Volume 42 Issue 6
Dec.  2018
Article Contents

Citation:

The characteristics of 18F-FDG PET/CT in pulmonary cryptococcosis

  • Corresponding author: Fengchun Hua, huafc@hotmail.com
  • Received Date: 2018-04-03
    Fund Project:

    Shanghai Sailing Program 18YF1403200

  • ObjectiveTo investigate the 18F-FDG PET/CT imaging characteristics and PET metabolic characteristics of pulmonary cryptococcosis (PC).MethodsA retrospective study was performed in 22 patients with PC (16 male and 6 female; 34-81 years old), confirmed through etiology or pathological examination from March 2011 to October 2015. To analyze the clinical data, CT patterns (single nodule, multiple nodules, pneumonia type, and mixed type), CT signs (vessel convergence sign, spiculation sign, halo sign, air bronchogram, and lobulation), and FDG metabolic patterns(hypermetabolism and hypometabolism) of PC were analyzed.ResultsPC was characterized by single nodule(9/22), multiple nodules(7/22), pneumonia type (1/22), and mixed type (5/22) for the 22 patients with PC. Most of the nodules were found in the inferior lobe of the lung. There were 15 cases(15/22, 68.18%) involving one or both inferior lobe of the lungs, of which 9 cases(9/22, 40.91%) involving the right inferior lobe, 2 cases(2/22, 9.09%) involving the left inferior lobe. Vessel convergence sign(12/21) was the most common sign, followed by spiculation(10/21), halo sign(8/22), air-bronchogram sign(6/21), and lobulation(4/21) with nodules on CT scan. The maximum standardized uptake value of PC was from 1.00 to 12.67 on 18F-FDG PET/CT scan, and hypermetabolism type (20/22) was the predominant pattern. Six patients with single nodule were misdiagnosed as malignant tumors.ConclusionsMost cases of PC were characterized with single and multiple nodules. A relative high rate of misdiagnosis was obtained using 18F-FDG PET/CT scan with varied standardized uptake value. Diagnosis of single nodule with high FDG metabolism in lung cancer should differentiate from PC.
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  • [1] 杨海, 刘子姗, 陈盈, 等.免疫正常患者肺隐球菌病的CT征象分析[J].中华全科医学, 2018, 16(2):279-282, 290. DOI:10.16766/j.cnki.issn.1674-4152.000078.Yang H, Liu ZS, Chen Y, et al. CT findings of pulmonary cryptococcosis in immunocompetent patients[J]. Chin J General Pract, 2018, 16(2):279-282, 290. DOI:10.16766/j.cnki.issn.1674-4152.000078.
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    [3] 陈挺, 张宏, 田梅. 18F-FDG PET/CT代谢半定量参数在非小细胞肺癌预后评估中的价值[J].国际放射医学核医学杂志, 2018, 42(3):269-273. DOI:10.3760/cma.j.issn.1673-4114.2018.03.014.Chen T, Zhang H, Tian M. Prognostic evaluation of patients with non-small cell lung cancer by using semi-quantitative metabolic parameters of 18F-FDG PET/CT[J]. Int J Radiat Med Nucl Med, 2018, 42(3):269-273. DOI:10.3760/cma.j.issn.1673-4114.2018. 03.014.
    [4] 谭延林, 董楚宁, 王云华. 18F-FDG PET/CT在肺癌疗效评估中的价值[J].国际放射医学核医学杂志, 2018, 42(4):357-362. DOI:10.3760/cma.j.issn.1673-4114.2018.04.013.Tan YL, Dong CN, Wang YH. The value of 18F-FDG PET/CT on evaluating therapeutic effect in the treatment of lung cancer[J]. Int J Radiat Med Nucl Med, 2018, 42(4):357-362. DOI:10.3760/cma.j.issn.1673-4114.2018.04.013.
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    [6] Nagelschneider AA, Broski SM, Holland WP, et al. The flip-flop fungus sign:an FDG PET/CT sign of benignity[J]. Am J Nucl Med Mol Imaging, 2017, 7(5):212-217.
    [7] 刘佳, 吴泰华, 翟文爽, 等. 22例误诊为周围型肺癌的肺隐球菌病患者临床分析[J].大连医科大学学报, 2017, 39(4):349-353. DOI:10.11724/jdmu.2017.04.08.Liu J, Wu TH, Zhai WS, et al. Analysis on 22 cases of pulmonary cryptococcosis misdiagnosed as peripheral lung cancer[J]. J Dalian Med Univ, 2017, 39(4):349-353. DOI:10.11724/jdmu.2017.04.08.
    [8] 梅周芳, 秦欣宇, 潘星月, 等.无免疫功能缺陷的肺隐球菌病19例误诊分析[J].临床误诊误治, 2016, 29(1):50-52. DOI:10.3969/j.issn.1002-3429.2016.01.019.Mei ZF, Qin XY, Pan XY, et al. Misdiagnosis Analysis on 19 Cases of Non-immunodeficiency Pulmonary Cryptococcosis[J]. Clin Misdiag Misther, 2016, 29(1):50-52. DOI:10.3969/j.issn.1002-3429.2016.01.019.
    [9] 谢丽璇, 李国雄, 刘志军, 等. 33例肺良性病变的18F-FDG PET/CT误诊原因分析[J].放射学实践, 2014, 29(5):541-544. DOI:10.13609/j.cnki.1000-0313.2014.05.020.Xie LX, Li GX, Liu ZJ, et al. Analysis in 33 cases of misdiagnosed pulmonary benign lesions by 18F-FDG PET/CT imaging[J]. Radiol Practice, 2014, 29(5):541-544. DOI:10.13609/j.cnki.1000-0313. 2014.05.020.
    [10] Wang SY, Chen G, Luo DL, et al. 18F-FDG PET/CT and contrast-enhanced CT findings of pulmonary cryptococcosis[J]. Eur J Radiol, 2017, 89:140-148. DOI:10.1016/j.ejrad.2017.02.008.
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    [13] Zhao M, Ma Y, Yang B, et al. A meta-analysis to evaluate the diagnostic value of dual-time-point F-fluorodeoxyglucose positron emission tomography/computed tomography for diagnosis of pulmonary nodules[J]. J Cancer Res Ther, 2016, 12(Suppl):C304S-C308. DOI:10.4103/0973-1482.200742.
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The characteristics of 18F-FDG PET/CT in pulmonary cryptococcosis

