犬心包积液的超声心动图和临床病理学特征:107 例 (1985–2006)

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Echocardiographic and clinicopathologic characterization of pericardial effusion in dogs: 107 cases (1985–2006)

目录

1 摘要

目的:评价超声心动图诊断犬心包积液心脏肿块的敏感性和特异性。

设计:回顾性案例系列。

动物:107 只患有心包积液的狗。

程序:回顾了 1985 年至 2006 年在加州大学戴维斯分校兽医教学医院检查的心包积液狗的记录。狗狗进行了包括超声心动图、心包切除术或尸检。计算了心包积液各种病因的敏感性、特异性和转移率。

结果: 107 只心包积液犬通过手术 (n = 48 ) 、尸检 (44) 或两者皆进行 (15) 进行评估。超声心动图显示无肿块 (n = 41)、右心房 (RA) 肿块 (38)、心基 (HB) 肿块 (23)、心包肿块 (2)、HB 和 RA 肿块 (2) 以及右心室肿块 (1)。检测心脏肿块的敏感性和特异性分别为 82% 和 100%;分别为 82% 和 99% 用于检测 RA 质量;分别为 74% 和 98% 用于检测 HB 肿块。大多数 HB 肿块为神经内分泌或异位甲状腺组织,但 3 例为血管肉瘤,4 例为间皮瘤。大多数 RA 肿块是血管肉瘤,但该组还包括神经内分泌肿瘤、异位甲状腺组织、间皮瘤、淋巴肉瘤和肉瘤。肿瘤病因的转移率没有差异(50%-66%)。

结论与临床相关性:超声心动图对心包积液犬的 RA 或 HB 肿块的诊断和鉴别具有较高的敏感性和特异性。所有原因导致的心脏肿块的转移率都很高。(J Am Vet Med Assoc 2009;235:1456–1461)


2 正文

心包积液是狗中一种相当常见的获得性心脏病。据报道,在转诊兽医医院检查的狗的患病率为 0.43% (1/233),在有心脏病临床症状的狗中,患病率约为 7%。[1] 它是一种多发病因疾病,预后范围广泛,从良好到严重不等。[2] 狗心包积液的最常见原因包括右心房血管肉瘤、特发性心包炎和心脏基底化学感受器瘤 (chemodectoma)。[3–5]

Pericardial effusion is a fairly common acquired cardiac condition in dogs. Prevalence has been reported to be 0.43% (1/233) for dogs examined at a referral veterinary hospital, and it accounts for approximately 7% of dogs with clinical signs of cardiac disease.[1] It is a multiple-etiologic disorder with a wide spectrum of prognoses that range from good to grave.[2] The mostcommon causes of pericardial effusion in dogs include hemangiosarcoma of the right atrium, idiopathic pericarditis, and chemodectoma of the heart base.[3–5]


确定心包积液的病因可提供有关适当治疗、临床进展和预后的宝贵信息。继发于肿瘤性原因的心包积液的狗预后不良,存活时间从 26 到 56 天不等,这比继发于非肿瘤性原因的心包积液的狗的较长生存时间 790 到 1,068 天要短得多。[3,6] 继发于心脏基础肿块的心包积液的狗通常比患有血管肉瘤的狗预后更好, 特别是当他们接受心包切除术时。[7–9] 接受心包切除术的心脏基底肿块的狗比未接受心包切除术的狗存活时间(中位生存时间,730 天)更长(中位生存时间,42 天)[7]。

Determination of the cause of pericardial effusion provides valuable information regarding appropriate treatment, clinical progression, and prognosis. Dogs with pericardial effusion secondary to neoplastic causes have a poor prognosis, with survival times ranging from 26 to 56 days, which is substantially shorter than the longer survival times of 790 to 1,068 days for dogs with pericardial effusion secondary to nonneoplastic causes.[3,6] Dogs with pericardial effusion secondary to a heart base mass typically have a better prognosis than dogs with hemangiosarcoma, especially when they undergo pericardectomy.[7–9] Dogs with heart base masses that underwent pericardectomy survived longer (median survival time, 730 days) than those that did not undergo pericardectomy (median survival time, 42 days).[7]


超声心动图是诊断心包积液以及评估病因的重要程序,包括心脏肿块的识别和定位、结构性或功能性心脏病的检测以及积液严重程度的评估,用于定义治疗计划。 首次检查的敏感性在 17% 到 50% 之间变化,重复检查时增加到 69%[4,11] 然而,尚未进行任何研究来评估超声心动图区分右心房肿块和心脏基底肿块的敏感性或特异性,这通常具有预后意义。此外,上述许多研究都是使用缺乏现代超声机的分辨率和帧速率的超声机进行的。

Echocardiography is an essential procedure for diagnosis of pericardial effusion as well as evaluation of the cause, including the identification and location of cardiac masses, detection of structural or functional cardiac disease, and assessment of the severity of the effusion, for use in defining a therapeutic plan.10 There is a wide range in the reported sensitivity for echocardiographic detection of cardiac masses, which varies between 17% and 50% for first-time examinations and increases to 69% for repeat examinations.[4,11] However, no studies have been conducted to evaluate the sensitivity or specificity of echocardiography for distinguishing right atrial masses from heart base masses, which often has prognostic implications. In addition, many of the aforementioned studies were performed with ultrasound machines that lacked the resolution and frame rates of modern ultrasound machines.


此报告的研究具体目标是确定超声心动图在检测心包积液狗的心脏肿块、区分右心房肿块与心包积液的其他原因以及区分心基底肿块与心包积液的其他原因的敏感性和特异性。次要目标包括确定心脏内肿瘤的具体肿瘤原因和位置,比较心包积液肿瘤原因的转移率,以及描述心包积液狗的临床病理异常。

The specific objectives of the study reported here were to determine the sensitivity and specificity of echocardiography for detection of a cardiac mass in dogs with pericardial effusion, for distinguishing right atrial masses from other causes of pericardial effusion, and for distinguishing heart base masses from other causes of pericardial effusion. Secondary objectives included defining the specific neoplastic causes and locations of neoplasms within the heart, comparing metastatic rates of neoplastic causes of pericardial effusion, and characterizing clinicopathologic abnormalities in dogs with pericardial effusion.


