Cardiopulmonar y Imaging • Original Research Ko et al. Clinicoradiologic Characteristics of Tuberculosis With Lymphatic Involvement

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Cardiopulmonary Imaging Original Research

Clinicoradiologic Evidence of Pulmonary Lymphatic Spread in Adult Patients With Tuberculosis Jeong Min Ko1 Hyun Jin Park1 Chi Hong Kim 2 Ko JM, Park HJ, Kim CH

Keywords: CT, lymphatics, micronodules, pulmonary tuberculosis DOI:10.2214/AJR.14.12908 Received March 25, 2014; accepted after revision June 19, 2014. 1 Department of Radiology, St. Vincent’s Hospital, College of Medicine, The Catholic University of Korea, 93 Ji-dong, Paldal-gu, Suwon, Kyeonggi-do 442-723, Republic of Korea. Address correspondence to H. J. Park ([email protected]). 2

Department of Internal Medicine, St. Vincent’s Hospital, College of Medicine, The Catholic University of Korea, Kyeonggi-do, Republic of Korea. AJR 2015; 204:38–43 0361–803X/15/2041–38 © American Roentgen Ray Society

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OBJECTIVE. The purpose of this study is to evaluate the prevalence and clinicoradiologic characteristics of pulmonary tuberculosis with lymphatic involvement. MATERIALS AND METHODS. A total of 126 adults with active tuberculosis who underwent CT were enrolled. A retrospective investigation of CT images focused on the presence of perilymphatic micronodules, as well as other CT features of active tuberculosis. We selected two groups of patients with micronodules according to distribution (perilymphatic vs centrilobular). We compared clinical and CT findings between the two groups. RESULTS. Fifteen patients were excluded because of coexisting pulmonary disease. Among 111 patients, the prevalence of perilymphatic micronodules, galaxy or cluster signs, and interlobular septal thickening was 64 (58%), 18 (16%), and 30 (27%), respectively. Of 106 patients with micronodules, 37 and 40 were classified into the perilymphatic and centrilobular groups, respectively. Compared with the centrilobular group, the perilymphatic group had statistically significantly lower frequencies of positive acid-fast bacilli smears (32% vs 70%), consolidation (70% vs 98%), and cavitation (30% vs 60%). However, frequencies of interlobular septal thickening (41% vs 18%), galaxy or cluster signs (30% vs 0%), and pleural effusion (43% vs 20%) were statistically significantly higher in the perilymphatic group. CONCLUSION. CT findings representing pulmonary perilymphatic involvement are relatively common in adults with tuberculosis. These findings may represent lymphatic spread of tuberculosis and provide an explanation for the unusual CT features of pulmonary tuberculosis mimicking sarcoidosis and the low detection of Mycobacterium tuberculosis in patients with micronodules.

L

ymphatic spread of tuberculosis plays an important role, particularly in the early stages of initial or primary infection [1]. The incidence of lymphatic dissemination in ­ postprimary pulmonary tuberculosis is likely low because of enhanced acquired immunity [1]. No matter how low the incidence is, it is hard to understand why there are no reports, to our knowledge, about CT findings of active tuberculosis with pulmonary lymphatic spread in adults. Moreover, considering the increasing incidence of primary tuberculosis in adults [2–5] and the common involvement of postprimary tuberculosis in immunocompromised patients [6], pulmonary lymphatic spread of tuberculosis should be better understood. Recent studies have reported atypical CT manifestations of tuberculosis [7–9] that mimic manifestations of pulmonary sarcoidosis, with a characteristic pathologic appear-

ance of granulomas primarily involving the pulmonary lymphatics [10]. On the basis of our experience, lesions with perilymphatic distribution that are commonly seen in sarcoidosis are not rare in pulmonary tuberculosis. This led us to assume that tuberculosis is more commonly spread through the pulmonary lymphatics than expected in adults. Accordingly, we evaluated the prevalence and clinicoradiologic characteristics of adult pulmonary tuberculosis suggestive of a perilymphatic distribution. Materials and Methods This study was approved by our institutional review board, which waived informed consent. A total of 126 consecutive patients older than 15 years with active pulmonary tuberculosis and CT scans obtained at the time of diagnosis were enrolled in this retrospective study at our institution from January 2011 to February 2013. We analyzed clinical data and pulmonary parenchymal changes

