Tuberculosis (TB) has re-emerged as a serious public
health problem in developed countries, particularly among young adults and children. The diagnosis of TB in children is often dicult to conrm, because Myco- bacterium TB is cultured only in a small percentage of cases [1, 2]. Whereas the diagnosis of active TB in adults is mainly bacteriological, in children it is usually epide- miological and indirect. In the absence of a positive culture, the strongest evidence for TB in a child is recent exposure to an adult with active disease [3]. Indirect diagnostic techniques, such as the tuberculin skin test, chest radiography and physical examination oer sup- portive information [4]. Central to the clinical diagnosis of childhood TB is the chest radiograph and the presence of lymphade- nopathy with or without parenchymal involvement is the single most important diagnostic feature [4]. The nodal enlargement typically involves the hilar and paratracheal nodes, with bilateral hilar lymphadenopathy identied in about 25% of cases. Dierent studies have docu- mented right-sided predominance of lymphadenopathy and parenchymal changes [5]. Both frontal and lateral views are necessary to evaluate lymphadenopathy. Of interest is the fact that enlarged lymph nodes may be Joaquim Bosch-Marcet Xavier Serres-Cre ixams Amalia Zuasnabar-Cotro Xavier Codina-Puig Margarita Catala` -Puigbo Jose L. Simon-Riazuelo Comparison of ultrasound with plain radiography and CT for the detection of mediastinal lymphadenopathy in children with tuberculosis Received: 21 February 2004 Revised: 1 April 2004 Accepted: 11 May 2004 Published online: 9 September 2004 Springer-Verlag 2004 Abstract Background: Lymphade- nopathy, with or without parenchy- mal abnormality, is the radiological hallmark of primary tuberculosis (TB) in children. However, lymph node enlargement may pass unde- tected on plain chest radiographs. Ultrasonography provides comple- mentary information to that ob- tained by radiographs. Objective: To assess the clinical value of US for the detection of mediastinal lymphade- nopathy in children with a positive intradermal tuberculin test. Materi- als and methods: Thirty-two children with a mean age of 6 years and a positive Mantoux test underwent chest radiography (frontal and lat- eral) and US (suprasternal and left parasternal access routes). Chest CT was performed at the discretion of the attending physician in six cases. Results: Eleven children had clinical symptoms and 90% a recent contact with a person with active TB. In 90.5% of children with chest radio- graphic images compatible with TB, coincident ndings in the mediasti- nal US study were found. By com- parison, 66.7% of those with normal chest radiography had evidence of mediastinal lymphadenopathy on the US scan. In all cases but one, US and CT ndings agreed. Conclu- sions: Mediastinal US is useful for the detection of enlarged lymph nodes in children with a positive tuberculin reaction and normal chest radiography. Keywords Mediastinum TB Lymphadenopathy Radiography Ultrasound CT Children Pediatr Radiol (2004) 34: 895900 DOI 10.1007/s00247-004-1251-3 ORIGINAL ARTICLE J. Bosch-Marcet (&) A. Zuasnabar-Cotro M. Catala` -Puigbo J. L. Simon-Riazuelo Department of Paediatrics, Avda. Francesc Ribas s/n, Hospital General de Granollers, 08400 Granollers, Barcelona, Spain E-mail: 8543jbm@telefonica.net Tel.: +34-93-8425039 Fax: +34-93-8425036 X. Serres-Cre ixams Department of Diagnostic Imaging, Hospital General de Granollers, Barcelona, Spain X. Codina-Puig Emergency Department, Hospital General de Granollers, Barcelona, Spain detected by ultrafast CT in 60% of children with tuberculous infection and normal ndings on chest radiography [6]. However, this technique would not be available in most cases and the cost is very high. We report the clinical value of US to detect mediastinal lymph node involvement in children with a positive intradermal tuberculin skin test. Materials and methods A retrospective review of the medical records of 32 chil- dren, 17 boys and 15 girls, with a mean age of 6 years (range 4 months to 17 years), who had a positive intra- dermal tuberculin skin test was made. These patients had been referred to our Department of Paediatrics for work- up studies and eventual