3 材料和方法

病例选择:通过搜索 1985 年至 2006 年加州大学戴维斯分校兽医医学教学医院数据库确定了心包积液的狗。所有狗都由董事会认证的兽医心脏病专家或受监督的心脏病学住院医师进行了超声心动图检查。所有狗都必须至少通过使用超声心动图确定轻度心包积液才能被纳入研究,并且没有心包积液的超声心动图证据的狗不包括在内。通过超声心动图确定轻度或更大程度心包积液的狗被纳入研究,当时在那次就诊期间或随后的就诊期间进行心包切除术或尸检以确认心包积液的原因。接受胸腔镜心包切除术的狗被排除在外,因为在手术过程中无法看到整个心脏。所有患有心脏或心包肿块的狗的肿瘤病因的诊断是通过对手术或尸检期间获得的活检标本进行组织学评估做出的。除了患有感染性心包炎的狗外,心包积液的非肿瘤性原因的诊断也通过组织学进行诊断。

Case selection — Dogs with pericardial effusion were identified by searching the University of California-Davis Veterinary Medical Teaching Hospital database from 1985 through 2006. All dogs had an echocardiogram performed by a board-certified veterinary cardiologist or a supervised cardiology resident. All dogs were required to have at least mild pericardial effusion identified by use of echocardiography to be included in the study, and dogs with echocardiographic evidence of a cardiac mass without pericardial effusion were not included. Dogs with mild or greater pericardial effusion identified by echocardiography were included in the study when pericardectomy or necropsy was performed during that visit or a subsequent visit to confirm the cause of the pericardial effusion. Dogs undergoing thoracoscopic pericardectomy were excluded because of an inability to view the entire heart during that procedure. Diagnosis of the neoplastic cause in all dogs with cardiac or pericardial masses was made by histologic evaluation of biopsy specimens obtained during surgery or necropsy. Except for dogs with infective pericarditis, diagnosis of nonneoplastic causes of pericardial effusion was also made histologically.


病历审查:获得多个超声心动图视图,以彻底评估狗的心脏肿块;这些视图包括右胸骨旁短轴和长轴视图、左心尖视图,以及最重要的左颅骨旁长轴视图,该视图提供了右心房的最佳图像。在研究期间使用了三台超声波机(机器A,a,1985年至1991年;机器B,b,1991年至2000年;机器C,c,c,2000年至2006年)。心包积液原因的超声心动图特征包括右心耳质量、心脏基底质量、心包质量、心脏质量的其他位置(如果适用)或无肿块证据的类别。

Medical records review — Multiple echocardiographic views were obtained to thoroughly evaluate dogs for cardiac masses; those views included right parasternal short-axis and long-axis views, left apical views, and, most importantly, the left cranial parasternal long-axis view that provides the best images of the right atrium. Three ultrasound machines were used during the study period (machine A,a 1985 through 1991; machine B,b 1991 through 2000; and machine C,c 2000 through 2006). Echocardiographic characterization of the cause of the pericardial effusion included the categories right atrial-auricular mass, heart base mass, pericardial mass, other location of a cardiac mass (if applicable), or no evidence of a mass.


敏感性和特异性是根据第一次超声心动图检查计算的,用于超声心动图检测心脏肿块与无肿块,检测心脏基础质量与其他原因,以及检测右心房质量与其他原因。为了评估超声心动图在系列检查期间的诊断能力是否有所提高,还通过使用多次检查的狗的最终超声心动图检查结果来计算超声心动图检测心脏肿块与其他原因的敏感性和特异性。使用二维超声心动图对心包填塞证据进行主观评估,当右心房、右心室或两者兼有心包积液舒张衰竭时,诊断为心包填塞。

Sensitivity and specificity were calculated on the basis of the first echocardiographic examination for echocardiographic detection of a cardiac mass versus no mass, for detection of a heart base mass versus other causes, and for detection of a right atrial mass versus other causes. To assess whether there was improved diagnostic capability of echocardiography during serial examinations, sensitivity and specificity of echocardiography for detection of a cardiac mass versus another cause were also calculated by use of findings from the final echocardiographic examination in dogs examined multiple times. Subjective evaluation for evidence of cardiac tamponade was performed by use of 2-D echocardiography, and cardiac tamponade was diagnosed when there was diastolic collapse of the right atrium, right ventricle, or both in addition to pericardial effusion.


记录了临床特征,包括信号和体重。对所有狗都进行了胸 X 光片检查,主观特征是是否存在球状心脏轮廓、是否存在心脏占位效应以及是否存在转移性肺部疾病。右心衰竭被识别并表征为腹水、胸腔积液或两者兼而有之,并通过使用超声检查确诊。标准做法包括在体格检查中检测到心律失常时进行心电图检查。对所有狗进行的临床病理学测试包括全血细胞计数和血清生化分析。在一些狗中分析了心包液,包括细胞学评估以及可能的需氧和厌氧微生物培养。

Clinical characteristics were recorded, which included signalment and body weight. Thoracic radiographs were obtained for all dogs and were characterized subjectively by the presence or absence of a globoid cardiac silhouette, presence or absence of a cardiac mass effect, and presence or absence of metastatic pulmonary disease. Right-sided heart failure was identified and characterized as ascites, pleural effusion, or both and was confirmed by use of ultrasonography. Standard practice included obtaining an ECG when there was an arrhythmia detected during physical examination. Clinicopathologic tests performed on all dogs included a CBC and serum biochemical analysis. Pericardial fluid was analyzed in some dogs, which included cytologic evaluation and possibly aerobic and anaerobic microbial culture.


统计分析:采用Fisher精确检验比较肿瘤性病因的转移率,比较肿瘤性病因和非肿瘤性病因的双腔积液、胸腔积液或腹水的发生率。显著性定义为 P < 0.05 的值。还通过审查医疗记录获得了生存数据,尽管许多狗在后续监测中丢失了。在后续监测中丢失的狗在最后一次医疗进入的日期被审查。针对心包积液的最常见原因生成了 Kaplan-Meier 曲线。使用 Tarone-Ware 秩检验确定显著性。中位生存时间是通过使用非参数生存分析计算的。学生 t 检验用于比较患有心包积液的肿瘤性和非肿瘤性原因的狗的年龄。在接受完全尸检的狗中计算转移率。

Statistical analysis — The Fisher exact test was used to compare the rate of metastasis for neoplastic causes and to compare the rates of bicavitary effusion, pleural effusion, or ascites between neoplastic and nonneoplastic causes. Significance was defined as values of P < 0.05. Survival data were also obtained from review of medical records, although many dogs were lost to follow-up monitoring. Dogs that were lost to follow-up monitoring were censored at the date of the last medical entry. Kaplan-Meier curves were generated for the most common causes of pericardial effusion. The Tarone-Ware rank test was used to determine significance. Median survival times were calculated by use of nonparametric survival analysis. Student t tests were used to compare ages of dogs with neoplastic and nonneoplastic causes of pericardial effusion. Metastatic rate was calculated in dogs that underwent complete necropsies.


