Journal of Pathology and Translational Medicine

Original Articles

Quilty Lesions in the Endomyocardial Biopsies after Heart Transplantation: Haeyon Cho, Jin-Oh Choi, Eun-Seok Jeon, Jung-Sun Kim; J Pathol Transl Med. 2019;53(1):50-56. Published online December 26, 2018; DOI: https://doi.org/10.4132/jptm.2018.11.30

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Background
The aim of this study was to investigate the clinical significance of Quilty lesions in endomyocardial biopsies (EMBs) of cardiac transplantation patients.
Methods
A total of 1190EMBs from 117 cardiac transplantation patients were evaluated histologically for Quilty lesions,acute cellular rejection, and antibody-mediated rejection. Cardiac allograft vasculopathy wasdiagnosed by computed tomography coronary angiography. Clinical information, including thepatients’ survival was retrieved by a review of medical records.
Results
Eighty-eight patients(75.2%) were diagnosed with Quilty lesions, which were significantly associated with acute cellularrejection, but not with acute cellular rejection ≥ 2R or antibody-mediated rejection. In patientsdiagnosed with both Quilty lesions and acute cellular rejection, the time-to-onset of Quilty lesionsfrom transplantation was longer than that of acute cellular rejections. We found a significant associationbetween Quilty lesions and cardiac allograft vasculopathy. No significant relationship wasfound between Quilty lesions and the patients’ survival.
Conclusions
Quilty lesion may be an indicator of previous acute cellular rejection rather than a predictor for future acute cellular rejection.

Citations

Citations to this article as recorded by

The human myocardium harbors a population of naive B-cells with a distinctive gene expression signature conserved across species
Kevin C. Bermea, Nicolas Kostelecky, Sylvie T. Rousseau, Chieh-Yu Lin, Luigi Adamo
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Examination of tracheal allografts after long-term survival in dogs
Tao Lu, Yiwei Huang, Yulei Qiao, Yongxing Zhang, Yu Liu
European Journal of Cardio-Thoracic Surgery.2021; 59(1): 155. CrossRef
Essentials in the diagnosis of postoperative myocardial lesions similar to or unrelated to rejection in heart transplant
Costel Dumitru, Ancuta Zazgyva, Adriana Habor, Ovidiu Cotoi, Horațiu Suciu, Carmen Cotrutz, Bogdan Grecu, Ileana Anca Sin
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Clinical outcome of donor heart with prolonged cold ischemic time: A single‐center study
Fazal Shafiq, Yixuan Wang, Geng Li, Zongtao Liu, Fei Li, Ying Zhou, Li Xu, Xingjian Hu, Nianguo Dong
Journal of Cardiac Surgery.2020; 35(2): 397. CrossRef
The XVth Banff Conference on Allograft Pathology the Banff Workshop Heart Report: Improving the diagnostic yield from endomyocardial biopsies and Quilty effect revisited
Jean-Paul Duong Van Huyen, Marny Fedrigo, Gregory A. Fishbein, Ornella Leone, Desley Neil, Charles Marboe, Eliot Peyster, Jan von der Thüsen, Alexandre Loupy, Michael Mengel, Monica P. Revelo, Benjamin Adam, Patrick Bruneval, Annalisa Angelini, Dylan V. M
American Journal of Transplantation.2020; 20(12): 3308. CrossRef

The Significance of Ventricular Volume in the Evaluation of Secondary Cardiomyopathy at Autopsy.: Joo Young Na, Byung Woo Min, Yeong Hui Kim, Seung Hyun Chung, Young Jik Lee, Hyung Seok Kim, Jong Tae Park; Korean J Pathol. 2011;45(4):336-347.; DOI: https://doi.org/10.4132/KoreanJPathol.2011.45.4.336