treatment between 1994 and 2000. None of the patients had been exposed to BCG vaccina- tion. All patients underwent a thoroughhistory (including exposure tracing), physical examination, frontal and lat- eral chest radiographs, and sonographic study of the mediastinum. The radiographic ndings considered rep- resentative of TB included nonspecic localized inl- trates, hilar adenitis, localized hyperaeration, atelectasis, segmental lesions, cavitation, calcication, and localized pleural eusion. CTof the chest was performed in selected patients at the discretion of the physicians in charge. Ultrasonography of the mediastinum was performed with high-resolution equipment (Logiq 700, General Electric) using a 5-MHz convex probe. The presence of one or more masses with an ovoid or round shape and hypoechoic appearance in the anterior or middle medi- astinum was recorded. The anterior mediastinum in- cluded the prevascular region, occupied by the thymus gland and the middle mediastinum, the right paratrac- heal, supra-aortic, aortopulmonary, and subcarinal re- gions. On US the normal thymus has a bilobulated appearance and homogeneous echotexture with some echogenic strands. It is hypoechoic relative to the thy- roid gland and has a smooth, well-dened margin due to its brous capsule. It is a soft organ that does not compress neighbouring vascular structures, a charac- teristic that can help the radiologist to dierentiate it from mediastinal masses. The normal thymus can vary considerably in position, extension, size and congura- tion. In small children, the organ can extend from the cervical region to the diaphragm. During respiration and particularly when the child is crying, the thymus can be above the manubrium and simulate a cervical mass. The mediastinum was accessed via the suprasternal and left parasternal approaches [7]. When using the suprasternal approach, the patient was placed in a supine decubitus position with a cushion under the back and the neck slightly extended. The transducer was placed above the manubrium and titled caudally. To obtain an oblique sagittal view, the probe was placed laterally to encounter the space between the trachea and the sternocleidomastoid muscle. For the left parasternal approach, the patient was placed in a left lateral decubitus position to move the mediastinum downwards and increase the size of the anatomic acoustic window. Five standard sonographic slices were used to visualize the complete anterior and mid- dle regions of the mediastinum. Three sonographic slices were obtained with the suprasternal approach (oblique coronal, coronal, and oblique parasagittal) and two with the left parasternal approach (axial and parasagittal views). The oblique coronal view through the suprasternal approach was used to visualize the paratracheal region and to study the aortopulmonary region; the coronal view was useful for visualizing the vessels, particularly the SVC; the oblique parasagittal view visualized the aortopulmonary region. The axial and parasagittal views through the left parasternal approach were used to study the subcarinal and pre- vascular regions. In all the cases, the number and size (long axis) of lymph nodes were determined. The following groups were established arbitrarily: no adenopathy or lymph nodes <10 mm in diameter (negative, group 0); a single lymph node >10 mm (positive +, group 1); a single lymph node >15 mm (positive ++, group 2); a single lymph node >20 mm (positive +++, group 3); more than one lymph node >15 mm (positive ++++, group 4). In the case of clearly matted nodes, the size of the whole mass was considered. When possible, the size of each of its components was measured. For each patient, the results of chest radiography, US of the mediastinum, and chest CT were compared. Results Of the 32 patients who had US studies of the mediasti- num, 90% had recent contact with a person with con- rmed pulmonary TB. Only 11 (34.4%) children had clinical manifestations such as fatigue, low-grade fever, mild cough, weight loss, night sweats, chills, and failure to thrive. The remaining 21 children were asymptomatic, but with a positive tuberculin skin test. Pulmonary radiographic ndings were suggestive of TB in 21 chil- dren, negative in nine, and uncertain in