4 结论

对医疗记录的审查导致将 107 只狗纳入研究。其中,48 人接受了心包切除术(开胸手术),44 人接受了尸检,15 人接受了两种手术。手术或尸检用于识别 66 只有心脏肿块的狗和 41 只没有肿块的狗。肿块位置包括 38 个右心房肿块、23 个心脏基底肿块、2 个并发右心房和心脏基底肿块、2 个心包肿块和 1 个右心室肿块(表 1)。超声心动图发现 66 只狗中有 53 只患有心脏肿块,包括 32 只患有右心房肿块的狗和 17 只患有心脏基底肿块的狗。超声心动图检测心脏肿块的敏感性和特异性分别为 80% 和 100%,超声心动图在区分右心房肿块与所有其他原因(分别为 84% 和 100%)或区分心脏基础肿块与所有其他原因(分别为 74% 和 98%)方面具有相同的敏感性和特异性。

Review of medical records resulted in the inclusion of 107 dogs in the study. Of these, 48 underwent pericardectomy (via thoracotomy), 44 underwent necropsy, and 15 underwent both procedures. Surgery or necropsy was used to identify 66 dogs with a cardiac mass and 41 dogs without a mass. Location of masses included 38 right atrial masses, 23 heart base masses, 2 concurrent right atrial and heart base masses, 2 pericardial masses, and 1 right ventricular mass (Table 1). Echocardiography identified 53 of 66 dogs with cardiac masses, including 32 of 38 dogs with right atrial masses and 17 of 23 dogs with heart base masses. Sensitivity and specificity of echocardiography for detection of a cardiac mass were 80% and 100%, respectively, and echocardiography had equal sensitivity and specificity for distinguishing right atrial masses from all other causes (84% and 100%, respectively) or for distinguishing heart base masses from all other causes (74% and 98%, respectively).

ECG.Table1.jpg


19 只狗进行了 1 >超声心动图评估,其中 11 只有心脏肿块的狗和 8 只没有心脏肿块的狗。在 12 只使用超声心动图在初次检查时未识别肿块的狗中,只有 4 只狗重复进行了超声心动图检查。对这 4 只狗重复超声心动图发现心脏肿块,将超声心动图检测心脏肿块的灵敏度提高到 88%。从初始超声心动图到重复超声心动图的间隔范围为 2 天至 7 个月(中位数为 75 天)。在初次超声心动图检查期间未发现的 12 只肿块的狗中,有 8 只在初次超声心动图检查时有少量心包积液。

Nineteen dogs had > 1 echocardiographic evaluation, including 11 dogs with cardiac masses and 8 dogs without cardiac masses. Of the 12 dogs in which use of echocardiography did not identify masses on initial examination, only 4 dogs had repeat echocardiography. Repeat echocardiography on those 4 dogs identified cardiac masses, which increased the sensitivity of echocardiography for detection of a cardiac mass to 88%. The interval from the initial echocardiography to repeat echocardiography ranged from 2 days to 7 months (median, 75 days). Eight of 12 dogs with masses that were not identified during the initial echocardiography had a small volume of pericardial effusion at the time of the initial echocardiographic examination.


确定了心包积液的具体病因。血管肉瘤是心包积液的最常见原因 (n = 36 只),其次是特发性心包炎 (21)、间皮瘤 (15)、鹅掌瘤 (9)、甲状腺腺癌 (6)、感染性心包炎 (5)、淋巴瘤 (3)、肉瘤 (2)、癌 (1)、继发于严重二尖瓣反流的左心房破裂 (1)、无菌异物 (1) 和肉芽肿 (1)。未对接受心包切除术手术(开胸术)的 6 只心脏基底肿块犬进行活检标本和组织学评估。一只狗并发患有右心房血管肉瘤和神经内分泌心脏基底肿块。

Specific causes of pericardial effusion were determined. Hemangiosarcoma was the most common cause of pericardial effusion (n = 36 dogs), followed by idiopathic pericarditis (21), mesothelioma (15), chemodectoma (9), thyroid gland adenocarcinoma (6), infective pericarditis (5), lymphoma (3), sarcoma (2), carcinomatosis (1), ruptured left atrium secondary to severe mitral valve regurgitation (1), sterile foreign body (1), and granuloma (1). Biopsy specimens and histologic evaluation were not performed for 6 dogs with heart base masses that underwent surgery (thoracotomy) for pericardectomy. One dog had a concurrent right atrial hemangiosarcoma and a neuroendocrine heart base mass.


肿瘤是大多数 (76/107 [71%]) 狗心包积液的原因。15 只患有间皮瘤的狗中有 5 只患有离散的心脏肿块,最常见的是心脏底部 (4/5),很少是右心房 (1/5)。大多数 (35/40 [88%]) 右心房肿块为血管肉瘤,其次是神经内分泌肿瘤、甲状腺腺癌、间皮瘤、淋巴瘤和肉瘤各 1 例 (3%)。心脏基底肿块最常见的是神经内分泌肿瘤(9/23 [39.1%]狗),其次是甲状腺腺癌(6/23 [26.1%])、间皮瘤(5/23 [21.7%])和血管肉瘤(3/23 [13%])。间皮瘤心脏基底肿块在超声心动图上表现为离散肿块。未分化肉瘤是右心室肿块的病因。5 只狗中有 3 只的感染性心包炎是由继发性细菌感染的异物(即狐尾锥)引起的。

Neoplasia was the cause of pericardial effusion in a majority (76/107 [71%]) of dogs. Five of 15 dogs with mesothelioma had discrete cardiac masses, most often of the heart base (4/5) and rarely of the right atrium (1/5). A majority (35/40 [88%]) of right atrial masses were hemangiosarcoma, followed by 1 (3%) each of neuroendocrine tumor, thyroid gland adenocarcinoma, mesothelioma, lymphoma, and sarcoma. Heart base masses were most often neuroendocrine tumors (9/23 [39.1%] dogs), followed by thyroid gland adenocarcinoma (6/23 [26.1%]), mesothelioma (5/23 [21.7%]), and hemangiosarcoma (3/23 [13%]). Mesothelioma heart base masses were apparent as discrete masses on echocardiography. An undifferentiated sarcoma was the cause of the right ventricular mass. Infective pericarditis in 3 of 5 dogs was caused by foreign bodies (ie, foxtail awns) with secondary bacterial infections.


