Small Airway Disease After Mycoplasma Pneumonia In

J Korean Radiol Soc 2003;48:361-367

Small Airway Disease after Mycoplasma Pneumonia in Children: HRCT Findings and Correlation with Radiographic Findings1 Jung-Eun Cheon, M.D.1, 3, Woo Sun Kim, M.D., In-One Kim, M.D., Young Yull Koh, M.D.2, Hoan Jong Lee, M.D.2, Kyung Mo Yeon, M.D.

Purpose: To assess the high-resolution CT (HRCT) findings of small airway abnormalities after mycoplasma pneumonia and correlate them with the findings of chest radiography performed during the acute and follow-up phases of the condition. Materials and Methods: We retrospectively evaluated HRCT and chest radiographic findings of 18 patients with clinical diagnosis of small airway disease after mycoplasma pneumonia (M:F=8:10, mean age: 8.3 years, mean time interval after the initial infection; 26 months). We evaluated the lung parenchymal and bronchial abnormalities on HRCT (n=18). In addition, presence of air-trapping was assessed on expiratory scans (n=13). The findings of HRCT were correlated with those of chest radiography performed during the acute phase of initial infection (n=15) and at the time of CT examination (n=18), respectively. Results: HRCT revealed lung parenchymal abnormalities in 13 patients (72%). A mosaic pattern of lung attenuation was noted in ten patients (10/18, 56%), and air-trapping on expiratory scans was observed in nine (9/13, 69%). In nine of 14 (64%) with negative findings at follow-up chest radiography, one or both of the above parenchymal abnormalities was observed at HRCT. In four patients (27%), parenchymal abnormalities were seen at HRCT in areas considered normal at acute-phase chest radiography. Bronchiectasis or ateclectasis was observed in eight (44%) and four (22%) patients, respectively, at HRCT. The CT features of Swyer-James syndrome such as a unilateral hyperlucent lung with reduced lung volume and attenuated vessels were noted in two patients (11%). Conclusion: HRCT can clearly demonstrate lung parenchymal and bronchial abnormalities of small airway disease after mycoplasma pneumonia in children.

Index words : Bronchiolitis obliterans Children, respiratory system Computed tomography (CT), high-resolution Lung, CT Mycoplasma pneumonia

1Department of Radiology, Seoul National University College of Medicine, Institute of Radiation Medicine, SNUMRC, Clinical Research Institute, Seoul National University Hospital 2Department of Pediatrics, Seoul National University College of Medicine 3Department of Radiology, Seoul Municipal Boramae Hospital Received January 21, 2003 ; Accepted March 11, 2003 Address reprint requests to : Woo Sun Kim, M.D., Department of Radiology, Seoul National University Children’s Hospital, 28 Yongon-dong, Chongno-gu, Seoul 110-744, Korea. Tel. 82-2-760-3608 Fax. 82-2-747-5781 E-mail: [email protected] ─ 361 ─ Jung Eun Cheon, et al : Small Airway Disease after Mycoplasma Pneumonia in Children

Pneumonia due to Mycoplasma pneumoniae is a com- ease, including obliterative bronchiolitis, is usually mon infection occurring primarily in children and based on radiological findings and abnormal pulmonary young adults (1, 2), and its radiologic findings have been function testing rather than on the results of histologic extensively described in the literature (3-7). The most examination, and in patients in whom obliterative bron- common of these is a focal or bilateral reticulonodular chiolitis is suspected, high-resolution computed tomog- pattern, and hazy or ground-glass consolidation is also raphy (HRCT) plays a major role (11, 12). The purpose frequent (3, 7). Most published reviews emphasize the of this study was to determine the HRCT findings of benign course of the condition (1-7), though long-last- children with clinically suspected obliterative bronchi- ing impairment of small airway function after clinical olitis after mycoplasma pneumonia, and to compare and radiographic recovery has been reported in children these with their chest radiographic findings. (8, 9). Obliterative bronchiolitis is a rare disease involving Materials and Methods the respiratory bronchioles and characterized by sub- mucosal and peribronchiolar fibrosis (11-14). It occurs Eighteen children [8 boys and 10 girls; age, 3-14 in various clinical settings. Because Mycoplasma pneu- (mean, 8.3) years] with a clinical diagnosis of obliterative moniae involves the bronchial epithelium, where in- bronchiolitis after mycoplasma pneumonia were re- flammatory host defense mechanisms are active, it is ferred for CT for the evaluation of lung parenchymal ab- likely that the organism is one of causes of obliterative normality. The main clinical features were as follows: 1) bronchiolitis (11-15). The diagnosis of small airway dis- initial clinical findings were consistent with acute lower