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Abstract PDF: BACKGROUND
The weight, shape and consistency of the heart, and the thickness of the ventricular wall are used as parameters for evaluating postmortem heart and diagnosing cardiomyopathy at autopsy.
METHODS
The weight and volume of the ventricles and the thickness of the left ventricular wall of 58 hearts were measured and analyzed.
RESULTS
In the group of dilated hearts, the ventricular weight, ventricular volume, ventricular volume/ventricular weight, and left ventricular volume/right ventricular volume increased, whereas ventricular wall thickness decreased. In the group of hypertrophied hearts, the ventricular weight, ventricular volume, and thickness of the ventricular wall increased but ventricular volume/ventricular weight and left ventricular volume/right ventricular volume did not change significantly. In the group of undetermined hearts, it was later found that four of the cases should have been included in the dilated heart group and another two cases in the hypertrophied heart group.
CONCLUSIONS
In addition to conventional methods, the measuring ventricular volume is useful for evaluating a postmortem heart and may suggest postmortem differential diagnoses of dilated or hypertrophied forms of secondary cardiomyopathies.

Pathological Analysis of Post-Transplantation Endomyocardial Biopsies.: Jaegul Chung, Soonae Oak, Gheeyoung Choe, Gyungyub Gong, Jooryung Huh, Eunsil Yu, Inchul Lee, Meong Gun Song, Kwang Hyun Sohn, Jae Joong Kim, Jong Goo Lee; Korean J Pathol. 1995;29(4):431-441.

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Abstract PDF: Heart transplantation was first performed in 1967. It is now regarded as a well-established treatment modality for end-stage cardiac diseases. Once the transplantation is performed, endomyocardial biopsy(EMB) is the examination of choice in monitoring the transplanted heart. We analyzed the pathological findings of follow-up EMB of 6 heart transplant patients. All patients have been suffered from severe heart failure. Four patients were adult male and two were adult females. All the hearts, except for one, displayed characteristic features of dilated cardiomyopathy. The remaining heart was diagnosed as having giant cell myocarditis. Post-transplantion EMBs were performed according to the protocol and standard cardiac biopsy grading of ISHT (1990). The standards were applied for grading of cellular rejection. In five patients, there were one or two episodes of biopsy proven acute rejection, grade II or IIIA without any clinical symptoms of rejection. Immediate "pulse therapy" was performed and follow-up biopsies were done. All episodes of rejection were cleared in subsequent biopsies. All patients are doing well without evidence of cardiac problem. The postoperative monitoring of acute rejection is critical since clinical signs of rejection are usually absent. At present, EMB is regarded as the most reliable method for diagnosis and grading of acute rejection and is an efficient guide to the monitoring of the cardiac recipients. Our experience of post-transplantation EMB corresponds with previously published reports.

Case Reports

Giant Cell Myocarditis: A case report.: Ho Jung Lee, Jae Gul Chung, In Chul Lee, Myeong Gun Song, Jae Jung Kim, Jong Goo Lee; Korean J Pathol. 1996;30(6):523-527.

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Abstract PDF: Giant cell myocarditis(GCM) is a rare inflammatory heart disease which is characterized by multinucleated giant cells and a granulomatous reaction. It usually progresses rapidly and results in a fatal course. We report a patient with giant cell myocarditis who was treated by cardiac transplantation. A 35-year-old male was admitted with dyspnea which had developed 4 months before. On echocardiography, the right and left ventricles were markedly dilated and severe global hypokinesia was noted. He was diagosed with dilated cardiomyopathy with secondary severe mitral regurgitation. His cardiac function deteriorated progressively. He underwent orthotopic heart transplantation. Grossly the heart was enlarged, weighing 420gm and round with a blunt apex. Both right and left ventricles were markedly dilated. There were numerous white patches, measuring up to 4cm, throughout the epi- and myocardium. Microscopically, extensive fibrosis and multiple exuberant granulomas with numerous scattered multinucleated giant cells were seen. Lymphocytes and eosinophils were also frequent. Coronary arteries were unremarkable. Neither microorganisms nor foreign materials were found. By serial endomyocardial biopsies of the transplanted heart, only mild perivascular lymphocytic infiltration was occasionally observed without any evidence of rejection or recurrence of giant cell myocarditis. The patient's postoperative course has been uneventful so far(postoperative 21 months). The etiology of GCM remains to be clarified, although various factors are suspected. No matter what the cause, our experience suggests that this grave disease might be treated well by heart transplantation.