对 59 只狗进行了完全尸检(仅尸检 44 次,心包切除术和尸检 15 次)。患有血管肉瘤(19/28 [67.9%])、间皮瘤(5/9 [55.6%])、甲状腺腺癌(2/3 [66.7%])或化疗瘤(4/6 [66.7%])的狗之间的转移率无显著差异(P = 1.00)。28 只患有心源性血管肉瘤的狗中有 8 只 (28.6%) 也患有脾脏血管肉瘤。所有患有淋巴瘤的狗都有转移性疾病。所有肿瘤犬最常见的转移部位是肺(18/59 [30.5%])。在患有心脏血管肉瘤的狗中,最常见的转移部位包括肺 (12/28 [42.9%])、脾脏 (8/28 [28.6%])、肝脏 (8/28 [28.6%]) 和肾脏 (4/28 [14.3%])。患有间皮瘤的狗最常见的转移部位包括胸内淋巴结 (6/9 [66.7%])、肺 (2/9 [22.2%]) 和胸膜 (2/9 [22.2%])。在患有神经内分泌肿瘤的狗中,最常见的转移部位是肺(3/6 [50%]),其次是脾脏(1/6 [16.7%])和肝脏(1/6 [16.7%])。患有甲状腺腺癌的狗最常见的转移部位是心包(2/3 [66.7%]),其次是肺转移(1/3 [33.3%])和心肌转移(1/3 [33.3%])和经腔血转移(1/3 [33.3%])。

Complete necropsy was performed on 59 dogs (44 necropsy alone and 15 pericardectomy and necropsy). The metastatic rate did not differ significantly (P = 1.00 for all comparisons) between dogs with hemangiosarcoma (19/28 [67.9%]), mesothelioma (5/9 [55.6%]), thyroid gland adenocarcinoma (2/3 [66.7%]), or chemodectoma (4/6 [66.7%]). Eight of 28 (28.6%) dogs with cardiac hemangiosarcoma also had splenic hemangiosarcoma. All dogs with lymphoma had metastatic disease. The most common site of metastasis for all neoplastic dogs was the lungs (18/59 [30.5%]). In dogs with cardiac hemangiosarcoma, the most common sites of metastasis included the lungs (12/28 [42.9%]), spleen (8/28 [28.6%]), liver (8/28 [28.6%]), and kidneys (4/28 [14.3%]). The most common sites of metastasis in dogs with mesothelioma included the intrathoracic lymph nodes (6/9 [66.7%]), lungs (2/9 [22.2%]), and pleurae (2/9 [22.2%]). In dogs with neuroendocrine tumors, the most common site of metastasis was the lungs (3/6 [50%]), followed by the spleen (1/6 [16.7%]) and liver (1/6 [16.7%]). The most common site of metastasis for dogs with thyroid gland adenocarcinoma was the pericardium (2/3 [66.7%]), followed by metastasis to the lungs (1/3 [33.3%]) and myocardium (1/3 [33.3%]) and transcoelomic metastasis (1/3 [33.3%]).


大多数患有心包积液的狗是大型犬;体重范围为 3.6 至 73.0 公斤(7.9 至 160.6 磅),中位数为 31.5 公斤(69.3 磅)。最常见的品种包括金毛猎犬(20/107 [18.7%])、拉布拉多猎犬(16/107 [14.9%])和德国牧羊犬(5/107 [4.7%])。有心脏肿块的狗(平均 9.7 岁)比没有肿块的狗(平均 7.9 岁)明显 (P = 0.006)。

Most dogs with pericardial effusion were largebreed dogs; body weight ranged from 3.6 to 73.0 kg (7.9 to 160.6 lb), with a median of 31.5 kg (69.3 lb). The most common breeds included Golden Retriever (20/107 [18.7%] dogs), Labrador Retriever (16/107 [14.9%]), and German Shepherd Dog (5/107 [4.7%]). Dogs with cardiac masses were significantly (P = 0.006) older (mean, 9.7 years) than dogs without masses (mean, 7.9 years).


67 只 (62.6%) 心包积液的狗有右心衰竭的证据。大多数狗 (36/107 [33.6%]) 并发胸腔积液和腹水,少数狗出现孤立性腹水 (17/107 [15.9%]) 或胸腔积液 (14/107 [13.1%])。双腔积液(P=1.00)、胸腔积液(P=0.84)或腹水(P=0.93)的肿瘤性和非肿瘤性病因之间没有差异。根据 107 只狗中有 42 只 (39%) 的超声心动图结果,主观怀疑心包填塞。在检查胸 X 光片时,107 只狗中有 56 只 (52.3%) 发现了球形心脏,这对检测心包积液的敏感性较差。在尸检或心包切除术中确认肺转移的 21 只狗中有 7 只 (33.3%) 在检查胸 X 线片时才发现肺转移。在对 63 只有肿块的狗中的 10 只进行胸 X 线片检查时,怀疑右心房或心脏基底肿块,特异性为 100%。

Sixty-seven (62.6%) dogs with pericardial effusion had evidence of right-sided heart failure. Most dogs (36/107 [33.6%]) had concurrent pleural effusion and ascites, with fewer dogs with isolated ascites (17/107 [15.9%]) or pleural effusion (14/107 [13.1%]). There was no difference between neoplastic and nonneoplastic causes for bicavitary effusion (P = 1.00), pleural effusion (P = 0.84), or ascites (P = 0.93). Cardiac tamponade was subjectively suspected on the basis of results of echocardiography in 42 of 107 (39%) dogs. A globoid-shaped heart was identified in 56 of 107 (52.3%) dogs during examination of thoracic radiographs, which yielded a poor sensitivity for detection of pericardial effusion. Pulmonary metastases were only identified during examination of thoracic radiographs in 7 of 21 (33.3%) dogs with confirmed pulmonary metastases during necropsy or pericardectomy. There was a suspicion of a right atrial or heart base mass during examination of thoracic radiographs in 10 of 63 dogs with masses, with a specificity of 100%.


最常见的心电图异常包括电交替(30/107 [28.0%]犬)、窦性心动过速(30/107 [28.0%])、QRS波群阻尼(即< 1 mV;26/107 [24.3%])和室性心律失常(14/107 [13.1%])。其他较少见的异常包括室上性心动过速 (3/107 [2.8%] 犬)、心房早衰复合体 (2/107 [1.9%])、心房颤动 (2/107 [1.9%])、ST 段增加 (2/107 [1.9%])、高级别二度房室传导阻滞 (1/107 [0.9%]) 和右束支传导阻滞 (1/107 [0.9%])。

The most common ECG abnormalities included electrical alternans (30/107 [28.0%] dogs), sinus tachycardia (30/107 [28.0%]), dampened QRS complexes (ie, < 1 mV; 26/107 [24.3%]), and ventricular arrhythmia (14/107 [13.1%]). Other less common abnormalities included supraventricular tachycardia (3/107 [2.8%] dogs), atrial premature complexes (2/107 [1.9%]), atrial fibrillation (2/107 [1.9%]), increase in ST segment (2/107 [1.9%]), high-grade second-degree atrioventricular block (1/107 [0.9%]), and right bundle-branch block (1/107 [0.9%]).