A B

Fig.1. A six-year-old boy with mycoplasma pneumonia. A. Chest radiography obtained during the acute phase of pneumonia shows air-space consolidation in the lateral portion of the right lower lung zone. Mild pleural changes and accentuation of the minor fissure is noted in the right side. B. Chest CT scan performed three years later. HRCT scan obtained at suspended full inspiration shows subtle inhomogeneous lung attenuation in the right lower lobe (arrows). C. Expiratory scan of the same level as the scan of (B) shows patchy air-trapping of mosaic pattern (arrows) in the right lower lobe.

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respiratory tract infection due to Mycoplsma pneumoniae, obstructive pattern (forced expiratory volume in 1sec and mycoplasma pneumonia had been diagnosed after [FEV1]/ forced vital capacity [FVC] less than 80%) was increased mycoplasma antibody titer (>1:640) or a four- observed, though no specific abnormality was seen in fold or higher rise of titer between the acute and conva- the other six. lescent period; 2) respiratory symptoms, signs, or both Chest radiographs obtained during the acute phase of [cough (n=12), wheezing (n=4), or crackles (n=4)] had pneumonia were available in 15 patients, regularly ob- persisted for months or years after the onset of illness; 3) served in our out-patient clinic for a mean period of 36 the patients were previously healthy, with no specific (3-54) months, and repeated chest radiographs were antecedent illness, including asthma. In two of eight pa- obtained during follow-up. For CT scanning, a HiSpeed tients who underwent a pulmonary function test, mild Advantage System (General Electric Medical Systems,

A B

C D Fig. 2. A seven-year-old boy with left-sided Swyer-James syndrome after mycoplasma pneumonia. A. Chest radiography obtained during the acute phase of pneumonia shows reticulonodular opacity mixed with patchy air-space consolidation in the left lower lung zone. B. Follow-up chest radiography obtained six months later shows sparse vascular marking in left upper lung zone and generally reduced lung attenuation in the left lung. The heart is shifted to the left due to decrease in the left lung volume. C. CT scan obtained at the level of lower lobes shows a small hyperlucent left lung with decreased pulmonary vascularity and a shift of the heart to the left. D. Expiratory scan obtained at the same level as the scan of (C) shows loss of normal decrease of lung volume and loss of normal increase of lung attenuation in the left lung suggesting air-trapping. Multiple small areas of air-trapping are also seen in the right lower lobe (arrows). ─ 363 ─ Jung Eun Cheon, et al : Small Airway Disease after Mycoplasma Pneumonia in Children

Milwaukee, Wis., U.S.A.) set at 200 mA and 120 KVp analyzed to determine the presence and extent of a mo- was used. In all patients, HRCT scans with 1.5 mm- saic pattern of lung attenuation on inspiratory scans or thick sections were obtained at 10 mm intervals and those obtained during quiet breathing, and of air-trap- processed using a bone algorithm, and in 13, suspended ping on expiratory scans. A mosaic pattern was defined full inspiratory and expiratory scanning was performed. as a patchwork of regions of hypoattenuation on CT In the remaining five, CT scans were obtained during scans. Areas of less attenuated pulmonary parenchyma, quiet breathing. Filming was performed with a constant especially where a less than normal increase in attenua- window setting (level -700, width 1500). The time inter- tion during expiration was observed, were considered to val between the initial episode of acute lower respirato- represent air-trapping (15, 16). Bronchiectasis or atelec- ry infection and CT examination ranged from 3 to 49 tasis was also assessed; the former was considered pre- (mean, 26) months. sent when at least one CT scan in any given individual Chest radiographs and CT scans were analyzed by two showed that the internal diameter of the bronchus was radiologists (J-EC, WSK). The location, extent and pat- greater than that of the adjacent pulmonary artery, and tern of parenchymal lesion revealed by chest radi- tapering of the bronchial lumen was absent (15, 16). CT ographs obtained during the acute phase of pneumonia, findings were correlated with the findings of chest radi- and changes in lung volume and lung density seen on ography performed during the acute phase of infection follow-up radiographs were reviewed. CT scans were (n=15) and at the time of CT examination (n=18).