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Clinicoradiologic Characteristics of Tuberculosis With Lymphatic Involvement on the CT scans. The diagnosis of active pulmonary tuberculosis, with or without tuberculous pleurisy, was based on positive results for acid-fast bacilli (AFB) staining or growth of Mycobacterium tuberculosis from sputum, bronchial washes, or pleural fluid; positive results for polymerase chain reaction (PCR) test for M. tuberculosis; a lymphocyte-predominant (> 50%) effusion meeting Light’s criteria [11] for exudative effusion, with the finding of an elevated adenosine deaminase level of greater than 40 IU/L; or radiologic and clinical improvement after administration of antituberculous drugs. Conventional CT scans with or without IV administration of contrast medium (100 mL at 2–2.5 mL/s) and high-resolution CT (HRCT) scans were obtained with two CT scanners (LightSpeed VCT, GE Healthcare; and Somatom Definition Flash, Siemens Healthcare). The decision to perform contrast enhancement was made by the attending clinicians on the basis of their suspicion for malignancy or tuberculosis lymphadenitis after evaluating chest radiographs of the patients. Scanning parameters included a 130-mA tube current, 120-kV tube voltage, 128 × 0.6-mm collimation, and 1.2 pitch. In conventional CT scan, all images were reconstructed into axial images with 5-mm slice thickness at 5-mm intervals and coronal images with 3-mm slice thickness. For HRCT scans, axial and coronal images with 1-mm slice thickness at 5-mm intervals and a bone algorithm were obtained. CT scans obtained before administration of antituberculous medication were analyzed for the presence and distribution of micronodules and the presence of clustered micronodules with the “sarcoid galaxy sign” (central large nodule surrounded by satellite micronodules) [12], or “sarcoid cluster sign” (cluster of multiple micronodules without central coalescence) [13], reversed halo sign (nodular walls or nodules inside the halo) [14], interlobular septal thickening, consolidation, and cavitation. The presence of pleural effusion and intrathoracic lymphadenopathy (short-axis diameter > 1 cm or central necrosis) were also checked. The distribution of micronodules was classified as centrilobular (micronodules limited to centrilobular regions), perilymphatic (micronodules along the bronchovascular and centrilobular interstitium, interlobular septa, and subpleural region), or random (uniform distribution of micronodules throughout the lung) [15, 16]. We selected two groups of patients according to the distribution of their micronodules: the perilymphatic group included patients with perilymphatic micronodules without centrilobular micronodules, and the centrilobular group included patients without perilymphatic micronodules but with centrilobular micronodules. Then we compared the clinical and CT findings between these two groups.

TABLE 1: Prevalence of CT Findings Among 111 Adults With Active ­Pulmonary Tuberculosis No. (%) of Patients

κ

Micronodules

106 (95)

0.840

Perilymphatic distribution

64 (58)

0.672

Centrilobular distribution

67 (60)

0.799

CT Finding

Random distribution

2 (2)

1.000

Galaxy or cluster sign

18 (16)

0.872

4 (4)

1.000

Interlobular septal thickening

Reversed halo sign

30 (27)

0.837

Consolidation or macronodule

96 (86)

0.922

Bronchial or bronchovascular bundle thickening

76 (68)

0.765

Cavitation

58 (52)

0.810

Pleural effusion

32 (29)

0.934

Intrathoracic lymphadenopathy

24 (22)

0.577

All CT scans and medical records were retrospectively reviewed by two chest radiologists (with 4 and 11 years of experience, respectively). Two radiologists independently and blindly checked the presence or absence of these CT findings. Interpretation of differences in observed findings were determined by consensus. The agreement between the two radiologists for the presence or absence of each CT finding was examined using kappa statistics. A kappa value of 0–0.20 indicated slight agreement, 0.21–0.40 indicated fair agreement, 0.41–0.60 indicated moderate agreement, 0.61–0.80 indicated substantial agreement, and 0.81–1.00 indicated almost perfect agreement. Comparisons between groups were performed using the independent t test for continuous variables and the chi-square or Fisher exact test for categoric variables. In all tests, p < 0.05 was considered statistically significant.

