Abnormal muscularization of the small pulmonary
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1 Surgical Indication for Congenital Heart Disease With Extremely Thickened Media of Small Pulmonary Arteries Shigeo Yamaki, MD, Ai Abe, MD, Masato Endo, MD, Takashi Tanaka, MD, Koichi Tabayashi, MD, and Tohru Takahashi, MD Department of Cardiology, Katta General Hospital, Shiroishi, and Department of Thoracic and Cardiovascular Surgery, Pediatrics, Tohoku University School of Medicine, Sendai, Japan. Background. Nineteen patients (mean age, 7.6 months) with a percent wall thickness of more than 33% in the small pulmonary arteries were found to have extremely thickened media. Based on our findings, a criterion of operative indication is proposed. Methods. The percentage of extremely thickened media of small pulmonary arteries for all pulmonary arteries was determined on microscopic lung sections and was introduced as an index for operative indication. Results. Operative repair was performed in 16 patients: 9 died intraoperatively and 7 survived more than 12 months. In 4 of 5 patients that had pulmonary artery banding, medial hypertrophy remained despite pulmonary artery banding. Operative repair also had no positive effect. In operative and late deaths and in survivors without a decrease of pulmonary arterial pressure, the percentage of extremely thickened media of small pulmonary arteries was shown to be more than 10%, whereas in 5 survivors and 1 operative death with a significant postoperative decrease of pulmonary arterial pressure, the value was less than 7%. Conclusions. If a patient has less than 7% of small pulmonary arteries with extremely thickened media, operative repair is likely to be effective. When the value is higher than 10%, not only operative repair but also pulmonary artery banding cannot be recommended because of ineffectiveness and hazard. (Ann Thorac Surg 1998;66:1560 4) 1998 by The Society of Thoracic Surgeons Abnormal muscularization of the small pulmonary arteries can occur because of unknown mechanisms operating in utero, forming extreme medial hypertrophy of the small pulmonary arteries, which is evident at birth. Here, by small pulmonary arteries, we mean both the intraacinar branches along the respiratory bronchioles and the supernumerary arteries [1]. This condition, when found in neonates or infants with right-to-left shunt caused by patent foramen ovale or patent ductus arteriosus, is known as idiopathic persistent pulmonary hypertension of neonates (IPPHN) [2]. We reported a case of coarctation of the aorta and aortic stenosis in which extremely thickened media were observed in the small pulmonary arteries [3]. In the present study, 19 patients with congenital heart disease having extremely thickened media of small pulmonary arteries are introduced. This category includes not only those with patent foramen ovale or patent ductus arteriosus, but those with various types of congenital heart disease, with the former corresponding to usual IPPHN. Changes of the small pulmonary arteries in such patients were analyzed by morphometry to establish criteria for an indication for cardiac surgical intervention. Accepted for publication May 18, Address reprint requests to Dr Yamaki, Department of Thoracic and Cardiovascular Surgery, Tohoku University School of Medicine, , Japan ( s-heart@mail.cc.tohoku.ac.jp). Patients and Methods A diagnosis of IPPHN is made whenever extremely thickened media of small pulmonary arteries are observed, but in such cases, the range of medial thickening has not been defined quantitatively. In the present study, a diagnosis of extremely thickened media of small pulmonary arteries was made when at least one small pulmonary artery had a mean medial thickness greater than the internal diameter of the vessel. This corresponds to the state in which the percent wall thickness (as defined in Fig 1) is more than 33% in a transection of a small pulmonary artery. Because the internal and external walls of small pulmonary arteries with extremely thickened media are not usually concentric circles, but rather oval and extremely distorted, the mean percent wall thickness of the major and minor axes was measured. In the present investigation, 19 cases (3.3%) were selected from a total of 560 autopsy and biopsy cases of congenital heart disease with pulmonary hypertension, the lung specimens of which were sent to the senior author from 75 hospitals for consultations between 1985 and In these specimens, a diagnosis of extremely thickened media of small pulmonary arteries was made clinically on the basis of data from cardiac catheterization and right-to-left shunt. Patients were excluded when pathologic analysis demonstrated either pulmonary parenchymal disorder or congenital malformation of the 1998 by The Society of Thoracic Surgeons /98/$19.00 Published by Elsevier Science Inc PII S (98)