    Corresponding author: Fengchun Hua, huafc@hotmail.com
  • 1. Department of Radiology, Shuyang Affiliated Hospital of Nanjing University of Chinese Medicine, Shuyang 223600, China
  • 2. PET Center, Huashan Hospital, Fudan University, Shanghai 200235, China
  • 3. Department of Infectious Disease, Huashan Hospital, Fudan University, Shanghai 200040, China
Fund Project:  Shanghai Sailing Program 18YF1403200

Abstract: ObjectiveTo investigate the 18F-FDG PET/CT imaging characteristics and PET metabolic characteristics of pulmonary cryptococcosis (PC).MethodsA retrospective study was performed in 22 patients with PC (16 male and 6 female; 34-81 years old), confirmed through etiology or pathological examination from March 2011 to October 2015. To analyze the clinical data, CT patterns (single nodule, multiple nodules, pneumonia type, and mixed type), CT signs (vessel convergence sign, spiculation sign, halo sign, air bronchogram, and lobulation), and FDG metabolic patterns(hypermetabolism and hypometabolism) of PC were analyzed.ResultsPC was characterized by single nodule(9/22), multiple nodules(7/22), pneumonia type (1/22), and mixed type (5/22) for the 22 patients with PC. Most of the nodules were found in the inferior lobe of the lung. There were 15 cases(15/22, 68.18%) involving one or both inferior lobe of the lungs, of which 9 cases(9/22, 40.91%) involving the right inferior lobe, 2 cases(2/22, 9.09%) involving the left inferior lobe. Vessel convergence sign(12/21) was the most common sign, followed by spiculation(10/21), halo sign(8/22), air-bronchogram sign(6/21), and lobulation(4/21) with nodules on CT scan. The maximum standardized uptake value of PC was from 1.00 to 12.67 on 18F-FDG PET/CT scan, and hypermetabolism type (20/22) was the predominant pattern. Six patients with single nodule were misdiagnosed as malignant tumors.ConclusionsMost cases of PC were characterized with single and multiple nodules. A relative high rate of misdiagnosis was obtained using 18F-FDG PET/CT scan with varied standardized uptake value. Diagnosis of single nodule with high FDG metabolism in lung cancer should differentiate from PC.