Results Among 126 patients, 15 with coexisting pulmonary disease (pneumonia [n = 10], pulmonary edema [n = 3], emphysema [n = 1], and diffuse interstitial pneumonitis [n = 1]) were excluded. Therefore, we evaluated clinicoradiologic findings from 111 patients with pulmonary tuberculosis (74 men and 37 women; mean age, 42 years; age range, 17– 87 years). Fifteen patients had chronic illnesses, including diabetes (n = 9), chronic obstructive lung disease (n = 5), malignancy (n = 1), renal failure (n = 2), and collagen vascular disease (n = 2); some patients had more than one chronic illness. There was no one with HIV infection. One hundred six patients underwent conventional CT scans with or without contrast agent infusion, and five patients underwent HRCT. Diagnoses of ac-

tive pulmonary tuberculosis were confirmed in 93 patients by positive microbiology results (AFB, n = 56; culture, n = 77; PCR, n = 69; some patients’ samples underwent more than one test). Increased adenosine deaminase levels in lymphocyte-dominant pleural fluid were seen in eight patients, and clinical or radiologic improvements of pulmonary lesions after antituberculous medications were found in 10 patients. The CT findings from patients with active pulmonary tuberculosis are summarized in Table 1. The interobserver agreement between the two radiologists for identifying micronodules, pleural effusion, galaxy or cluster signs, reversed halo sign, interlobular septal thickening, consolidation, cavitation, and miliary micronodules was almost perfect. There was substantial agreement in identifying perilymphatic and centrilobular distributed micronodules and bronchial or peribronchovascular bundle thickening. There was moderate agreement for identifying intrathoracic lymphadenopathy. Among 111 patients, 106 (95%) had micronodules. Perilymphatic micronodules were detected in 64 of 111 patients with active tuberculosis (58%). Among the 64 patients with perilymphatic micronodules, the nodules were present along the bronchovascular bundle in 63 patients (98%). Micronodules along the interlobular septum and subpleural region were detected in 49 (78%) and 33 (52%) patients, respectively. Centrilobular micronodules were noted in 67 cases (60%). Miliary nodules with a random distribution were seen in two patients (2%). Galaxy or cluster signs, reversed halo sign,

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Ko et al. TABLE 2: Comparison of Clinical and CT Findings in the Perilymphatic and Centrilobular Groups Characteristic

Perilymphatic Group (n = 37)

Centrilobular Group (n = 40)

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Sex, no. of patients

pa 0.229

Male

27

24

Female

10

16

41 (17–81)

41 (18–87)

0.916b

0.4 ± 0.7 (0–2)

1.5 ± 1.4 (0–4)

< 0.001b

32 (11/34)

70 (26/37)

0.001

PCR positive for M. tuberculosis

40 (14/35)

79 (30/38)

0.001

Culture positive for M. tuberculosis

69 (24/35)

79 (30/38)

0.313

Extrathoracic tuberculous involvement

14 (5/37)

3 (1/40)

0.100

Interlobular septal thickening

41 (15/37)

18 (7/40)

0.025

Galaxy or cluster sign

30 (11/37)

0 (0/40)

< 0.001

Age (y), mean (range) No. of AFB present on sputum smear, mean ± SD (range) AFB test positivity

CT finding

Reversed halo sign

8 (3/37)

0 (0/40)

0.106

Consolidation or macronodule

70 (26/37)

98 (39/40)

0.001

Cavitation

30 (11/37)

60 (24/40)

0.008

Bronchial or bronchovascular bundle thickening

70 (26/37)

60 (24/40)

0.345

Pleural effusion

43 (16/37)

20 (8/40)

0.048

Intrathoracic lymphadenopathy

22 (8/37)

25 (10/40)