A B

Fig. 3. A four-year-old boy with left-sided Swyer-James syndrome after mycoplasma pneumonia. A. Chest radiography obtained during the acute phase of pneumonia shows air-space consolidation in the left lower lung zone with moderate amount of pleural effusion. A patchy consolidation is also noted in the right upper lobe. B. Follow-up chest radiography obtained 14 months later shows a hyperlucent left lung and atelectasis of the left lower lobe. The right lung is emphysematous. C. CT scan obtained at the level of lower lobes shows small left lung volume, diminished lung attenuation, and attenuated pulmonary vessels. Note bronchiectasis with parenchymal destruc- tion in the left lower lobe (open arrows). Mosaic pattern of lung attenuation is also seen in the right lower lobe (arrows).

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Results Discussion

Initial chest radiography (n=15) revealed air-space Mycoplasma pneumonia is a community-acquired in- consolidation (Figs. 1A and 3A) in nine patients (60%), fection frequently encountered in clinical practice. reticular or reticulonodular opacities in four (27%), and Although clinically apparent pneumonia occurs in only a mixed pattern (Fig. 2A) in two (13%). Parenchymal ab- 3 to 10 percent of infected persons, it probably accounts normalities were unilateral in eleven patients and bilat- for up to 30 percent of all pneumonia in the general pop- eral in four. Zonal distribution was as follows: left lower ulation (1, 2). The clinical course of mycoplasma pneu- lung (n=10), right lower lung (n=5), left upper lung monia is typically benign and self-limiting. However, a (n=2), and right upper lung (n=2). Pleural effusion was follow-up study of 50 children undertaken by Mok et al. noted in three patients (Fig. 3A). demonstrated persistent abnormalities of small airway Chest radiographs obtained at the time of CT (n=18) function after mycoplasmal respiratory illness (8). were normal in 14 patients (78%). The remaining four Sabato et al. (9) also demonstrated persistent pulmonary had unilateral emphysema (n=2) (Fig. 2B), localized em- function abnormality, even in symptom-free children, at physema of the left lower lobe (n=1), or atelectasis of three-year follow-up. According to Kim et al. (10), a con- the left lower lobe (n=1) (Fig. 3B). siderable proportion of children have abnormal HRCT HRCT (n=18) demonstrated lung parenchymal abnor- findings after mycoplasma pneumonia, and younger age malities in 13 patients (72%), with a mosaic pattern of and higher antimycoplasmal antibody titer may be risk lung attenuation in ten (56%) (Figs. 1B and 3C). The le- factors for sequelae. sions were unilateral in six patients and bilateral in four; HRCT is currently regarded as a useful adjunct to con- in each of the ten, the mosaic pattern involved one to ventional diagnostic procedures including ventilation- four lobes (18 in total). At expratory CT (n=13), air-trap- perfusion scintigraphy and pulmonary function test in ping was observed in nine patients (69%), with unilater- the evaluation of small airway disease (11, 12, 18-20). al (n=6) or bilateral (n=3) distribution (Figs. 1C and 2D). The CT findings of obliterative bronchiolitis are a mosa- Air-trapping in the absence of inspiratory scan abnor- ic pattern of lung attenuation, air trapping and bronchial malities was noted in three patients (23%). Bronchiecta- dilatation, as well as centrilobular nodular or branching sis (n=8, 44%) and segmental or lobar atelectasis (n=4, structures related to thickening of the bronchiolar wall. 22%) were also present (Fig. 3C). Centrilobular nodules As the term “mosaic pattern of lung attenuation” is non- suggesting bronchiolar lesions were not found in any pa- specific and refers to a pattern that occurs in a variety of tients. The CT features of Swyer-James syndrome (re- lung diseases, paired inspiratory-expiratory CT scanning duced lung volume with hypoattenuation at the affected is useful for distinguishing small airway disease from side, diminished vascular marking, bronchial dilatation, other causes of a mosaic pattern of lung attenuation. In and air-trapping) were, however, seen in two patients small airway disease, the hyperlucent area of the lung (11%) (Figs. 2C, 2D and 3C). In four patients (22%), CT seen at inspiration will remain hyperlucent at expiration revealed no abnormality. because of air trapping, showing no or minimal decrease In ten of 15 patients (66%), the involved lobes seen at in volume (18-20). HRCT corresponded with the involved area depicted by Swyer-James syndrome is a variant of postinfectious chest radiographs obtained during the acute phase of bronchiolitis obliterans and at radiography is character- pneumonia (Fig. 1). In four of the 15 (27%), CT revealed ized by a unilateral small lung with hyperlucency and a mosaic pattern of lung attenuation or air-trapping in air trapping (15, 21, 22). The CT findings of Swyer- areas shown to be normal at acute-phase chest radiogra- James syndrome may include hyperlucent lung, re- phy (Figs. 2D and 3C). Nine of 14 