在 107 只狗中分析了 47 只心包积液。液体分析确定了 47 只狗中有 6 只 (12.8%) 心包积液的原因,其中包括 5 只患有感染性心包炎的狗和 1 只患有淋巴瘤的狗。大多数心包积液分为出血性积液(40/47 [85%]犬),其次是化脓性炎症(6/47 [12.8%])、化脓性肉芽肿性炎症(4/47 [8.5%])、改良渗出液(2/47 [4.3%])和乳糜性积液(1/47 [2.1%])。47 只狗中有 25 只 (53.2%) 发现了间皮反应性。在 1 只患有淋巴瘤、间皮瘤和特发性心包炎的狗中发现了肿瘤细胞。

Pericardial effusion was analyzed in 47 of 107 dogs. Fluid analysis identified the cause of the pericardial effusion in 6 of 47 (12.8%) dogs, which included 5 dogs with infective pericarditis and 1 dog with lymphoma. Most pericardial effusion was classified as hemorrhagic fluid (40/47 [85%] dogs), followed by suppurative inflammation (6/47 [12.8%]), pyogranulomatous inflammation (4/47 [8.5%]), a modified transudate (2/47 [4.3%]), and chylous effusion (1/47 [2.1%]). Mesothelial reactivity was identified in 25 of 47 (53.2%) dogs. Neoplastic cells were identified in 1 dog each with lymphoma, mesothelioma, and idiopathic pericarditis.


细胞学分析在患有球孢子菌病的狗中鉴定出球孢子菌属生物。47 只狗中有 4 只 (8.5%) 的细菌培养结果呈阳性,包括拟杆菌属、放线菌属、犬链球菌各 1 例,以及由巴斯德菌属、消化链球菌属和拟杆菌属组成的混合感染。

Cytologic analysis identified Coccidioides organisms in a dog with coccidiodomycosis. Four of 47 (8.5%) dogs had positive results for bacterial culture, including 1 each of Bacteroides spp, Actinomyces spp, Streptococcus canis, and a mixed infection consisting of Pasteurella spp, Peptostreptococcus spp, and Bacteroides spp.


在一些病例中,诊断结果不一致是显而易见的。根据心包液的细胞学分析,一只患有特发性心包炎的狗被归类为间皮瘤。一只患有化疗瘤的狗有脓性心包积液。放线菌属是从患有组织学证实的间皮瘤的狗中培养的。心包组织学检查错误地识别出 1 只患有间皮瘤的狗,该犬患有特发性心包炎和心外膜炎,在对第二次心包切除术期间获得的样本进行组织学检查时以及此后不久的尸检中发现。

Discordant diagnostic results were evident in several instances. One dog with idiopathic pericarditis was classified with a mesothelioma on the basis of cytologic analysis of pericardial fluid. One dog with a chemodectoma had purulent pericardial effusion. Actinomyces spp were cultured from a dog with histologically confirmed mesothelioma. Histologic examination of the pericardium incorrectly identified 1 dog with mesothelioma that had idiopathic pericarditis and epicarditis identified 2 years later during histologic examination of samples obtained during a second pericardectomy as well as during necropsy shortly thereafter.


血液学和血清生化分析结果可用于 90 只心包积液犬的审查。贫血是检测到的最常见的异常(23/90 [25.6%] 犬)。所有狗的贫血均为轻度(PCV,30%-37%)、色素正常、细胞正常且不可再生,但 2 只狗的 PCV < 30% 除外。在任何狗中均未检测到形态学红细胞异常。贫血最常见于患有血管肉瘤 (n = 8 只狗)、心包炎 (6) 和间皮瘤 (4) 的狗。90 只狗中有 21 只 (23.3%) 检测到肝酶活性增加;这些增长都被认为是温和的。在患有血管肉瘤 (n = 9)、化疗瘤 (5)、心包炎 (4)、不明确的心脏基底肿块 (2) 和甲状腺腺癌 (1) 的狗中检测到肝酶的高活性。血小板减少症(< 200,000 个血小板/μL)是第三大最常见的实验室异常,在 90 只狗中有 12 只 (13.3%) 发现。在患有血管肉瘤 (n = 6)、心包炎 (4) 和淋巴肉瘤 (2) 的狗中检测到血小板减少症。其他不常见的异常包括轻度氮质血症(4/90 只狗);凝血酶原时间、部分凝血活酶时间或两者轻微延长 (3);轻度高钙血症(3);和轻度高钾血症 (2)。在具有 3 种最常检测到的血液学或生化异常(贫血、肝酶活性高或血小板减少症)的狗中,心包积液的最常见原因是血管肉瘤。

Results of hematologic and serum biochemical analysis were available for review in 90 dogs with pericardial effusion. Anemia was the most common abnormality detected (23/90 [25.6%] dogs). Anemia was mild (PCV, 30% to 37%), normochromic, normocytic, and nonregenerative in all dogs, except for 2 in which the PCV was < 30%. Morphological RBC abnormalities were not detected in any of the dogs. Anemia was most commonly detected in dogs with hemangiosarcoma (n = 8 dogs), pericarditis (6), and mesothelioma (4). Increases in activities of liver enzymes were detected in 21 of 90 (23.3%) dogs; those increases were all considered mild. High activities of liver enzymes were detected in dogs with hemangiosarcoma (n = 9), chemodectoma (5), pericarditis (4), nondefined heart base masses (2), and thyroid gland adenocarcinoma (1). Thrombocytopenia (< 200,000 platelets/μL) was the third most common laboratory abnormality evident and was found in 12 of 90 (13.3%) dogs. Thrombocytopenia was detected in dogs with hemangiosarcoma (n = 6), pericarditis (4), and lymphosarcoma (2). Other uncommon abnormalities included mild azotemia (4/90 dogs); slight prolongation of the prothrombin time, partial thromboplastin time, or both (3); mild hypercalcemia (3); and mild hyperkalemia (2). In dogs with the 3 most commonly detected hematologic or biochemical abnormalities (anemia, high activities of liver enzymes, or thrombocytopenia), the most common cause of pericardial effusion was hemangiosarcoma.