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  • 肺隐球菌病(pulmonary cryptococcosis,PC)是由新型隐球菌感染引起的深部真菌病,呈亚急性或慢性病程的机会性感染性疾病。PC多见于获得性免疫缺陷综合征、器官移植、免疫抑制剂治疗等免疫功能低下者,但在免疫功能正常者中也并不少见;该病的CT影像学表现以单发或多发结节较为常见,也可以表现为肺间质浸润、肺叶实变、胸膜浸润甚至巨大肿块[1-2]。由于PC的影像学表现的多样性,肺隐球菌感染难以与肺癌及转移瘤鉴别诊断。18F-FDG PET/CT主要用于良恶性病变的鉴别诊断,肿瘤分期、疗效评价及预后评估。随着PET/CT临床应用的日益增多,PC受检者也越来越多,为了更好地了解PC的PET/CT影像学特征,避免误诊误治,笔者对复旦大学附属华山医院PET中心收治的PC患者的临床资料及其PET/CT图像特征进行回顾性分析,以期提高对PC影像学特征的认知。

1.   资料与方法

    1.1.   一般资料

  • 选取2011年3月至2015年10月于复旦大学附属华山医院PET中心行PET/CT检查并最终确诊为PC的患者22例,其中男性16例、女性6例,年龄34~81(49.9±10.1)岁。纳入标准:①经病理结果证实为PC;②患者在行PET/CT检查前未行抗炎及其他肿瘤相关治疗;③患者行PET/CT检查与病理证实时间间隔不超过两周。反之则为排除标准。所有患者均对本研究知情同意并签署知情同意书。

  • 1.2.   显像方法

  • PET/CT显像仪为德国Siemens Biograph 64 HD型。18F-FDG由复旦大学附属华山医院PET中心自行生产,放化纯度>95%。患者禁食6 h以上,控制血糖<8.0 mmol/L,按体重(3.70~5.55 MBq/kg)静脉注射18F-FDG显像剂。安静休息1 h后进行PET/CT显像,6例受检者于2 h后行延迟显像。先行CT扫描,管电压120 kV,管电流根据体重自动调节(care dose 100~120 mA),层厚5.0 mm;后行PET扫描,采用三维模式,2 min/床位,5~6个床位。应用CT数据进行衰减校正,迭代法重建,最终获得CT、PET及PET/CT融合图像。

  • 1.3.   图像分析方法

  • 由复旦大学附属华山医院PET中心2名有5年以上PET/CT诊断经验的医师独立分析并达成一致意见。CT图像:根据病灶形态,将其分为单发结节型、多发结节型、肺炎型、混合型(含有以上两种及两种以上特征);从CT重建图像上选取较大层面测量病灶大小(长径)。PET图像:沿病灶边缘勾画ROI,由计算机自动得出病变FDG SUVmax;与纵隔血池SUVmax比较,将病变分为FDG低代谢型与高代谢型。

2.   结果

    2.1.   PC的临床特征

  • 22例PC患者中,咳嗽咳痰7例、痰中带血2例、发热7例、无症状体检发现6例;22例均无明确的鸽子接触史;既往合并肿瘤4例:胃癌2例、肝癌介入及伽玛刀治疗后1例、非霍奇金淋巴瘤1例;既往食管炎治疗后1例;经手术病理证实16例,经皮肺穿刺活检确诊5例,支气管镜刷检确诊1例。

  • 2.2.   PC的CT影像学特征

  • 22例PC患者中,单发结节型9例、多发结节型7例、肺炎型1例、混合型5例。发病部位以下肺为主,病灶累及一侧或双侧肺下叶15例(15/22,68.18%),其中仅累及右肺下叶9例(9/22,40.90%),仅累及左肺下叶2例(2/22,9.09%)。

    9例单发结节型患者中,右肺上叶2例、右肺下叶4例、左肺上叶2例、左肺下叶1例。单发结节型病灶最大径为1.0~2.7(1.56±0.61)cm。

    7例多发结节型患者中,双肺多发3例、右肺下叶多发2例、左肺下叶多发2例。各病例均选取较大的病灶,最大径为1.0~2.4(1.81±0.59)cm。

    1例肺炎型患者病灶位于右肺下叶,表现为右肺下叶条索灶。

    5例混合型患者中,右肺上叶、中叶多发1例,右肺下叶多发1例,双肺多发3例。实性病灶最大径为1.7~7.6(4.46±2.37)cm。

    22例患者中,有实性结节病灶21例,其中可见毛刺征10例(10/21,47.62%);血管集束征12例(12/21,57.14%)(图 1);分叶征4例(4/21,19.05%);支气管充气征6例(6/21,28.57%);空洞1例(1/21,4.76%);晕征8例(8/21,38.10%);呈宽基底与胸膜相连2例(2/21,9.52%);双侧胸腔积液2例(2/21,9.52%);纵隔淋巴结肿大1例(1/21,4.76%)。