two. With regard to US of the mediastinum, there were ve children in group 0, 15 in group 1, two in group 2, four in group 3, and six in group 4. CT of the chest was performed in six children. Details of ndings of chest radiography, mediastinal US and chest CT are shown in Table 1 and in Figs. 1, 2. In the group of nine children with normal ndings on chest radiography, US of the mediastinum conrmed lymphadenopathy in six cases (66.7%) and was negative in the remaining three. One of these three patients had a 896 normal chest CT scan and in the other two, CT exami- nation was not performed. All patients but two with compatible radiological ndings of TB had visible mediastinal lymph nodes on US. Therefore, 90.5% (19 out of 21) of patients with pathologic images in the chest radiographs, had visible mediastinal lymphadenopathy in the ultrasonographic study. In the two patients with doubtful radiological images, ultrasonography con- rmed the diagnosis of tuberculous lymphadenopathy in two. Table 1 Reults of chest roentgenograms, mediastinal ultrasonography, and chest CT scans in 32 children with positive intradermal tuberculin skin test Case Sex and age Chest X-ray Mediastinal lymph nodes by ultrasonography Mantoux (mm) Chest CT scan 1 Female, 7 years Normal Present (+) 20 ND 2 Male, 2 years Compatible TB Present (++++) 16 ND 3 Male, 2 years Compatible TB Present (+) 20 ND 4 Male, 7 months Normal Present (++) 10 ND 5 Female, 14 years Compatible TB Present (+) 10 Conrmatory 6 Female, 16 months Compatible TB Present (+) 10 ND 7 Female, 11 years Compatible TB Present (++++) 16 Conrmatory 8 Female, 3 years Compatible TB Present (+) 10 ND 9 Male, 16 years Compatible TB Present (++) 10 ND 10 Male, 18 months Compatible TB Present (++++) 10 ND 11 Male, 13 years Doubtful Present (+++) 10 Normal 12 Male, 8 years Normal Present (++++) 10 ND 13 Female, 2 years Compatible TB Present (+) 10 ND 14 Male, 22 months Compatible TB Present (+++) 28 ND 15 Female, 4 years Compatible TB Present (++++) 14 ND 16 Female, 12 years Compatible TB Present (+++) 10 Conrmatory 17 Female, 11 years Doubtful Present (+) 10 ND 18 Male, 4 months Compatible TB Present (++++) 10 ND 19 Male, 2 years Compatible TB Present (+) 10 ND 20 Female, 17 years Compatible TB Present (+) 22 ND 21 Female, 14 months Normal Present (+++) 16 ND 22 Male, 14 months Compatible TB Present (+) 14 ND 23 Female, 14 months Compatible TB Present (+) 10 ND 24 Male, 7 months Compatible TB Absent 12 ND 25 Male, 3 years Compatible TB Present (+) 9 ND 26 Male, 14 years Normal Present (+) 20 Conrmatory 27 Male, 2 years Normal Present (+) 10 ND 28 Female, 15 years Compatible TB Present (+) 10 ND 29 Female, 13 months Normal Absent 10 ND 30 Female, 15 months Normal Absent 10 ND 31 Male, 12 years Normal Absent 10 Normal 32 Male, 5 years Compatible TB Absent 14 ND ND not done Fig. 1 Results of chest radiog- raphy 897 The chest CT examination, which was carried out in six patients, conrmed the results of US in four. In one patient with normal radiographic ndings and absence of mediastinal adenopathy, the CT scan was also nega- tive, whereas in the other patient with uncertain radio- graphic ndings and mediastinal lymphadenopathy in the ultrasound examination, the CT scan was negative. This patient, however, was given antituberculous treat- ment and his clinical symptoms resolved and radiologi- cal images cleared. In ve of six (83.3%) patients a concordance between results of mediastinal ultrasonog- raphy and CT examination was observed. The case of a patient with lymphadenopathy in the right paratracheal region using the suprasternal ap- proach is shown in Fig. 3. In this case, results of US were conrmed by CT (Fig. 3). In the case of a 14-year- old patients with active TB involving the left upper lobe, the suprasternal approach revealed a lymph node, 1.8 cm in diameter, in the aortopulmonary region (Fig. 4). A lymphadenopathy in the subcarinal space was detected in a patient with normal chest roentgeno- gram using the left parasternal approach (Fig. 5). Discussion Most TB infections in children and adolescents are asymptomatic when the tuberculin skin test is positive. In the present series, only 34.4% of patients had non- specic symptoms, such as fever, cough, weight loss, and failure-to-thrive