通过将各组分为 2 个时间段(1985 年至 1995 年的 42 只狗和 1996 年至 2006 年的 65 只狗)来评估心包积液原因分布的变化。所有 5 只患有感染性心包炎的狗都在第一个时间段内被发现,而 42 只 (14.3%) 患有特发性心包炎的狗中有 6 只在第一个时间段内被发现,65 只 (23.1%) 犬中有 15 只(23.1%)在第二个时间段内被发现。患有间皮瘤的狗的比例从第一个时间段的 3/42 只狗 (7.1%) 增加到第二个时间段的 12/65 狗 (18.5%)。相比之下,第一个时间段的 42 只狗中有 6 只 (14.3%) 患有化疗瘤,而第二个时间段的 65 只狗中只有 3 只 (4.6%)。在两个时间段之间,所有其他原因的比例相似。在 2 因素数据列联表上使用 Fisher 精确检验显示,间皮瘤 (P = 0.09)、化疗瘤 (P = 0.15) 或特发性心包炎 (P = 0.32) 的诊断频率在两个时间段之间没有显着差异。为了评估由于超声机的时间和空间分辨率的提高,在后期心脏肿块的诊断是否有所改善,比较了两个时间段之间使用超声心动图无法识别肿块的狗的数量。早期(5/42 [11.9%] 犬未发现肿块)与后期(7/65 [10.8%]犬未发现肿块)的百分比没有差异。

Changes in distribution of causes of pericardial effusion were evaluated by separating the groups into 2 time periods (42 dogs from 1985 through 1995 and 65 dogs from 1996 through 2006). All 5 dogs with infective pericarditis were identified in the first time period, whereas 6 of 42 (14.3%) dogs with idiopathic pericarditis were identified in the first time period and 15 of 65 (23.1%) dogs with idiopathic pericarditis were identified in the second time period. The proportion of dogs with mesothelioma increased from 3 of 42 (7.1%) dogs in the first time period to 12 of 65 (18.5%) dogs in the second time period. In contrast, 6 of 42 (14.3%) dogs in the first time period had chemodectomas, compared with only 3 of 65 (4.6%) dogs in the second time period. The proportions for all other causes were similar between the 2 time periods. Use of the Fisher exact test on a 2-way data contingency table revealed no significant difference in frequency of diagnosis of mesothelioma (P = 0.09), chemodectoma (P = 0.15), or idiopathic pericarditis (P = 0.32) between the 2 time periods. To assess whether there was improvement in diagnosis of cardiac masses in the later time period as a result of improvements in temporal and spatial resolution of ultrasound machines, the number of dogs in which use of echocardiography did not identify the mass was compared between the 2 time periods. There was no difference in the percentage of masses that were not identified between the early period (masses not identified in 5/42 [11.9%] dogs), compared with the percentage for the later period (masses not identified in 7/65 [10.8%] dogs).


根据超声心动图分类,无心脏肿块的狗的寿命(P < 0.001)明显长(中位生存时间,10.10个月)比有心脏肿块超声心动图证据的狗(中位生存时间,0.53个月;图1)。通过使用超声心动图诊断为心脏基础肿块的狗<寿命显着长(P 0.001)(中位生存时间,5.17个月)比使用超声心动图诊断为右心房肿块的狗(中位生存时间,0.03个月)。所有记录在案的死亡都是心包积液的特定原因的结果,而不是其他全身性疾病的结果。关于心包积液的具体原因,非肿瘤性病因的狗的寿命(P < 0.001)明显长于肿瘤病因的狗(中位生存时间,0.63个月),比肿瘤病因的狗(中位生存时间,0.63个月)长(P 0.001)。患有血管肉瘤的狗的中位生存时间(0.07个月)明显(P < 0.001)比所有其他肿瘤原因的狗(5.17个月)短。患有间皮瘤的狗的中位生存时间(6.50 个月)与患有心脏基底肿块的狗的中位生存时间(P = 0.51)没有显着差异,包括趋化瘤、异位甲状腺组织或非特异性原因(5.17 个月)。

On the basis of echocardiographic classification, dogs with no cardiac mass lived significantly (P < 0.001) longer (median survival time, 10.10 months) than did dogs with echocardiographic evidence of a cardiac mass (median survival time, 0.53 months; Figure 1). Dogs with a heart base mass diagnosed by use of echocardiography lived significantly (P < 0.001) longer (median survival time, 5.17 months) than did dogs with a right atrial mass diagnosed by use of echocardiography (median survival time, 0.03 months). All deaths recorded were the result of the specific cause of the pericardial effusion and not the result of other systemic disease. Regarding specific causes of pericardial effusion, dogs with nonneoplastic causes lived significantly (P < 0.001) longer (median survival time, 24.83 months) than did dogs with neoplastic causes (median survival time, 0.63 months). Dogs with hemangiosarcoma had a significantly (P < 0.001) shorter median survival time (0.07 months) than did dogs with all other neoplastic causes combined (5.17 months). Median survival time of dogs with mesothelioma (6.50 months) did not differ significantly (P = 0.51) from that of dogs with heart base masses, which included chemodectoma, ectopic thyroid gland tissue, or nonspecific causes (5.17 months).

ECG.Fig1.jpg

图 1:由各种原因引起的心包积液狗的 Kaplan-Meier 生存曲线。A—有心包积液且无心脏肿块超声心动图证据的狗(方块)比有心脏肿块超声心动图证据的狗(圆圈)存活时间明显长(P < 0.001)。B—通过使用超声心动图(方块)诊断为心脏基础肿块的狗比使用超声心动图诊断为右心房肿块的狗(圆圈)存活时间明显长 (P = 0.002)。C—非肿瘤性心包积液原因的狗(根据组织学检查确定;方块)比有肿瘤性心包积液原因的狗存活时间明显长(P < 0.001)(圆圈)。D—患有血管肉瘤的狗(根据组织学检查确定;圆圈)的中位生存时间明显(P < 0.001)比所有其他肿瘤原因的狗加起来(平方)短。请注意,x 轴的刻度因面板而异。

Figure 1: Kaplan-Meier survival curves for dogs with pericardial effusion attributable to various causes. A—Dogs with pericardial effusion and no echocardiographic evidence of a cardiac mass (squares) survived significantly (P < 0.001) longer than did dogs with echocardiographic evidence of a cardiac mass (circles). B—Dogs with a heart base mass diagnosed by use of echocardiography (squares) survived significantly (P = 0.002) longer than did dogs with a right atrial mass diagnosed by use of echocardiography (circles). C—Dogs with a nonneoplastic cause of pericardial effusion (as determined on the basis of histologic examination; squares) survived significantly (P < 0.001) longer than did dogs with a neoplastic cause of pericardial effusion (circles). D—Dogs with hemangiosarcoma (as determined on the basis of histologic examination; circles) had a significantly (P < 0.001) shorter median survival time than did dogs with all other neoplastic causes combined (squares). Notice that the scale for the x-axis differs among panels.