patients (64%) with duced or normal lung volume, bronchiectasis, attenuat- negative findings at chest radiography performed at the ed vascular markings, and air trapping at expiratory CT time of CT examination showed a mosaic pattern of (21, 22). Swyer-James syndrome as a sequela of my- lung attenuation and/or air-trapping at HRCT. coplasma pneumonia has been reported in the literature (15). From this preliminary experience of using HRCT for the evaluation of lung parenchymal change occurring af- ─ 365 ─ Jung Eun Cheon, et al : Small Airway Disease after Mycoplasma Pneumonia in Children ter mycoplasma pneumonia, we have found that the Radium Ther Nucl Med 1975;124:417-422 7. Reittner P, Mu¨ller NL, Heyneman L, et al. Mycoplasma pneumo- modality is sensitive in detecting a mosaic pattern of niae pneumonia: radiographic and high-resolution CT features in lung attenuation and air trapping, and superior to radi- 28 patients. AJR Am J Roentgenol 2000;174:37-41 ography in showing its extent and distribution. HRCT is 8. Mok JY, Waugh PR, Simpson H. Mycoplasma pnuemoniae infection. A follow-up study of 50 children with respiratory illness. also excellent for the detection of bronchial abnormali- Arch Dis Child 1979;54:506-511 ties. We therefore believe that it can be a useful diagnos- 9. Sabato AR, Martin AJ, Marmion BP, Kok TW, Cooper DM. tic modality for the detection of late sequelae of my- Mycoplasma pneumoniae: acute illness, antibiotics, and subse- coplasma pneumonia, especially in patients without quent pulmonary function. Arch Dis Child 1984;59:1034-1037 10. Kim CK, Chung CY, Kim JS, Kim WS, Park Y, Koh YY. Late ab- chest radiographic abnormalities in spite of the presence normal findings on high-resoluation computed tomography after of respiratory symptoms. However, our study suffers mycoplasma pneumonia. Pediatrics 2000;105:372-378 certain limitations. First, because we did not collect data 11. Hartman TE, Primack SL, Lee KS, Swensen SJ, Muller NL. CT of from a consecutive group of patients with mycoplasma bronchial and bronchiolar diseases. RadioGraphics 1994;14:991- 1003 pneumonia, we could not estimate the incidence of late 12. Mu¨ller NL, Miller RR. Diseases of the bronchioles: CT and parenchymal complications arising after mycoplasma histopathologic findings. Radiology 1995;196:3-12 pneumonia. Second, the possibility of subclinical infec- 13. Isles AF, Masel J, O’Duffy J. Obliterative bronchiolitis due to tion other than mycoplasma pneumonia during the fol- Mycoplasma pneumoniae infection in a child. Pediatr Radiol 1987; 17:109-111 low-up period could not be completely ruled out. 14. Prabhu MB, Barber D, Cockcroft DW. Bronchiolitis obliterans and In conclusion, HRCT can clearly show lung parenchy- Mycoplasma pneumonia. Respir Med 1991;85:535-537 mal and bronchial abnormalities of small airway disease 15. Stokes D, Sigler A, Khouri NF, Talamo RC. Unilateral hyperlucent lung (Swyer-James syndrome) after severe Mycoplasma pneumo- after mycoplasma pneumonia in children. Further study niae infection. Am Rev Respir Dis 1978;117:145-152 of the correlation between parenchymal changes ob- 16. Austin JH, Mu¨ller NL, Friedman PJ, et al. Glossary of terms for served at HRCT and clinical symptoms or pulmonary CT of the lungs: recommendations of the Nomenclature Commit- function abnormlities is required. tee of the Fleischner Society. Radiology 1996;200:327-331 17. Stern EJ, Mu¨ller NL, Swensen SJ, Hartman TE. CT mosaic pattern of lung attenuation: etiologies and terminology. J Thorac Imaging References 1995;10:294-297 18. Stern EJ, Webb WR. Dynamic imaging of lung morphology with 1. Mansel JK, Rosenow EC 3rd, Smith TF, Martin JW Jr. ultrafast high-resolution computed tomography. J Thorac Imaging Mycoplasma pneumoniae pneumonia. Chest 1989;95:639-646 1993;8:273-282 2. Cassell GH, Cole BC. Mycoplasmas as agents of human disease. N 19. Johnson JL, Kramer SS, Mahhoubi S. Air trapping in children: Engl J Med 1981;304:80-89 evaluation with dynamic lung densitometry with spiral CT. 3. John SD, Ramanathan J, Swischuk LE. Spectrum of clinical and ra- Radiology 1998;206:95-101 diographic findings in pediatric mycoplasma pneumonia. 20. Arakawa H, Webb WR, McCowin M, Katsou G, Lee KN, Seitz RF. RadioGraphics 2001;21:121-131 Inhomogeneous lung attenuation in thin-section CT: diagnostic 4. Guckel C, Benz-Bohm G, Widemann B. Mycoplasmal pneumonias value of expiratory scans. Radiology 1998;206:89-94 in childhood. Roentgen features, differential diagnosis and review 21. Moore AD, Godwin JD, Dietrich PA, Verschakelen JA, Henderson of literature. Pediatr Radiol 1989;19:499-503 WR Jr. Swyer-James syndrome: CT findings in eight patients. AJR 5. Finnegan OC, Fowles SJ, White RJ. Radiographic appearances of Am J Roentgenol 1992;158:1211-1215 mycoplasma pneumonia. Thorax 1981;36:469-472 22. Marti-Bonmati L, Ruiz Perales F, Catala F, Mata JM, Calonge E. 6. Putman CE, Curtis AM, Simeone JF, Jensen P. Mycoplasma pneu- CT findings in Swyer-James syndrome. Radiology 1989;172:477- monia. Clinical and roentgenographic patterns. Am J Roentgenol 480