    Figure 1.  Pulmonary cryptococcosis with FDG hypermetabolism in a 45-year-female

  • 2.3.   PC的18F-FDG PET/CT特征

  • 22例患者均进行了同机18F-FDG PET/CT扫描,与纵隔血池比较,2例呈FDG低代谢型,SUVmax分别为1.00、1.67;20例呈FDG高代谢型(图 1)。所有病变SUVmax为1.00~12.67(5.25±3.38)。单发结节型SUVmax为1.67~12.67(4.72±3.46),其中6例误诊为恶性病变,误诊率为66.7%(6/9)。多发结节型SUVmax为1.00~12.04(4.92±3.43),均诊断为炎性病变。肺炎型SUVmax为3.14。混合型SUVmax为2.17~10.92(7.07±3.52),均诊断为炎性病变。9例病灶呈现小病灶而SUV高摄取。6例结节型病灶2 h后进行了延迟显像,其中,1例病灶SUVmax减低(2.17%),2例SUVmax增高小于10%(6.41%、6.43%),余3例SUVmax增高分别为19.35%、38.64%、49.28%。21例实性病灶中误诊为恶性肿瘤性病变6例(6/21,28.57%),均为单发结节型,其中3例行延迟显像。

3.   讨论
  • PC主要是由隐球酵母属中的新型隐球菌及其变种引起的真菌病,新型隐球菌普遍存在于自然界中,经呼吸道吸入感染,因此初感染灶多位于肺部,肺外主要侵袭中枢神经系统,也可侵犯骨骼、皮肤、黏膜和其他脏器。PC的分型以结节型最常见,分布以下肺区、周围型为主[1]。本研究病例大多表现为结节型(16/22),且9例单发结节型均为小于3 cm的孤立性结节,为其鉴别诊断造成了一定的难度。本研究病例病灶累及一侧或双侧肺下叶15例,仅累及右肺下叶9例,病灶多靠近胸膜下及叶间胸膜下,这可能与右肺主支气管与气管夹角较大,且右肺主支气管较粗、较直有关,更易吸入病菌导致感染。

    PC的CT影像学表现具有多样性,如毛刺征、血管集束征、晕征、支气管充气征等,钙化较少见[1-2]。本研究病例以毛刺征、血管集束征、晕征最常见,支气管充气征及分叶征次之,以上CT特征并非PC的特征性改变,同样见于肺癌、肺结核及其他感染性病变,特别是对于单发结节型病灶来讲,鉴别诊断的难度较大。

    PET/CT将PET和CT两种影像学技术有机地结合在一起,18F-FDG PET/CT能同时显示病变的解剖特征及葡萄糖代谢特征。SUV是18F-FDG PET常用的半定量指标,是局部组织摄取脱氧葡萄糖的放射性活度与全身所注射放射性显像剂活度的比值,反映了病变组织细胞葡萄糖代谢的活跃程度[3-4]。活动性结核或结核球、急性或慢性肺炎、肺脓肿、真菌感染、寄生虫感染都会导致FDG代谢增高,原因主要是炎性组织中的巨噬细胞和中性粒细胞活跃,细胞吞噬作用及化学趋化、纤维母细胞增生都会导致葡萄糖代谢增加[5-6]。本研究病例多经其他检查未能明确诊断或高度怀疑肿瘤而行PET/CT,结果表明FDG高代谢型病例高达90.90%(20/22);SUVmax < 2.5的仅3例,若简单地以SUV=2.5作为阳性诊断标准,其误诊率极高。本研究中结节型PC的误诊率高达28.57%(6/21),均为单发的孤立性肺结节,小结节呈现FDG高代谢征象,若仅靠SUV很难与肿瘤进行鉴别,极易造成误诊。同样,多发结节型表现为SUV增高且摄取范围变化较大,需与转移瘤进行鉴别。因多发结节病灶的形态不规则或部分具有炎性病变的CT影像学表现,而转移瘤多为形态规则、边缘光整,故较易作出正确诊断。