Lipoma of the Heart: An Autopsy case report.: Min Hee Jung, Suk Hee Lee, Sang Han Lee, Jong Min Chae, Jung Sik Kwak; Korean J Pathol. 1996;30(8):746-748.

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Abstract PDF: Lipomas of the heart are benign neoplasms and have rarely been described. Due to the fact that they normally cause no symptoms, diagnosis is often purely accidental. Because of the rarity of these tumors, it seems worthwhile to present an example studied at autopsy. It was associated with the sudden death of a 15-year-old boy. The tumor arose from the wall of the left ventricle and occupied the pericardial cavity, measuring 13x7x6 cm in size. The tumor was whitish-yellow, translucent, and soft. Microscopically, the tumor was composed of mature adipose tissue which extended between muscle fibers. This current case, the giant cardiac lipoma is believed to produce disturbances of the conduction system and distrubances of cardiac filling.

Original Articles

Pathologic Analysis of Endomyocardial Biopsies in Heart Transplantation.: Mee Hye Oh, Jeong Wook Seo, Kook Yang Park, Young Tak Lee, Yoon Seop Jeong, Suk Keun Hong, Joon Ryang Rho, Byung Hee Oh, Sung Sook Kim; Korean J Pathol. 1998;32(2):104-114.

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Abstract PDF: Endomyocardial biopsy (EMB) is a valuable diagnostic procedure for the surveillance of cardiac allograft rejection. Interpretation of individual cases is still problematic due to variations of findings for grading of rejection and other associated lesions. We reevaluated an experience on endomyocardial biopsies to develop better diagnostic criteria for rejection and other complications. Immunohistochemical studies against cytokines were performed to assess the usefulness of the method for the diagnosis or researches. A total of 249 EMBs taken from 33 cardiac allograft recipients were reviewed. There were 25 males and 8 females. Dilated cardiomyopathy was present (24 cases) and valvular heart disease (4 cases), restrictive cardiomyopathy (3 cases) were also common conditions. We applied the grading system of the International Society for Heart Transplantation (ISHT) for the assessment of acute cellular rejection. Grades of 0, 1A, 1B, 2, 3A and 3B were 39.0%, 28.1%, 11.2%, 11.5%, 12.4% and 1.6% respectively, but 3.2% were inadequate. Thirty five episodes of grade 3A or 3B were present in 17 patients. The response to therapy was assessed using a next follow up biopsy, which revealed resolving or resolved rejection in 85% of patients. The intensity of immunohistochemical stains for IL-6 and TNF-alpha was increased in proportion to the histologic grade but Quilty lesion and cardiomyopathy also showed a positive reaction. The other pathologic findings were ischemic change, previous biopsy site, interstitial edema and fibrosis, and Quilty lesion. These findings showed usefulness of endomyocardial biopsy not only for the evaluation of cardiac allograft rejection but also for the diagnosis of associated cardiac lesions. Immunohistochemical study of the cytokines was related to the degree of inflammation rather than degree of rejection.

The Role of Cell Proliferation and Apoptosis in the Cardiac Development.: Eo Jin Kim, Hyo Soo Kim, Jeong Wook Seo; Korean J Pathol. 1998;32(12):1049-1057.