0.726

Note—Unless otherwise specified, data are percentages with numbers used to calculate the percentages in parentheses. The perilymphatic group includes patients with perilymphatic micronodules without centrilobular micronodules, whereas the centrilobular group includes patients with centrilobular micronodules without perilymphatic micronodules. AFB = acid-fast bacilli, PCR = polymerase chain reaction, M. tuberculosis = Mycobacterium tuberculosis. aUnless otherwise noted, the chi-square or Fisher exact test was used. bIndependent t test was used.

and interlobular septal thickening were observed in 18 (16%), four (4%), and 30 (27%) patients, respectively. Consolidation, cavitation, and bronchial or bronchovascular bundle thickening were detected in 96 (86%), 58 (52%), and 76 (68%) patients, respectively. Tuberculous pleurisy was seen in 32 patients (29%). Twenty-four patients (22%) had intrathoracic lymphadenopathy.

A 40

Of 106 patients with micronodules, 37 and 40 were classified into the perilymphatic and centrilobular groups, respectively (Table 2); 27 patients had both centrilobular and perilymphatic distribution of their micronodules (Figs. 1 and 2), and the remaining two patients had randomly distributed micronodules. Compared with the centrilobular group, the numbers of AFB present on spu-

B

tum smears (0.4 ± 0.7 vs 1.5 ± 1.4; p < 0.001) and the frequency of positive results for AFB (32% vs 70%, p = 0.001) and PCR (40% vs 79%; p = 0.001) were statistically significantly lower in the perilymphatic group. Interlobular septal thickening (41% vs 18%; p = 0.025), galaxy or cluster signs (30% vs 0%; p < 0.001), and pleural effusion (43% vs 20%; p = 0.048) were statistically significantly more

Fig. 1—39-year-old man with active pulmonary tuberculosis. A and B, CT shows tree-in-bud opacities, suggesting bronchogenic spread of tuberculosis in lateral and posterior basal segments of left lower lobe. In contrast, perilymphatic micronodules with peribronchiolar thickening and nodularities are seen in anteromedial basal segment of left lower lobe. Note round, oval, or branching tubular radiolucencies representing open bronchioles.

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Clinicoradiologic Characteristics of Tuberculosis With Lymphatic Involvement Fig. 2—18-year-old man with active pulmonary tuberculosis. A and B, Note focal area of clustered micronodules (arrowheads, A), which cannot be explained by centrilobular or miliary distribution on CT. Tubular or branching radiolucencies representing bronchioles kept open and subpleural nodularities are identified within focal area. This finding may represent perilymphatic involvement such as “sarcoid cluster sign” in cases of sarcoidosis. Typical appearance of tree-in-bud (arrow, A) is also seen.

A

B

frequent in the perilymphatic group, whereas the frequency of consolidation (70% vs 98%; p = 0.001) and cavitation (30% vs 60%; p = 0.008) were statistically significantly higher in the centrilobular group. Bronchial or bronchovascular bundle thickening (70% vs 60%; p = 0.345), reversed halo sign (8% vs 0%; p = 0.106), intrathoracic lymphadenopathy (22% vs 25%; p = 0.726), positive culture result (69% vs 79%; p = 0.313), and extrathoracic involvement (14% vs 3%; p = 0.100) did not differ between the two groups (Figs. 3 and 4).

CT findings characteristic of pulmonary tuberculosis described by many investigators [17–20] are lung consolidation and cavitation indicating local progression. Another reported CT finding that is considered to be a common manifestation of active pulmonary tuberculosis is centrilobular nodules with branching linear opacities representing bronchogenic dissemination [17, 19]. CT findings of miliary micronodules resulting from hematogenous dissemination of pulmonary tuberculosis consist of innumerable micronodules distributed in a diffuse random pattern throughout both lungs [1, 21–23]. A CT finding supporting the lymphatic spread of tuberculosis is lymphadenopathy. Tuberculosis is thought to reach the nodes and subpleural regions via the pulmonary lymphatics, but, to our knowledge, no reports of CT findings are available involving pulmonary lymphatics in active pulmonary tuberculosis. Among the four pathways, the frequency of