pattern in young infants. All patients were referred for evaluation because of the tuberculin skin test and in 90% of them, a recent exposure to an adult with active disease was present. It should be noted that there were two patients aged between 15 and 17 years of age. Despite the fact that these patients were adolescents, they were referred for evaluation to our department because 18 years is the upper age limit as- signed to pediatrics by our health care system. On the other hand, the fact that 32 patients with a tentative diagnosis of TB had been referred for work-up studies during the study period indicates that although signi- cant progress has been made in the control of TB in developed countries, this communicable disease has not yet been eradicated. Furthermore, children with primary tuberculous infection are the reservoir from which future cases will emerge. One of the major practical problems in diagnosing TB in children is that isolation of Mycobacterium TB from gastric aspirates or sputum is dicult [8]. Sputum for acid-fast stain and culture is rarely available from infants and children. Optimal collection of gastric aspi- rates requires hospitalization to sample the swallowed secretions that accumulate overnight. However, the Fig. 2 Results of mediastinal US Fig. 3 Right paratracheal lymphadenopathy. a Suprasternal, oblique coronal US section. The echogenic line originated in the right upper lobe is displaced by the mass. b Axial CT section conrming the US ndings. IA innominate artery, LBV left brachiocephalic vein, AO aorta, TR trachea, RUL right upper lobe, LN lymph node 898 sensitivity of acid-fast stain for gastric contents is usu- ally below 10%. The low yield of positive cultures from gastric aspirates is a result of the small number of organisms in primary TB in childhood and possible inadequate techniques for collection of gastric washings. Therefore, the diagnosis is frequently based solely on detecting typical radiographic abnormalities in a child with a reactive tuberculin skin test and with history of contact of an infectious case. The Mantoux method is helpful in supporting the diagnosis. Although a reaction of 10 mm induration is the usual cut-point for dening a signicant reaction, a reaction of 5 mm is considered signicant for symptomatic children and for recent contacts with infectious cases [9]. However, a negative Fig. 4a, b 14-year-old patient with active TB. Suprasternal oblique parasagittal (a) and suprasternal oblique coronal (b) US sections showing a lymph node 1.8 cm in diameter in the aortopulmonary region involving the left upper lobe. IA innominate artery, LBV left brachiocephalic vein, RUL right upper lobe, TR trachea, AO aorta, LN lymph node, LPA left pulmonary artery, LB left bronchus, LC left carotid artery; LS left subclavian artery, LB left bronchus, RPA right pulmonary artery, LA left atrium Fig. 5 Positive US with negative radiograph. a Normal frontal chest radiograph. b Left parasternal axial US section in the same patient shows lymphadenopathy in the subcarinal space. TH thymus gland, AO aorta, RPA right pulmonary artery, LC left carotid artery, LS left subclavian artery, LA left atrium, LB left bronchus, LBV left brachiocephalic vein, LPA left pulmonary artery, LN lymph node 899 reaction in a child who has signs and symptoms com- patible with TB does not rule out the diagnosis. In the present series, indurations ranged between 9 and 28 mm. Lymphadenopathy, with or without parenchymal abnormality, is the radiological hallmark of primary TB in children [10]. Children less than 3 years of age show a higher prevalence of lymphadenopathy and a lower prevalence of parenchymal abnormalities compared with children 415 years [5]. In early childhood, lymphade- nopathy as the sole radiological manifestation of disease was seen in 49% of cases versus 9% in late childhood and adolescence according to data reported by Leung et al. [11]. Bronchi in infants are of smaller calibre and more easily compressed by enlarging hilar lymph nodes. As the hilar lymph nodes enlarge, bronchial obstruction may occur and signs of air trapping may develop. Al- though hilar lymphadenopathy may be the only sug- gestive nding of TB in the chest radiographs, in the present study, 66.7% of patients