5 讨论

在此报告的研究中,由董事会认证的兽医心脏病专家或受监督的心脏病学住院医师进行的超声心动图对诊断心包积液狗的心脏肿块具有高敏感性 (82%) 和特异性 (100%)。超声心动图在鉴别心脏基底肿块与心包积液的其他原因以及右心房肿块与其他心包积液原因方面也具有很高的敏感性和特异性。重复超声心动图检查可将检测心脏肿块的敏感性从 80% 提高到 88%。在使用超声心动图未识别肿块的狗中,所有重复超声心动图检查的狗都检测到肿块 (n = 4)。不幸的是,许多狗没有进行重复的超声心动图检查,这可能有助于在 12 只狗中检测出肿块,其中肿块未通过超声心动图识别。使用超声心动图未检测到的大多数肿块发生在有少量心包积液的狗中。

In the study reported here, echocardiography performed by a board-certified veterinary cardiologist or supervised cardiology resident had high sensitivity (82%) and specificity (100%) for diagnosis of a cardiac mass in dogs with pericardial effusion. Echocardiography also had high sensitivity and specificity for differentiating heart base masses from other causes of pericardial effusion and right atrial masses from other causes of pericardial effusion. Repeat echocardiographic examinations increased the sensitivity for detection of cardiac masses from 80% to 88%. Of the dogs in which use of echocardiography did not identify a mass, masses were detected in all dogs that had repeat echocardiographic examinations (n = 4). Unfortunately, many dogs did not have repeat echocardiographic examinations, which could have aided in detection of masses in the 12 dogs in which a mass was not echocardiographically identified. Most masses that were not detected by use of echocardiography were in dogs with a small volume of pericardial effusion.


准确诊断心脏肿块并确定心脏肿块的位置可以提供重要的预后信息,在确定治疗计划时很有用。在这里报告的研究中,有心脏肿块超声心动图证据的狗不能像使用超声心动图检测到没有肿块的狗那样存活。更重要的是,无论组织学特征如何,超声心动图诊断为右心房肿块的狗都不能像有心脏基础肿块超声心动图证据的狗那样存活。区分右心房肿块和心脏基底肿块很重要,因为具有心脏基底肿块的狗可能会从部分心包切除术中受益,以改善生存时间.2,7,8 关于心包积液的具体原因,血管肉瘤的预后最严重,生存时间比其他肿瘤疾病的生存时间短。

Accurate diagnosis of a cardiac mass and defining the location of the cardiac mass can yield important prognostic information and be useful when determining the therapeutic plan. In the study reported here, dogs with echocardiographic evidence of a cardiac mass did not survive as long as dogs without a mass detected by use of echocardiography. More importantly, dogs with an echocardiographic diagnosis of a right atrial mass did not survive as long as dogs with echocardiographic evidence of a heart base mass, irrespective of histologic characterization. It is important to distinguish right atrial masses from heart base masses because dogs with heart base masses may benefit from partial pericardectomy to improve survival time.2,7,8 Regarding specific causes of pericardial effusion, hemangiosarcoma conferred the gravest prognosis, with a shorter survival time than that for other neoplastic conditions.


本研究中心包积液最常见的 2 个原因是血管肉瘤 (36/107 [33.6%] 狗) 和特发性心包炎 (21/107 [19.6%]),这与其他报告的结果一致.1,4 间皮瘤也是该系列犬心包积液的重要原因 (15/107 [14%]),比化疗瘤 (9/107 [8.4%]) 或甲状腺腺癌 (6/107 [5.6%]) 的比例更常见。相比之下,研究人员在 1984 年的一项早期研究4 中没有发现任何由间皮瘤引起的心包积液的狗,并报告说 12% 的病例是由化疗瘤引起的。令人惊讶的是,15 种间皮瘤中有 5 种引起离散的心脏肿块,大多数 (4/5) 是心脏基底肿块,其余 1 种是右心房肿块。另一个出乎意料的发现是,在心包液的细胞学分析过程中,根据间皮细胞形态异常,将感染性心包炎误诊为间皮瘤的频率(1 只狗)很少,与早期研究的结果相比12,研究人员发现 13% 的非肿瘤病例被误报为肿瘤。与其他报告的结果一致,4,7,8 我们研究的狗中心脏基底肿瘤的最常见原因是化疗瘤 (9/23 [39.1%]),其次是甲状腺腺癌 (6/23 [26.1%])。此外,23 例心脏基底肿块中有 3 例 (13%) 由血管肉瘤引起,与心脏基底肿块的典型病因相比,血管肉瘤的预后更严重。

The 2 most common causes of pericardial effusion in this study were hemangiosarcoma (36/107 [33.6%] dogs) and idiopathic pericarditis (21/107 [19.6%]), which is consistent with results in other reports.1,4 Mesothelioma was also an important cause of pericardial effusion in this series of dogs (15/107 [14%]) and was more common than the proportion for chemodectomas (9/107 [8.4%]) or thyroid gland adenocarcinomas (6/107 [5.6%]). In contrast, investigators in an earlier study4 in 1984 did not detect any dogs with pericardial effusion caused by mesothelioma and reported that 12% of cases were caused by chemodectoma. Surprisingly, 5 of 15 mesotheliomas caused discrete cardiac masses, with the majority (4/5) being heart base masses and the remaining 1 being a right atrial mass. Another unexpected finding was the infrequency (1 dog) of misdiagnosis of infective pericarditis as mesothelioma on the basis on abnormal mesothelial cell morphology during cytologic analysis of pericardial fluid, compared with results in an earlier study12 in which investigators found that 13% of nonneoplastic cases were falsely reported as neoplastic. Consistent with results of other reports,4,7,8 the most common cause of heart base tumors in the dogs of our study was chemodectoma (9/23 [39.1%]), which was followed by thyroid gland adenocarcinoma (6/23 [26.1%]). In addition, 3 of 23 (13%) heart base masses were caused by hemangiosarcoma, which would confer a graver prognosis than for the typical causes of heart base masses.