Discussion Progression or extension of tuberculous lesions can occur in a variety of ways, including local progression, lymphangitic dissemination, bronchogenic dissemination, and hematogenous dissemination [1, 17]. Local progression is a fundamental and wellknown route of disease progression in pulmonary tuberculosis. Therefore, common

A

B

local progression and miliary micronodules with hematogenous dissemination from previous studies did not differ from our results. However, we had results different from those of previous studies regarding bronchogenic and lymphatic dissemination. Micronodules on CT in active pulmonary tuberculosis, except for miliary nodules, have been considered as centrilobular opacities reflecting bronchogenic dissemination [24, 25]. However, micronodules interpreted as perilymphatic in our study cannot represent endobronchial inflammation or spread of infection according to generally accepted definitions of micronodular distribution [15, 16]. By definition, micronodules along the peribronchovascular bundles, interlobular septa, and subpleural regions indicate perilymphatic disease. We suspected that these micronodules represented granulomas in the pulmonary interstitium, which is not unusual histopathologically [26, 27]. Early lesions

Fig. 3—57-year-old man with intestinal tuberculosis. A and B, High-resolution CT shows nodular thickening of bronchovascular bundle and clustered micronodules with galaxy sign in both lungs. Note nodular thickening of interlobular septum (arrows, A) and right major fissure (arrowheads, A). These findings are indistinguishable from typical CT features of sarcoidosis. Active pulmonary tuberculosis was confirmed by positive result of polymerase chain reaction from bronchial wash fluid.

AJR:204, January 2015 41

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Ko et al. that developed in the perivascular and peribronchiolar connective tissue corresponding to pulmonary lymphatics have also been identified in an animal study with guinea pigs experimentally infected aerogenically with M. tuberculosis [28]. We thought that perilymphatic micronodules in adult pulmonary tuberculosis are not a novel radiologic manifestation, but have been neglected or misinterpreted as centrilobular nodules with branching linear opacities. Actually, we could find perilymphatic micronodules on some figures in the previous studies about active tuberculosis [29, 30]. In our study, the galaxy or cluster signs and reversed halo sign were found in 16% and 4% of patients, respectively. Heo et al. [7] described pulmonary tuberculosis as showing a “sarcoid galaxy sign” indistinguishable from that seen in sarcoidosis. In their report, eight of 86 patients with active pulmonary tuberculosis had single or multiple large nodules composed of coalescent small nodules. They thought that both tuberculosis and sarcoidosis are granulomatous diseases and that both show the same clusters of small nodules on thin-section CT; therefore, tuberculous and sarcoid clusters may indeed share a similar pathologic profile. Recently, the sarcoid cluster sign has been reported in cases of sarcoidosis as a new HRCT sign [13]. Those authors defined it as the presence of a cluster of micronodules without central coalescence in the lung. These tiny nodules were correlated with noncaseating necrotizing granulomas along the lymph vessel on histopathologic examination. A similar CT finding was also described in a patient with active pulmonary tuberculosis [9]. The reversed halo sign represents a focal round area of groundglass opacity surrounded by a crescent or ring-shaped opacity. It was first described as a finding specific for cryptogenic organizing pneumonia and has been reported subsequently in a wide spectrum of infectious and noninfectious diseases [8, 14]. However, Marchiori et al. [14] reported that the nodular pattern of the ring component of the reverse halo sign is highly suggestive of granulomatous diseases, including sarcoidosis and tuberculosis. Although these CT signs have not been considered a well-known characteristic of tuberculosis, they may be unusual appearances of perilymphatic micronodules such as those in sarcoidosis. Interlobular septal thickening is a common CT finding in active pulmonary tuberculosis [17, 19]. Im et al. [17] reported that

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A

B

C Fig. 4—56-year-old man with sputum test that was smear negative for pulmonary tuberculosis. A–C, CT shows multifocal areas of perilymphatic distributed micronodules of both lungs. Note large foci of confluent micronodules mimicking ground-glass opacities in right lower lobe. Subpleural micronodules, bronchovascular nodular thickening, and multifocal clusters of micronodules with or without central coalescence are identified. Note also reverse halo sign in left lower lobe.