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Abstract: The functional and morphologic cardiac developments are determined by the morphogenesis, growth and remodeling of the heart resulted from the cell proliferation and apoptosis. We studied the distribution of the proliferation and apoptotic activity of myocardial cells according to the developmental stages in embryos of C57bl/6 mice. Serial histologic sections were stained with PCNA and TUNEL method and were analyzed with image analyzer (BMI, Seoul). The ventricular myocardium of an embryonic heart could be divided into trabecular, inner compact and outer compact layers. Proliferation indices at layers of the left ventricular myocardium on embryonal days (ED) 13, 14, 16, 17 and 18 were 19.9%/47.4%/60.4%, 16.1%/45.8%/60.3%, 24.6%/45.6%/38.1%, 23.3%/17.7%/18.3% and 31.2%/28.0%/19.4% (trabecular/ inner compact/ outer compact) and the right ventricle, 11.0%/34.4%/60.5%, 23.0%/44.0%/69.0%, 29.2%/42.9%/35.1%, 30.4%/30.5%/22.3% and 32.4%/28.4%/16.3%. The apoptotic indices of the left ventricle/VIF were 0.23%/3.66% on ED 13-14, 0.42%/1.31% on ED 16 and 0.05%/0.60% on ED 17-18. The results show that the proliferation of the myocytes was maximal at the outer compact layer on ED 13 and 14 but lowest on ED 17 and 18. This decrease was more pronounced at the left ventricle. The innermost trabecular layer showed a constant proliferation activity of 11.0-32.4%. The presence of spatiotemporal differences in the cell proliferation reveals regional regulation in the developmental timing of cardiac development. Functional maturation is considered to be responsible for the change of proliferation activity. The apoptosis was most frequent and intense in the VIF and crux throughout the periods of each embryonal day where as rarely seen in the ventricular myocardium, especially in the trabecular layer of myocardium. These findings suggest that the apoptosis plays the role in the development of atrioventricular, ventriculoarterial septation and valve formation. Our results also reveal that the participation of apoptosis in formation of the trabeculation can be denied.

Relation of Heart Weight to Body Weight, Body Surface Area, Height, and Age in Normal Korean Men and Women.: Hee Soo Yoon, Hea Soo Koo, Joong Seok Seo, Sang Yong Lee, Jung Duck Park, Moo Yeol Lee, Sang Ho Cho; Korean J Pathol. 1999;33(1):1-8.

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Abstract PDF: Cardiovascular diseases have been the most serious threat to life and health. The socioeconomic ramifications of heart disease have long been a source of vexing legal as well as medical problems with no easy resolution as yet in hand. Heart weight, one of the important factors for the diagnosis of cardiomegaly and various heart diseases, shows extreme variability according to the height, weight, age, sex, nutritional status of individuals as well as other various factors. The purpose of this investigation was to find a practical method for calculating expected normal range of heart weight in a given individual. The study was performed on 259 autopsy cases of normal Korean men and women, consisting of 123 men and 136 women in age from newborn to 77 years old. Height, body weight, and heart weight were measured and the body surface area was calculated by height (cm)0.725 x weight (kg)0.425 x 71.84 and height (cm)0.7763 x weight (kg)0.4081 x 71.84 in men and women, respectively. The results showed that the mean heart weight of men and women older than 20 years old were 316.20 +/- 51.15 g (n=96) and 275.87 +/- 44.69 g (n=108), respectively. Heart weight was gradually increased according to the age. The body weight (men: r=0.81, women: r=0.84) and body surface area (men: r=0.83, women: r=0.83) were better univariate predictors of normal heart weight than body height (men: r=0.78, women: r=0.75) and age (men: r=0.42, women: r=0.57). No significant difference was found in predictive precision between body weight and body surface area. Since the body surface area was calculated from body weight and height, measuring the body weight was essential for calculating expected normal range of heart weight in a given individual, and calculation of expected normal range of heart weight using body weight was simpler method than using body surface area.

Morphometric Study for Muscular and Microvascular Remodeling of Left Ventricular Free Wall and Interventricular Septum in Hypertrophic Cardiomyopathy.: Young Jik Lee, Hyung Suk Kim, Jong Tae Park, Chang Soo Park; Korean J Pathol. 1999;33(9):675-683.

