intussusception, consisting of multiple concentric rings surrounding echogenic center. Three enlarged lymph nodes are present in intussusception (arrows). Largest lymph node measures 11 mm at its long axis. Trapped fluid is not detected.

 


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Fig. 3. 16-month-old girl with intussusception and no history of gastroenteritis; hydrostatic reduction was successful. Typical sonogram of target appearance of intussusception is shown, in which multiple concentric rings are clearly visible. No lymph nodes are revealed in intussusception's echogenic center.

 


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Fig. 4. 11-month-old male infant with intussusception and current gastroenteritis history; hydrostatic reduction failed. Transverse sonogram of right upper abdomen reveals doughnutlike appearance of intussusception. Intussusception's external hypoechoic ring is thick. Four lymph nodes are seen in intussusception (arrows). Largest lymph node length was 12 mm.

 


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Fig. 5. 6-month-old male infant with intussusception and history of gastroenteritis. Enema reduction was successful. Transverse sonogram of right mid abdomen shows typical doughnutlike appearance of intussusception. Hypoechoic outer rim is thick (arrowheads). Encircled by outer rim, structure consists of hyperechoic crescent-shaped center, which represents entrapped mesentery, eccentrically surrounded by heterogeneously hypoechoic area that is formed by central limb of intussusceptum, probably including cecoappendiceal complex. Hypoechoic dots in hyperechoic mesentery represent vessels. No lymph nodes are revealed in intussusception.

 


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Fig. 6. 6-month-old female infant with intussusception and history of gastroenteritis. Transverse Doppler sonogram of right mid abdomen reveals small crescent hypoechoic area representing trapped intraperitoneal fluid (arrow) and three lymph nodes in intussusception (large arrowheads). Largest lymph node had length of 13 mm. Intussusception was ileo-ileocolic. Hydrostatic reduction failed because of the following current characteristics: trapped fluid, enlarged nodes, and ileo-ileocolic nature. Other two hypoechoic areas correspond to vessels as shown (small arowheads).

 

Results of success in hydrostatic reduction for all the sonographic features of intussusception are summarized in Table 1. An estimated odds ratio implied that the selected patients with lymph nodes had a 4.9-fold risk for reduction failure. The overall reduction rate was significantly lower in children with lymph nodes in the intussusception, as selected by the criteria set (xldf2 = 8.55, p < 0.005). A Fisher's exact test failed to show significant reduction differences with the intussusception patterns depicted in Table 1. Also, a chi-square with a Yates correction applied to the doughnut subgroup as a total, without infragroups according to the hypoechogenic external ring thickness, failed to show a significant difference. The Fisher's exact test failed to discriminate between the reduced populations and the doughnutlike pattern with and without trapped fluid in both patients with lymph nodes (p = 0.311) and those without lymph nodes (p = 0.355).


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TABLE 1 Rate of Hydrostatic Reduction in Relation to Presence of Lymph Nodes in Intussusception

 

The number of attempts for a successful hydrostatic reduction are shown in Table 2. There was a significant difference in the number of attempts required between the study and reference groups (x2df2 = 7.375, p = 0.025). Most of the patients without lymph nodes underwent a successful hydrostatic reduction at the first attempt, whereas most of the patients with enlarged lymph nodes required a second attempt.


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TABLE 2 Successful Intussusception Reduction in Patients With and Without Enlarged Lymph Nodes in Intussusception

 

The number and the long-axis measurement of lymph nodes in the study group are shown in Table 3. A chi-square test failed to discriminate between failed and successful reductions in patients with less than three lymph nodes and three or more lymph nodes in the intussusception (xldf2 = 0.48, p = 0.488), implying that the lymph node number may not be associated with the reduction outcome. In all intussusception patterns, the long axis of the largest lymph node measured 11-14 mm. In one case, a fourth small lymph node was found, and in another case, two small lymph nodes were found. In cases with successful reduction, the largest node had a long axis of 11-12 mm. An unpaired t test conducted on the maximal lymph node length in each patient from both groups (Table 1) revealed a significant difference in the variable between the patients with failed reduction and those with successful reduction (t = -3,751, df = 26, p = 0.0008). This finding suggests that the maximal lymph node length is a variable indicating reduction failure. In contrast, the average lymph node length in each child may not be related to the reduction outcome (t = 1.181, df = 26, p = 0.243).


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TABLE 3 Sonographic Measurements of the Longest Axis of Each Lymph Node Detected in Intussusception in the Study Group

 

Additionally, enlarged mesenteric lymph nodes in the right abdomen were sonographically detected in all children (in the study group) with enlarged lymph nodes in the intussusception. The number of lymph nodes was more than four, and the long axis of at least three of them was more than 10 mm. In 26% of the patients from the reference group, more than three mesenteric lymph nodes were sonographically visualized in the right abdomen, with at least two of them having a long axis more than 10 mm.

Intussusception was ileocolic in 62 patients and ileo-ileocolic in two patients without a history of gastroenteritis and in one patient with a history of gastroenteritis (trapped fluid and three enlarged lymph nodes were also recognized in the latter patient [Fig. 6]). No bowel perforation occurred during the hydrostatic reduction attempts. In all patients, no other lead point except the enlarged lymph nodes was recognized during the sonographic examination, hydrostatic reduction, or surgery. Intraoperative findings verified the presence of lymph nodes at the base of the intussusception and their measurements, as previously recorded.