12 of 41 (29%) patients with active pulmonary tuberculosis showed interlobular septal thickening on CT scans. They thought that these findings suggest a local increase in lymphatic flow from exudative lesions or impaired lymphatic drainage due to associated central lymphadenopathy. However, until now there have been no reports of radiologicpathologic correlation of interlobular septal thickening in active tuberculosis. The exception is miliary tuberculosis, for which pathologic evidence of interstitial involvement has been reported that could account for interlobular septal thickening [22, 31]. Together with the different CT features associated with the distribution of micronodules, our results of comparing clinical and other radiologic findings between perilymphatic and centrilobular groups could support pulmonary lymphatic involvement of tuberculosis. The perilymphatic group was associated with statistically significantly lower numbers of AFB and frequency of positive AFB tests, lower positivity of PCR,

and a lower incidence of consolidation and cavitation than those of the centrilobular group (Table 2). These results differ from those of prior studies evaluating the relationship between CT findings and sputum AFB in active pulmonary tuberculosis. Previous studies concluded that the presence of micronodules (centrilobular opacities) is not associated with positivity or number of sputum AFB [24, 32]. By exclusion of perilymphatic micronodules, the presence of micronodules showed a positive relationship with sputum AFB smear and PCR in the centrilobular group of our study. In our opinion, the previous results might be due to misinterpretation of all micronodules as centrilobular distributed micronodules. Considering that centrilobular micronodules in pulmonary tuberculosis represent endobronchial spread, our result is more understandable. In our study, the difference in positivity of sputum culture was insignificant between two groups. It may have been caused by the higher sensitivity of culture studies, compared with spu-

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Clinicoradiologic Characteristics of Tuberculosis With Lymphatic Involvement tum AFB smear [33]. Furthermore, the high prevalence of the galaxy or cluster signs and interlobular septal thickening in the perilymphatic group may also support our hypothesis that micronodules with perilymphatic distribution represent lymphatic dissemination of tuberculosis. The limitations of our study must be acknowledged. First, our study has no pathologic correlation with CT findings that may represent pulmonary lymphatic involvement of tuberculosis. None of our patients underwent open lung biopsy. However, those CT findings have been recognized as representing perilymphatic disease for a long time and in many studies [34–36]. Second, we retrospectively analyzed CT images with 3to 5-mm slice thickness. At our institution, contrast-enhanced MDCT rather than HRCT is performed routinely when evaluating micronodules, because the main reason for the scan is to examine the presence of lymphadenitis or other associated findings, or to rule out diseases other than pulmonary tuberculosis, such as lung cancer. Nonetheless, the resolution of MDCT was improved, which facilitates the evaluation of subtle abnormalities such as micronodules and septal lines, and, if needed, multiplanar reconstruction with thin slice thickness is feasible by applying appropriate software (Syngo.via, Siemens Healthcare). Therefore, there was no problem in the interpretation of micronodules related to CT protocol. In conclusion, micronodules with perilymphatic distribution should be regarded as a common CT feature of pulmonary tuberculosis among adults. Considering these findings, tuberculosis commonly spreads through the pulmonary lymphatics in adults, as well as via direct erosion and the airways. Given this different mechanism of dissemination, unusual CT features of pulmonary tuberculosis mimicking sarcoidosis and low detection of M. tuberculosis in patients with micronodules can be explained. References 1. Pratt PC. Pathology of tuberculosis. Semin Roentgenol 1979; 14:196–203 2. Choyke PL, Sostman HD, Curtis AM, et al. Adult-onset pulmonary tuberculosis. Radiology 1983; 148:357–362 3. Miller WT, MacGregor RR. Tuberculosis: frequency of unusual radiographic findings. AJR 1978; 130:867–875 4. Palmer PE. Pulmonary tuberculosis: usual and unusual radiographic presentations. Semin Roent-

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Clinicoradiologic evidence of pulmonary lymphatic spread in adult patients with tuberculosis.

The purpose of this study is to evaluate the prevalence and clinicoradiologic characteristics of pulmonary tuberculosis with lymphatic involvement...
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