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Abstract PDF: Hypertrophic cardiomyopathy (HCMP) is characterized myofiber hypertrophy and structural remodeling with changes in the proportion of the muscular, vascular, and interstitial compartments. A study was done to determine the structural remodeling patterns and the role of microvasculature of hearts in HCMP. Forty-two postmortem hearts were analyzed including 14 from patients who died of HCMP (group 1), 8 patients with HCMP but who died from extracardiac causes (group 2), 10 patients with ischemic heart disease (group 3), and 10 normal adult hearts (group 4). Macro- and microscopic examination, immunohistochemical study using CD34 antibody, and morphometric studies using image analyzer were performed. Mean cardiac weight and wall thickness were significantly higher in the HCMP group. Myocardial hypertrophy, and a variety of myocardial disarray and fibrosis involved the whole area of the left ventricles with HCMP. The percentage areas of microvessels were 6.40 0.7 in group 1, 5.90 0.6 in group 2, 4.98 0.3 in group 3, 4.85 0.4 in group 4, respectively, and the numbers of microvessels were 198.0 20.7 in group 1, 230.0 22.3 in group 2, 211.7 11.2 in group 3, and 236.4 11.4 in group 4, respectively (mean SE). The percentage area of microvessels was significantly higher in group 1 than in other groups. However, the number of microvessels in that group was lower than in the other groups, although it was statistically insignificant. Since flow-dependent vasodilation is preserved in HCMP, we considered flow-dependent vasodilation the cause of the discrepancy between the area and the number of microvessels. Ischemic changes observed in chronic HCMP and related heart failure were considesed to be due to the relative deficiency of the coronary flow compared to the increasing cardiac mass.

Case Reports

Cardiac Sarcoidosis Treated by Cardiac Transplantation: A Case Report.: Jaejung Jang, Kwangseon Min, Gyeong cheon Jung, Jaejung Kim, Inchul Lee; Korean J Pathol. 2001;35(1):71-75.

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Abstract PDF: Sarcoidosis, in general, has a low mortality rate. But cardiac sarcoidosis (CS) is a serious condition which may lead to death. Here, we report a rare case of CS that was treated by heart transplantation. A 47-year-old male had occasional syncopes and atypical chest pain. Ventricular tachycardia with right bundle branch block was noted by electrocardiogram. Multiple fixed myocardial perfusion defects in the interventricular septum and both the inferior-posterior ventricular walls were observed by thallium scan. Coronary angiography was unremarkable. Neither perihilar nor mediastinal lymphadenopathy was noted. The patient also suffered three times from tonic-clonic generalized seizures in 3 years, but no neurologic abnormalities were detected. The explanted heart displayed multiple white patches on the endomyocardial surface, measuring up to 8x7 cm. On microscopic examination, the lesion consisted of multiple well-formed and confluent granulomas with numerous scattered multinucleated giant cells, CD68-positive epithelioid histiocytes, and T-lymphocytes. Neither microorganisms nor foreign material was identified on special stain and culture study. It has been six months since the heart transplant, and the patient has been doing well.

Plexogenic Pulmonary Arteriopathy in Congenital Heart Disease: A Report of Two Cases.: Seung Yeon Ha, Kook Yang Park, Hyun Yee Cho, Young Ha Oh, Jae Gul Chung, Dong Hae Chung, Chung Yeul Kim, Han Kyeom Kim; Korean J Pathol. 2002;36(6):412-415.

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Abstract PDF: Hypertensive pulmonary vascular disease can develop in those cases of congenital cardiac shunt in which critical levels of pulmonary artery pressure and flow are reached and exceeded. We have experienced two cases of plexogenic arteriopathy in complex congenital heart disease and tried to evaluate of distribution of arterial lesions by total mapping of the explanted lung. Case 1 and 2 were 12-year-old boy and 36 year-old man. They were treated with combined heart-lung transplantation. Mapping of the both lungs was done, and graded according to Heath and Edward's grading scheme. The elastic pulmonary artery was tortuous, dilated and aortic configuration. Both lungs showed mostly grade 3. Plexiform lesion or veinlike branches of hypertrophied muscular arteries arosed in a lateral branch of a muscular artery that might be proximal to an area of occlusion. Comprising the right and left lung, the right was more severe than the left. By getting closer to the distal part, the grade tended to increase to 4 to 5. By analyzing the pulmonary lobe, severe pulmonary hypertension of grade 4 or 5 was comparatively disseminated throughout the right lung. On the other hand, in the left lung, the grade of the lower lobe was higher than that of the upper lobe, and within the upper lobe, there was a tendency for the grade of inferior segment to be higher than that of the corresponding apical segment.

Lipomatous Hypertrophy of the Interatrial Septum: A Case Report.: Ji Eun Kwak, Han Seong Kim, Mee Joo, Sun Hee Chang, Sang Hwa Shim, Je G Chi, Wook Sung Kim; Korean J Pathol. 2007;41(3):213-215.