Discussion
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Abstract
Introduction
Materials and Methods
Results
Discussion
References
 
The present study clearly shows that the sonographic presence of enlarged lymph nodes in the intussusception is a predictor of hydrostatic irreducibility. The children who were studied had a minimum of two lymph nodes with at least one measuring 11 mm or more at its long axis. Most of the study group patients had a history of current or recent gastroenteritis. Enlarged mesenteric lymph nodes were also found sonographically in the right abdomen in all the children (in the study group) with lymph nodes in the intussusception. In patients with failed reduction, operative findings verified that lymph nodes were present on sonography.

Most of the cases of intestinal intussusceptions that occur during childhood are considered to be idiopathic, resulting from hyperplasia of lymphoid tissue in the distal ileum [9, 15, 16]. Otherwise, the incidence of a pathologic lead point in intussusception is low, ranging between 1.5% and 12%, and is related to the patient's age [17]. A predisposing infection has long been considered to contribute to the development of intussusception in some cases. In 20% of intestinal intussusception cases, the patients had a history of viral gastroenteritis or upper respiratory infection [18]. Most patients in our study group had a recent or current history of viral gastroenteritis. A viral intestinal infection would produce enlargement of lymphoid tissue, especially in the ileum. In our study, enlarged mesenteric lymph nodes were a common finding in all the patients from the study group and were found in 26.3% of the patients from the reference group. Enlarged mesenteric lymph nodes in children with gastroenteritis and intussusception, and with other abdominal diseases, have been well documented [14, 19]. Such enlarged mesenteric lymph nodes have been suggested to act as a lead point in intussusception [18]. Mesenteric lymph nodes may not only provoke intussusception but may also be trapped with mesentery in the intussusception [9, 20]. This sequence of events explains how enlarged lymph nodes are found at the base of intussusception, especially in patients with an intestinal viral infection. Our results may well represent the end step in a series of events reflecting lymphoid tissue implication in the genesis of intussusception in children.

The presence of lymph nodes on sonographic scans is easily depicted in the hyperechoic mesentery (Fig. 2). The mesentery is dragged between the entering and returning limb of intussusceptum at the base of the intussusception where its amount is maximal, and it is absent at the apex [6, 9].

The hydrostatic reduction rate was dramatically decreased when lymph nodes were found sonographically in the intussusception. The lymph nodes act as a wedge, together with the edematous mesentery, impeding the exit of intussusceptum. We found that the largest lymph node length was a prominent indicator for a poor reduction, whereas the average lymph node length in each child may not be associated with the reduction outcome. Therefore, we consider that the main reduction obstacle is the size rather than the number of lymph nodes. For children without lymph nodes in the intussusception, the overall reduction rate presented and the reduction rate of each pattern group are aligned to those previously reported in a larger series from our center [21].

Although the overall reduction rate results could not be statistically verified in each one of the intussusception patterns because of the low number of patients included, the subgroups' reduction rate row data deserve comment. The targetlike appearance of the intussusception on sonography represents less edematous intussusception followed by easy reduction. Although all our reference group patients with the target pattern of intussusception had a successful hydrostatic reduction when lymph nodes were encountered in the target intussusception pattern, only one third of the study group was reduced. In these patients, it seems that lymph nodes at the base of the intussusception, in the absence of severe edema, are the principal reduction obstacles. In the doughnutlike mass pattern, the edema of the intussusceptum and intussuscepiens layers can well be surpassed in children without lymph nodes trapped in the intussusception, whereas in the study group, the presence of enlarged lymph nodes in the intussusception resulted in a half rate success of hydrostatic reduction in such cases. Finally, trapped fluid in the intussusception has consistently been regarded as an index of irreducibility [7, 21], probably signaling an already highly congestive situation and an ischemia further worsened by lymph nodes in the intussusception.

In conclusion, our study supports the theory that a viral infection induces lymph node hypertrophy, which can then act as a lead point for intussusception. The consistent finding of enlarged mesenteric lymph nodes is reflected in the intussusception. Lymph nodes in the intussusception are considered a sign of irreducibility. The only criterion prohibiting a hydrostatic reduction attempt is the absence of blood flow in the intussusceptum. We considered that the presence of enlarged lymph nodes in the intussusception was not a criterion by itself because we still had a 46.4% reduction rate in the study group. The presence of enlarged lymph nodes should be taken into account, with other sonographic criteria, as the coexistence of a thick hypoechoic ring in the doughnut intussusception pattern and the presence of trapped fluid in the intussusception. According to our results, radiologists should be alert when large lymph nodes, 11 mm or greater, are found in the intussusception at a half rate reduction and mostly at a second attempt. Certainly, further study, including more patients, is necessary to substantiate our results and to prove their validity separately for each of the intussusception sonographic patterns, a goal not achieved.


Acknowledgments
 
We thank Dominique Lagragne, National Institute of Agronomy, Paris-Grignon, France, for her assistance with the statistical analysis.


References
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
 

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