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대한방사선의학회지2003;48:361-367

소아 마이코플라즈마 폐렴 후유증으로 생긴 소기도 질환: 고해상CT소견 및 흉부 촬영 소견과의 상관 관계1

1서울대학교 의과대학 방사선과학교실, 방사선의학 연구소, 서울대학교병원 임상의학연구소 2서울대학교 의과대학 소아과학교실 3서울시립 보라매병원 방사선과

천정은1, 3·김우선·김인원·고영률 2·이환종 2·연경모

목적: 마이코플라즈마 폐렴을 앓고 난 환자에서 나타나는 소기도 질환의 고해상CT 소견을 알아보고, 고해상CT 소견과 폐렴 급성기 및 추적 관찰기의 흉부 촬영 소견과의 상관 관계를 알아보고자 하였다. 대상과 방법: 마이코플라즈마 폐렴을 앓고 난 후에 임상적으로 소기도 질환이 진단된 18명의 환자에서 고해상CT와 흉 부 촬영 소견을 후향적으로 분석하였다(남: 여=8: 10, 평균 연령 8.3세, 폐렴 급성기에서 CT까지 평균 기간; 26 개월). 고해상 CT에서 폐실질과 기관지의 이상 소견을 살펴보았고 호기시 시행한 고해상CT(n=13)에서 공기포획이 있는지 를 알아보았다. 흉부 촬영은 마이코플라즈마 폐렴의 급성기(n=15)와 CT를 시행한 시점의 추적 관찰기(n=18)로 나 누어 분석하였고, 이러한 흉부 촬영 소견과 고해상 CT 소견의 상관관계를 알아보았다. 결과: 고해상 CT에서 폐실질 내 이상 소견은 13명(72%)에서 발견되었다. 모자이크 형태의 저감쇄도의 폐음영이 10명 (56%)에서 보였고, 호기시 스캔을 시행한 13명중 9명(69%)에서 공기포획이 나타났다. 추적 흉부 촬영 소견에서 정상 소견을 보였던 14명중 9명(64%)에서 고해상CT에서 이러한 폐실질 이상 소견을 볼 수 있었다. 4명(27%)의 환자에서 폐렴 초기 흉부 촬영상 정상 소견으로 보인 부위에서 고해상CT영상에서는 이상 소견을 발견할 수 있었다. 기관지 확장 증과 무기폐는 각각 8명(44%)과 4명(22%)에서 보였다. Swyer-James 증후군을 시사하는 CT소견, 즉 폐용적 감소 와 혈관 감쇄를 동반한 일측성 과투과성 폐가 2명(11%)에서 관찰되었다. 결론: 고해상 CT는 소아 마이코플라즈마 폐렴의 후유증으로 발생한 소기도 질환에서 폐실질과 기관지의 이상을 찾는 데 유용하다.

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