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Abstract PDF: Lipomatous hypertrophy of the interatrial septum is a benign cardiac mass that is characterized by excessive deposition of fat in the interatrial septum. It typically occurs in elderly, obese patients and may cause arrhythmia. We report a case of lipomatous hypertrophy of the interatrial septum. A 45-year-old man was admitted for evaluation of chest discomfort. Transthoracic echocardiography revealed a cardiac mass, which was suspected as a myxoma. A resection of the tumor was performed. Grossly, the mass was 1.3x1.2x0.8 cm, and showed yellow soft consistency and good demarcation. Microscopically, the mass consisted of mature adipose tissue, intermixed cardiac muscle fibers, entrapped nerve fibers and ganglion cells. Lipomatous hypertrophy of the interatrial septum should be differentiated pathologically from tumorous cardiac mass such as lipoma and myxoma.

Original Article

Morphologic Difference of the Atrial Chambers and Determination of the Atrial Situs in the Normal and Congenitally Malformed Heart.: Eo Jin Kim, Jeong Wook Seo; Korean J Pathol. 2004;38(3):174-180.

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Abstract PDF: BACKGROUND
Identification of atrial situs is the initial step in any segmental analysis and classification of congenital heart malformations. To elucidate the differences for both atria of the normal and congenitally malformed heart, we performed morphological studies on the human heart with or without abnormal laterality syndrome.
METHODS
Five normally formed human hearts, five hearts with right isomerism and five hearts with left isomerism were used in this study. The postero-superior walls of the atrial chambers were examined.
RESULTS
Although the division line of the ventral and dorsal compartments was not as conspicuous as was seen in the right atrium of rat embryo previously studied, this division line existed as a well-developed terminal crest and vestigial structure of the antero-lateral extension of the terminal crest. These structures were noted in the right atrial chambers of normal human hearts and in the bilateral atrial chambers of right isomerism. However, they were totally absent in the bilateral atrial chambers in hearts with left isomerism.
CONCLUSIONS
Our study showed that the right atrial chamber in the normally developed human heart has vestigial components of division between the ventral and dorsal compartment, and hearts with right isomerism and left isomerism have differential development of the ventral and the dorsal compartment.

Case Reports

Alagille Syndrome: A Case Report.: Hyosup Shim, Chanil Park, Soon Il Kim, Young Nyun Park; Korean J Pathol. 2004;38(1):56-59.

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Abstract PDF: Alagille syndrome is a rare autosomal dominant disorder showing complicated systemic manifestations, although the hepatic manifestations are predominant in many patients. We report a case of Alagille syndrome in a male baby who presented with a heart murmur at 2 days old and his echocardiography showed aortic stenosis. He presented with acholic stool and jaundice at 3 months old and a liver biopsy revealed paucity of the interlobular bile duct in the portal tract. This progressed to cirrhosis, for which a liver transplantation was performed at 10 months old. The explanted liver showed biliary-type cirrhosis with severe cholestasis. There was an absence of the interlobular bile ducts on microscopic examination. Bile duct paucity, associated with cholestasis, a peculiar face (prominent forehead, deep-set eyes, pointed mandible and bulbous nasal tip), and cardiac anomaly were observed, which were consistent with Alagille syndrome. He died of heart failure.

Sirenomelia: An autopsy case report.: Yeong Ju Woo, Hye Kyoung Yoon, In Sook Lim; Korean J Pathol. 1994;28(1):96-98.

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Abstract PDF: Sirenomelia is a severe form of caudal regression syndrome that results in a fusion of the lower extremities, which is not compatible with life. A various spectrum of anomalies affecting primarily the musculoskeletal, genitourinary and gastrointestinal systems also can occur. This rare malformation has a reported incidence rate of approximately 1 in 60,000 births, with a range of 1 to 1 percent of all malformed infants. We experienced a sirenomelic case with combined anomalies of genitourinary, cardiovascular and gastrointestinal systems. Maternal obstetric history revealed oligohydramnios and intrauterine fetal growth retardation, and the baby was spontaneously delivered at 37 weeks of gestational age, but died I hour after birth.

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