与另一份报告1的发现相比,各种肿瘤病因(血管肉瘤、间皮瘤、化学感受器瘤和甲状腺腺癌)的转移率没有显着差异。本文报告的研究中,化学感受器瘤 (chemodectoma)、甲状腺腺癌和间皮瘤的转移率相当高(50%-66%)。在所有肿瘤病因中,肺部是最常见的转移部位。胸部 X 线摄影期间肺转移的检测灵敏度低,因为 21 只 (33.3%) 有肺转移的狗中只有 7 只是通过使用 X 线摄影发现的。令人惊讶的是,双腔积液、胸腔积液或腹水的发生率在肿瘤性病因和特发性心包炎之间没有差异。一种可能的解释是,心包积液的肿瘤性和非肿瘤性原因都常导致心包填塞和随后的右心衰竭。

In contrast to findings in another report,1 the metastatic rate of the various neoplastic causes (hemangiosarcoma, mesothelioma, chemodectoma, and thyroid gland adenocarcinoma) did not differ significantly. Metastatic rates for chemodectomas, thyroid gland adenocarcinomas, and mesotheliomas were quite high (50% to 66%) in the study reported here. The lungs were the most common site for metastasis of all neoplastic causes combined. Detection of pulmonary metastases during thoracic radiography had low sensitivity because only 7 of 21 (33.3%) dogs with pulmonary metastases were identified by use of radiography. It was surprising that the rate of bicavitary effusion, pleural effusion, or ascites did not differ between neoplastic causes and idiopathic pericarditis. A possible explanation is that both neoplastic and nonneoplastic causes of pericardial effusion often lead to cardiac tamponade and subsequent right-sided heart failure.


大多数不一致的诊断试验结果用于区分特发性心包炎和间皮瘤。在对大约一半的狗的心包积液进行细胞学分析时,诊断出间皮细胞反应性,这不能区分特发性心包炎和间皮瘤。尽管心包组织学检查是目前用于鉴别特发性心包炎和间皮瘤的标准,但该技术的诊断也可能存在差异(3 只狗被错误识别)。使用特殊的免疫组织化学染色可以帮助临床医生和研究人员更好地区分这两种疾病。

Most of the discordant diagnostic test results were for the differentiation of idiopathic pericarditis from mesothelioma. Mesothelial cell reactivity was diagnosed during cytologic analysis of pericardial effusion in approximately half of all dogs, which does not discriminate between idiopathic pericarditis and mesothelioma. Although histologic examination of pericardium is the current standard used for differentiation of idiopathic pericarditis from mesothelioma, there can also be discrepancies in diagnosis with this technique (3 dogs were incorrectly identified). Use of special immunohistochemical stains may help clinicians and researchers better discriminate between these 2 diseases.


研究的局限性包括回顾性设计,而回顾性设计具有固有的局限性。少数狗使用超声心动图无法识别心脏肿块,在超声心动图检查后短时间内没有进行心包切除术或尸检,也没有对肿块进行重复的超声心动图评估。因此,超声心动图检测肿块的敏感性可能高于本文报告的研究中反映的灵敏度。鉴于该研究的回顾性,许多狗在后续监测中丢失,并在 Kaplan-Meier 生存分析中被视为删失变量。安乐死可能会混淆对存活率的评估,因为主人对继续治疗预后不良的心脏肿块狗的承诺可能存在差异。

Study limitations included the retrospective design, which has inherent limitations. A small number of dogs, in which use of echocardiography did not identify a cardiac mass, did not have pericardectomy or necropsy performed within a short time after the echocardiographic examination and did not have repeat echocardiographic assessment for a mass. Therefore, it is possible that the sensitivity of echocardiography for detection of masses was higher than reflected in the study reported here. Given the retrospective nature of the study, many dogs were lost to follow-up monitoring and were treated as censored variables in the Kaplan-Meier survival analysis. Euthanasia may confound assessment of survival rates because there may be differences in owner commitment for continued treatment of dogs with cardiac masses that have a poor prognosis.


在此报告的研究中,由获得委员会认证的兽医心脏病专家或受监督的心脏病学住院医师进行的超声心动图对于检测心脏肿块以及区分心包积液的狗的心脏基底肿块和右心房肿块具有很高的敏感性和特异性。重复进行超声心动图检查可提高诊断心脏肿块的敏感性。所有心包积液的肿瘤性病因的转移率都很高,为 50%-66%,且特定肿瘤病因之间的转移率没有差异。

In the study reported here, echocardiography performed by a board-certified veterinary cardiologist or supervised cardiology resident had high sensitivity and specificity for detection of a cardiac mass and for discriminating between heart base masses and right atrial masses in dogs with pericardial effusion. Repeat echocardiographic examinations improved the sensitivity for diagnosis of a cardiac mass. All neoplastic causes of pericardial effusion had high metastatic rates of 50% to 66%, and the metastatic rates did not differ between the specific neoplastic causes.


6 References

1. Tobias AH. Pericardial disorders. In: Ettinger SJ, Feldman EC, eds. Textbook of veterinary internal medicine. 6th ed. St Louis: Elsevier Saunders, 2005;1104–1118.

2. Dunning D, Monnet E, Orton EC, et al. Analysis of prognostic indicators for dogs with pericardial effusion: 46 cases (1985–1996). J Am Vet Med Assoc 1998;212:1276–1280.

3. Kerstetter KK, Krahwinkel DJ Jr, Millis DL, et al. Pericardiectomy in dogs: 22 cases (1978–1994). J Am Vet Med Assoc 1997;211:736–740.

4. Berg RJ, Wingfield W. Pericardial effusion in the dog: a review of 42 cases. J Am Anim Hosp Assoc 1984;20:721–730.

5. Thomas WP, Sisson D. Detection of cardiac masses in dogs by two-dimensional echocardiography. Vet Radiol 1984;25:65–72.

6. Stafford Johnson M, Martin M, Binns S, et al. A retrospective study of clinical findings, treatment and outcome in 143 dogs with pericardial effusion. J Small Anim Pract 2004;45:546–552.

7. Ehrhart N, Ehrhart EJ, Willis J, et al. Analysis of factors affecting survival in dogs with aortic body tumors. Vet Surg 2002;31:44–48.

8. Vicari ED, Brown DC, Holt DE, et al. Survival times of and prognostic indicators for dogs with heart base masses: 25 cases (1986–1999). J Am Vet Med Assoc 2001;219:485–487.

9. Weisse C, Soares N, Beal MW, et al. Survival times in dogs with right atrial hemangiosarcoma treated by means of surgical resection with or without adjuvant chemotherapy: 23 cases (1986–2000). J Am Vet Med Assoc 2005;226:575–579.

10. Shaw SP, Rush JE. Canine pericardial effusion: diagnosis, treatment, and prognosis. Compend Contin Educ Pract Vet 2007;29:405–411.

11. Fruchter AM, Miller CW, O'Grady MR. Echocardiographic results and clinical considerations in dogs with right atrial/auricular masses. Can Vet J 1992;33:171–174.

12. Sisson D, Thomas WP, Ruehl WW, et al. Diagnostic value of pericardial fluid analysis in the dog. J Am Vet Med Assoc 1984;184:51–55.




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