2 Ann Thorac Surg YAMAKI ET AL 1998;66: EXTREMELY THICKENED PULMONARY ARTERIES 1561 Fig 1. A diagnosis of extremely thickened media of small pulmonary arteries was made when there were small pulmonary arteries in which the percentage wall thickness was 33% or greater, ie, when a b 2c. lung and upper airways. In the 19 patients thus selected, 9 were autopsied; in the other 10, prospective lung biopsy was performed to determine operability. Comparative retrospective examination was made with regard to the relationship between the results of operation and preoperative hemodynamics and pulmonary arterial changes. The ages of the 19 patients at the time of autopsy or lung biopsy ranged from 1 to 22 months, with a mean age of 7.6 months. There were 12 boys and 7 girls. The diagnoses are listed in Table 1. Lung biopsy or autopsy specimens were usually taken from the right middle lobe and fixed in 10% formalin for 3 days (simple formalin fixation). The size of the lung biopsy specimen was more than half the patient s thumb (about 15 6 mm). Thirty semiserial sections at 50- m intervals were prepared from each paraffin-embedded block. Each section usually included small pulmonary arteries with extremely thickened media that did not appear in the previous section. Sections were stained with modified Goldner trichrome combined with Weigert stain for elastic fibers [4]. This staining ensured clear discrimination of the internal and external elastic membranes and intimal lesions such as cellular or fibrous proliferation. The first of the semiserial sections of lung biopsy, corresponding to the deepest part of the biopsy specimen, contained a minimum of 12 and a maximum of 76 small pulmonary arteries. The total number of small pulmonary arteries in which morphometric analysis was performed was a minimum of 312 and a maximum of 1,908. The severity of the intimal lesions of small pulmonary arteries was determined according to our previously reported index of pulmonary vascular disease (IPVD) [5] and the Heath-Edwards classification [6]. Medial thickness was measured according to percent wall thickness. As simple formalin fixation might cause partial collapse of arteries, we usually use a Table 1. Clinical Findings and Morphometric Results in the Patients With Extremely Thickened Media of Small Pulmonary Arteries Case Age (mo) Cardiac Anomalies PAP (mm Hg) PVR (units m 2 ) IPVD HE Arterial Ratio (%) Operation Status 1 5 CAVC, Down 70/30 (48) Op repair Op death 2 8 CoA, VSD 50/12 (24) PAB, Op repair Op death 7 mo after PAB 3 9 PDA, ASD 100/60 (80) Op repair Op death 4 4 VSD, ASD 56/14 (35) Op repair Op death 5 1 PDA, CoA 65/27 (45) Op repair Op death 6 22 VSD, PDA, Down 93/46 (65) PAB, Op repair Op death 4 mo after PAB 7 10 ASD 69/24 (45) Not done Late death 8 6 VSD, PDA 70/41 (51) PAB Late death 9 7 CoA, AS 76/30 (49) Op repair Alive 10 6 VSD, ASD 96/46 (65) Op repair Alive VSD, Down 84/26 (54) Op repair Alive 12 9 VSD, PDA, Down 76/45 (60) Op repair Alive 13 2 DORV, VSD, MS 53/33 (41) BH, PAB Alive 14 9 VSD, PFO 83/39 (56) Op repair Alive 15 6 VSD, PDA, ASD 74/30 (52) Op repair Alive 16 7 DORV, VSD 60/27 (42) Op repair Op death CAVC 75/28 (49) Op repair Op death 18 4 CAVC, PDA, Down 92/50 (62) Op repair Alive 19 3 CoA, ASD, PDA 70/35 (50) PAB, Op repair Op death 6 mo after PAB Arterial ratio percent of arteries with more than 33% wall thickness; AS aortic stenosis; ASD atrial septal defect; BH Blalock-Hanlon; CAVC complete atrioventricular canal defect; CoA coarctation of the aorta; DORV double outlet right ventricle; Down down syndrome; HE Heath-Edwards classification; IPVD index of pulmonary vascular disease; MS mitral stenosis; Op operative; PAB pulmonary artery banding; PAP pulmonary arterial pressure; PDA patent ductus arteriosus; PFO patent foramen ovale; PVR pulmonary vascular resistance; VSD ventricular septal defect.