    肺癌与肺肉芽肿性病变可能呈现不同的代谢模式;原发性初诊肺癌随病程进展逐渐增大,呈FDG高代谢,且FDG摄取高于转移性小淋巴结;急性期肉芽肿的肺部病变和纵隔淋巴结的FDG代谢都增高,但肺部结节FDG活性降低速度明显快于引流淋巴结(淋巴结亚急性期持续存在)[5-6]。肉芽肿FDG代谢模式(肉芽肿肺结节FDG代谢低于淋巴结,称为flip-flop现象)有别于肺癌及转移淋巴结(肺癌结节FDG代谢高于转移淋巴结),因此,把肺结节FDG代谢低于同侧肺门或纵隔淋巴结的征象定义为FFF征(flip-flop fungus sign),这有助于良性疾病的诊断。Nagelschneider等[6]对209例符合有肺部结节及引流淋巴结FDG阳性特征的病灶进行分析,其中良性病灶为70例,FFF征诊断良性病灶的灵敏度为60.0%,特异度为84.9%,阳性预测值为66.7%,阴性预测值为81.0%。严格的FFF征(除外伴钙化的结节、超过一个月缓慢生长的结节、肺外病理性FDG摄取病灶)能提高良性疾病诊断的特异度(98.6%)和阳性预测值(90.0%)[6]。FFF征阳性主要由肉芽肿性病变(91%)所致,尤其是组织胞浆菌病(73%)[6]。本研究中21例有肺部结节的病例,仅1例符合入组FFF征阳性,因此,FFF征对于单发肺部结节或肿块型的肺隐球菌感染的诊断价值比较有限,但在临床工作中如果病灶符合FFF征,需要考虑肉芽肿性病变。

    免疫功能正常的PC患者,其临床误诊率很高,影像学表现形式多种多样,需与肺结核、肺癌及机化性肺炎相鉴别[7-9]。Song等[2]研究结果表明,PC以聚集性结节型为主(10/23),其次为孤立性结节型(4/23);行PET或PET/CT的10例肺部隐球菌病灶,6例FDG呈高摄取(SUVmax为4.8~7.3)(其中5例FDG高代谢的多发结节被误诊为转移性肿瘤),另外4例表现为良性的FDG低代谢模式(SUVmax为1.8~2.9)。6例FDG高代谢的病例在确诊前CT诊断为结核2例,误诊为肺癌、乳腺癌转移、淋巴瘤肺部浸润及机化性肺炎各1例;4例FDG低代谢的病例在确诊前CT诊断为结核3例、乳腺癌转移1例;较多误诊为结核(5例)[2]。Wang等[10]对42例PC患者的研究结果表明,PC以单发性结节为主(29/42);病理确诊前除1例诊断为PC,其余诊断为肺结核17例,肺癌12例,炎性肉芽肿6例,肿瘤转移、淋巴瘤肺部浸润、机化性肺炎各2例;37例(88.1%)肺部病变表现为FDG高代谢,5例(11.9%)表现为FDG低代谢。

    既往有研究者认为PET双时相显像SUV变化对肺结节良恶性的鉴别有价值[11]。但近来的研究结果表明在肉芽肿高发区域PET双时相并不能改善肺恶性肿瘤的诊断[12]。Meta分析结果也表明双时相与单次PET显像的灵敏度、特异度相似[13]。Huang等[14]对7例PC患者的研究结果表明,4例肺结节延迟显像SUV升高(17.6%~32.3%),另外3例延迟显像SUV有所减低。这与本研究结果一致,表明PET双时相显像对肉芽肿性病变的判定存在偏差,需要仔细甄别以免误诊。因此,病原学和组织病理学检查对于PC的诊断至关重要,FDG代谢高低与病变炎症活动性有关,有助于定位穿刺有活性的病变组织。

    PC因其CT形态学特征与肿瘤具有共性,特别是肺部孤立性结节,PET显像上呈现葡萄糖代谢与肿瘤极为相似,因此,我们在考虑肺癌、肺结核的同时,需要与PC鉴别。综上,正确认识不同性质良性病变的好发部位、CT征象及葡萄糖代谢特点有助于减少误诊。

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