with chest radiographs considered unrevealing showed mediastinal lymphade- nopathy in the ultrasound examination. Lymph nodes can sometimes be dicult to visualize on frontal plain radiographs. Occasionally, lymphadenopathy is visible only on the lateral lm [12]. Apical-lordotic views may aid in visualizing lesions obscured by the heart. When no lymphadenopathy is present on the standard radio- graphic examination of the chest, special imaging tech- niques such as CT may be of particular value [13]. It has been shown that CT scan may reveal mediastinal aden- opathies which are not evident on the chest radiograph [6]. Ultrafast CT scanning, however, is costly, not available in many institutions, includes radiation, and may require the use of sedation in young children. In contrast, US is much less expensive, the use of sedatives or contrast medium is not necessary, and can be easily obtained both in the hospital and in primary care set- tings. Although subcarinal adenopathy has recently been reported to be the most common site of lymphadenop- athy in children with TB [14], we have detected small adenopathies more frequently in the paratracheal region and aortopulmonary window because of a better echo- graphic access. In the subcarinal region, we have docu- mented large lymph nodes due to limitations in the echographic access and artifacts (e.g., the oesophagus). As far as we are aware, no previous study regarding the usefulness of mediastinal ultrasonography for the diagnosis of lymphadenopathy in TB in children has been published. For this reason, the present results cannot be compared to those reported by others. Conclusions In the present series of 32 patients with positive tuber- culin skin test, 90.5% of those with chest radiographic images compatible with TB had coincident ndings in the mediastinal ultrasonographic study. On the other hand, 66.7% of those with normal chest radiography had evidence of mediastinal lymphadenopathy on US. In all cases but one, US and CT ndings agreed. In view of the usefulness of US of the mediastinum for the diagnosis of lymphadenopathy in children with TB, this non-invasive method could also be of value in the con- trol and follow-up of children receiving antituberculous chemotherapy. Acknowledgement We thank Marta Pulido, MD, for editing the manuscript and for editorial assistance. References 1. Vallejo JG, Ong LT, Starke JR (1994) Clinical features, diagnosis, and treat- ment of TB in infants. Pediatrics 94:17 2. American Thoracic Society (1990) Diagnostic standards and classication of TB. Am Rev Respir Dis 142:725735 3. Hilman BC (1993) Pulmonary TB and tuberculous infection in infants, chil- dren, and adolescents. In: Hilman BC (ed) Pediatric respiratory disease: diag- nosis and treatment. Saunders, Phila- delphia, pp 311319 4. Snider DE, Rieder HL, Combs D et al (1988) TB in children. Pediatr Infect Dis 7:271278 5. Burroughs M, Beitel A, Kawamura A et al (1999) Clinical presentation of TB in culture-positive children. Pediatr In- fect Dis 18:440446 6. Delacourt C, Mani TM, Bonnerot V et al (1993) Computed tomography with normal chest radiograph in tuberculous infection. Arch Dis Child 69:430432 7. Lucaya J, Strife J (2001) Pediatric chest imaging: chest imaging in infants and children. Springer, Berlin Heidelberg New York, pp 125 8. Starke JR (1988) Modern approach to the diagnosis and treatment of TB in children. Pediatr Clin N Am 35:441464 9. American Thoracic Society and the Centers for Disease Control and Pre- vention (2000) Diagnostic standards and classication of TB in adults and children. Am J Respir Crit Care Med 161:13761395 10. Omlor GJ (2001) Pulmonary lymph- adenopathy. Pediatr Infect Dis 20:437 438 11. Leung AN, Mu ller NL, Pineda PR et al (1992) Primary TB in childhood: radiographic manifestations. Radiology 182:8791 12. Smuts NA, Beyers N, Gie RP et al (1994) Value of the lateral chest radio- graph in TB in children. Pediatr Radiol 24:478480 13. Vallejo JG, Starke JR (1996) Intratho- racic TB in children. Semin Respir Dis 11:184195 14. Andronikou S, Joseph E, Lucas S et al (2004) CT scanning for the detection of tuberculous mediastinal and hilar lymphadenopathy in children. Pediatr Radiol 34:232236 900
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