3 1562 YAMAKI ET AL Ann Thorac Surg EXTREMELY THICKENED PULMONARY ARTERIES 1998;66: Fig 2. Case 8. Small pulmonary arteries with extremely thickened media from a patient who died 10 months after pulmonary artery banding. Each small artery has an extremely thickened media, and the luminal space is small, leaving room for only a few red blood cells (RBC) to pass through. standardized technique [5] to offset the effect of collapse. In the present study, however, we applied percent wall thickness as described above, because postmortem contraction and collapse were slight if present in the very small pulmonary arteries with markedly thickened media. Moreover, this simple method allowed rapid measurement of many arteries. In cardiac catheterization, pulmonary flow was measured by the Fick method. Oxygen consumption was calculated based on the assumed oxygen consumption formula of Fixler and associates [7]. Oxygen saturation of the pulmonary vein was measured directly, but when a catheter did not enter the pulmonary vein, saturation of the wedged pulmonary artery was measured. Results The pulmonary arterial systolic pressure (PASP) of the 19 cases was between 50 and 100 mm Hg (mean, 74.3 mm Hg). The pulmonary arterial mean pressure (PAMP) was between 24 and 80 mm Hg (mean, 51.2 mm Hg). Pulmonary vascular resistance (PVR) was between 3.1 and 19.0 units m 2 (mean, 9.1 units m 2 ) (Table 1). The pulmonary arterial intimal changes remained mild, and IPVD ranged between 1.0 and 1.4 (mean, 1.1). The Heath- Edwards classification was grade 1 in 15 cases and grade 2 in 4. There were no cases classified as grade 3 or more. Operative repair was performed in 16 patients: 9 patients died during or shortly after operation and 7 patients survived for more than 12 months. Pulmonary artery banding (PAB) was performed in 5 patients (cases 2, 6, 8, 13, and 19), and in 4 of them (cases 2, 6, 8, and 13), the pulmonary trunk was tightly banded. Three of the 5 (cases 2, 6, and 19) died soon after operative repair was performed at 7, 4, and 6 months after PAB, respectively. On microscopic examination of the lung taken at autopsy of these patients, there were no signs of medial retardation in pulmonary arteries. In case 8, PAB was performed Fig 3. Case 10. The small pulmonary arteries show strongly hypertrophic media 4 months after operative repair. (RBC red blood cells.)
4 Ann Thorac Surg YAMAKI ET AL 1998;66: EXTREMELY THICKENED PULMONARY ARTERIES 1563 Fig 4. Comparison of cardiac catheterization in the operative survivors versus deceased patients. Asterisks indicate late deaths. (PAMP pulmonary arterial mean pressure; PASP pulmonary arterial systolic pressure; PVR pulmonary vascular resistance.) 1 month after birth and resulted in decreased pulmonary arterial pressure (PAP) to 20/17 (18) mm Hg immediately, apparently from tight banding (the length of the band was 23 mm). But in cardiac catheterization at 4 months of age, high PAP of 70/39 (50) mm Hg was ascertained, and the patient died at 10 months of age without receiving correction. The results of lung biopsy at 6 months of age indicated no retardation of hypertrophic media (Fig 2). In Case 10, PAP was 72/24 (43) mm Hg and operative repair was performed at age 2 months; 4 months later, however, the PAP was shown to be further increased to 96/46 (65) mm Hg, and PVR was as high as 19 units m 2. Lung biopsy at that time showed severe medial hypertrophy (Fig 3). In Figure 4, preoperative cardiac catheterization, PAP, and PVR are compared for the 19 patients who survived and those who died. In the operative and late deaths, PASP ranged from 50 to 100 mm Hg (mean, 70.7 mm Hg) and PAMP from 24 to 80 mm Hg (mean, 48.5 mm Hg). In the survivors, PASP ranged from 53 to 96 mm Hg (mean, 79.3 mm Hg) and PAMP from 41 to 62 mm Hg (mean, 54.9 mm Hg). Statistical analysis showed no significant Fig 5. The numerical percentage of small pulmonary arteries with percent wall thickness greater than 33% (percentage of thickened arteries) in 19 cases. Asterisks indicate cases in which pulmonary arterial pressure did not decrease. difference in PASP and PAMP between the operative deaths and the survivors (Fig 4). Pulmonary vascular resistance ranged from 3.1 to 13.3 units/m 2 (mean, 6.8 units/m 2 ) in the operative deaths and from 5.2 to 19.0 units/m 2 (mean, 11.7 units/m 2 ) in the survivors. Here also the differences were not significant. On the basis of microscopic observation of lung vessels among these patients, we introduce a criterion for determining operative indication, ie, the numeric percentage of small pulmonary arteries having a wall thickness greater than 33% for all pulmonary arteries in the sections (percentage of thickened arteries). The value was greater than 20% in the five operative deaths and in one of the late deaths after PAB (Fig 5). It was between 10% and 20% in three survivors, in three operative deaths after operative repair, and in one late death after lung biopsy. In these three survivors and in the late death, PAP did not decrease postoperatively. These results indicate that in these patients the operation was not an appropriate decision. The value was less than 7% in five survivors, four after operative repair and one after a Blalock-Hanlon operation and PAB, with a significant decrease in PAP confirmed in all. There was one operative death with a low value of 4.7%. Despite a significant decrease of PAP after operative repair (systolic pressure less than 30 mm Hg), this patient died suddenly after a pulmonary hypertensive crisis 3 days postoperatively. These results indicate that if a patient has less than 7% of the small pulmonary arteries with extremely thickened media, total correction should be performed. However, if more than 10% of small arteries have extremely thickened media, we do not recommend total correction or PAB because it will be without positive effect. Comment When pulmonary hypertension is present at birth and causes a right-to-left shunt through the patent ductus arteriosus or patent foramen ovale, it is termed persistent pulmonary hypertension of neonates. It is generally thought that persistent pulmonary hypertension of neonates is caused by many disorders, such as pulmonary parenchyma or congenital malformation of the lung and upper airways [8 10]. If there is abnormal medial thickening of the small pulmonary arterioles in the absence of such disorders, it is classified as IPPHN. The cause of such abnormal thickening of small pulmonary arterioles is uncertain and may be from chronic intrauterine hypoxia and sustained fetal pulmonary vasoconstriction [2]. In this study, we used the term extremely thickened media of small pulmonary arteries instead of IPPHN to include patients having not only patent foramen ovale or patent ductus arteriosus but also those with various types of congenital heart disease, because in the latter, the grade of medial hypertrophy was found to be the same or more severe. The indication for surgical intervention in cases of congenital heart disease with pulmonary hypertension is generally determined on the basis of hemodynamics measured by cardiac catheterization. In the present study, no difference was found in the hemodynamic data
5 1564 YAMAKI ET AL Ann Thorac Surg EXTREMELY THICKENED PULMONARY ARTERIES 1998;66: between the survivors and the fatalities with extremely thickened media of small pulmonary arteries. This result might be because we used the assumed oxygen consumption of Fixler and associates [7], which might not evaluate exactly the transient hypoxic changes induced by sedatives commonly used in infants during catheterization, especially those with Down syndrome. We conclude that, when right-to-left shunt is clinically dominant and severe pulmonary hypertension is ascertained, it is not possible to make a determination of operability on the basis of hemodynamics alone, where pathologic study is indispensable. There are detailed morphologic studies on the media of small pulmonary arteries in IPPHN [11, 12]. However, they do not provide a clear standard for a diagnosis of IPPHN with regard to thickness of the media. The present study allowed us to define a percentage wall thickness of 33% or more as diagnostic of extremely thickened media of small pulmonary arteries. This means that the thickness of the media is equal to or exceeds the diameter of the vascular lumen. In this condition, the vessels themselves must be extremely small (with diameter less than 30 m), and concurrently the media must be extremely hypertrophic. Operation using PAB in cases of congenital heart disease is usually effective in moderating pulmonary hypertension and helps retard the hypertrophic media of small pulmonary arteries [13, 14]. However, in four cases (cases 2, 6, 8, and 13), despite tight banding, there was no retardation of the medial hypertrophy of small pulmonary arteries 7, 4, 10, and 6 months after PAB, respectively. Moreoever, at biopsy 4 months after operative repair, no retardation of medial hypertrophy was comfirmed in case 10, indicating that even total correction fails to reduce the medial hypertrophy of small pulmonary arteries. With regard to the question of why PAB and operative repair fail to reduce the medial hypertrophy of small pulmonary arteries, we speculate that the pathogenesis of extremely thickened media of small pulmonary arteries is different from that of other congenital heart diseases with pulmonary hypertension. That is, in congenital diseases, medial hypertrophy is caused by increasing intraarterial pressure and results in retardation in proportion to the decreasing intraarterial pressure. Conversely, in extremely thickened arteries, the cause of medial hypertrophy in a fetus is unknown. Therefore, hypertrophy might not be retarded without removing the causes. Although PAB or operative repair generally is not effective for extremely thickened media of small pulmonary arteries, it might be indicated if such abnormally hypertrophied vessels comprise a small percentage of the total number of the arteries, ensuring that sufficient blood flow to the lungs is maintained by other vessels. The present results indicate that surgical correction may be appropriate when the percentage of these arteries is less than 7%. Even in such cases, however, there is a danger of postoperative pulmonary hypertensive crisis, as seen in case 16, indicating the need for intensive postoperative care, including administration of vasodilators such as prostaglandin E 1, prostaglandin E 2 and nitric oxide, as well as oxygen. We thank the following doctors for supplying us with materials: Kiyoshi Nagumo, MD, Hokkaido University School of Medicine, Sapporo; Toshio Kikuchi, MD, Katsuhiko Tatsuno, MD, and Yasuo Murakami, MD, The Sakakibara Heart Institute, Tokyo; Shigeo Tanaka, Aomori Prefectural Central Hospital, Aomori; Susumu Yonesaka, MD, Hirosaki University School of Medicine, Hirosaki; Tetsuo Sato, MD, Yamagata University School of Medicine, Yamagata; Takeo Sakai, MD, Tohoku University School of Medicine, Sendai; Kensuke Sakata, MD, Shimonoseki Saiseikai Hospital, Shimonoseki; Taketsugu Tsuda, MD, Fukui University School of Medicine, Fukui; Fumio Iwaya, MD, Fukushima Medical College, Fukushima; Kunitaka Shiroo, MD, and Akira Sese, MD, Kyushu Koseinenkin Hospital, Kitakyushu; Masamichi Tamura, MD, Akita University School of Medicine, Akita; Michio Yokota, MD, Shizuoka Childrens Hospital, Shizuoka; Motoyoshi Satomi, MD, Nagano Childrens Hospital, Nagano; Noboru Sai, MD, Chukyo Hospital, Nagoya; Seiichi Watanabe, MD, Tsuchiura Kyoudo Hospital, Tsuchiura; Masaki Aota, MD, Shinichi Nomoto, MD, and Toshihiko Ban, MD, Kyoto University School of Medicine, Kyoto. We also thank the following technical assistants, Mrs Takako Kato, Miss Junko Kato, and Mr Mitsuru Sasaki, Sendai City Medical Center, Sendai. References 1. Elliott FM, Reid LM. Some new facts about the pulmonary artery and its branching pattern. Clin Radiol 1965;16: Moller JH, Neal WA. Fetal, neonatal, and infant cardiac disease. In: Emmanouilides GC, ed. Persistent pulmonary hypertension in the neonate. Norwalk, Connecticut: Appleton & Lange, 1990: Aota M, Nomoto S, Yamaki S, Ban T. Pulmonary hypertension caused by medial hypertrophy associated with aortic stenosis and preductal coarctation. Ann Thorac Surg 1997;64: Goldner J. A modification of the Masson trichrome technique for the routine laboratory purposes. Am J Pathol 1938; 14: Yamaki S, Tezuka F. Quantitative analysis of pulmonary vascular disease in complete transposition of the great arteries. Circulation 1976;54: Heath D, Edwards JE. The pathology of hypertensive pulmonary vascular disease: description of six grades of structural changes in the pulmonary arteries with special reference to congenital cardiac septal defects. Circulation 1958;18: Fixler DE, Carell T, Browne R, Willis K, Miller WW. Oxygen comsumption in infants and children during cardiac catheterization under different sedation regiments. Circulation 1974;50: Drummond W, Gregory G, Heymann M, Phibbs R. The independent effects of hyperventilation, tolazoline and dopamine on infants with persistent pulmonary hypertension. J Pediatr 1981;98: Rowe RD, Hoffman T. Transient myocardial ischemia of the newborn infants. A form of severe cardiorespiratory distress in full-term infants. J Pediatr 1972;81: Hageman JR, Adams MA, Gardner TH. Persistent pulmonary hypertension of the newborn: trends in incidence, diagnosis, and management. Am J Dis Child 1984;138: Murphy JD, Rabinovitch M, Goldstein JD, Reid LM. The structural basis of persistent pulmonary hypertension of the newborn infant. J Pediatr 1981;98: Haworth SG, Reid LM. Persistent fetal circulation: newly recognized structural features. J Pediatr 1976;88: Wagenvoort CA, Wagenvoort N, Draurans-Noe Y. Reversibility of plexogenic pulmonary arteriopathy following banding of the pulmonary artery. J Thorac Cardiovasc Surg 1984; 87: Yamaki S, Ajiki H, Haneda K, Takanashi Y, Ban T, Takahashi T. Pulmonary arterial changes in patients dying after a modified Fontan procedure following pulmonary artery banding. Heart Vessels 1993;9:263 8.
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