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. 2022 Oct 24;54(6):1123–1127. [Article in Chinese] doi: 10.19723/j.issn.1671-167X.2022.06.011

唾液腺超声对干燥综合征的诊断价值

Diagnostic performances of salivary gland ultrasonography for Sjögren's syndrome

Yang LIU 1, Fang CHENG 1, Yan-ling WANG 1, Xiang-yan AI 1, Zhen-hang ZHU 1, Fu-tao ZHAO 1,*
PMCID: PMC9761832  PMID: 36533343

Abstract

Objective

To evaluate the diagnostic performances of salivary gland ultrasonography(SGUS)in Sjögren's syndrome(SS).

Methods

A total of 246 patients with dry mouth and/or eyes who were treated in the outpatient department and inpatient department of Rheumatology and Immunology Department of the Ninth People's Hospital, Shanghai Jiaotong University School of Medicine from December 2019 to January 2022 were collected. All patients received SGUS examination and scored by 2019 outcome measures in rheumatology clinical trial (OMERACT)ultrasonic scoring system.Their general information, unstimulated saliva flow rate(USFR), Schirmer test and serological test results were recorded. In the study, 193 cases had lip gland biopsy. The 2016 American College of Rheumatology(ACR)/ European League Against Rheumatism(EULAR)classification criteria were adopted as the diagnostic standard of SS. χ2 test was used to compare the difference of salivary gland ultrasonic scores between the two groups. The receiver operating characteristic(ROC) curve was used to evaluate the accuracy of SGUS in diagnosing SS, and the disease characteristics of SGUS positive group and negative group in the SS patients were compared.

Results

A total of 175 patients were SS group according to the ACR/EULAR classification, and the remaining 71 patients were non-SS group.There was no significant difference in age [(54.2±11.8) years vs. (53.4±14.9) years, P=0.705] and female (94.4% vs.93.1%, P=1.000) between SS and non-pSS groups. A total of 109 patients were SGUS positive (≥ 2 points), of whom 104 patients met the SS diagnosis and 5 patients did not meet the SS diagnosis. The positive rate of SGUS in SS group was significantly higher than that in non-SS group (59.4% vs. 7.0%, P < 0.001). The accuracy of 2019 OMERACT ultrasonic scoring system to predict ACR/EULAR classification was good, with an area under the curve of 0.762 (95%CI 0.701-0.823). The absolute agreement between the SGUS outcome and ACR-EULAR classification was 69.1%(170/246), with a sensiti-vity of 59.4%(104/175), specificity of 93%(66/71), positive predictive value of 95.4%(104/109) and negative predictive value of 48.2% (66/137). A total of 81 patients were positive SGUS combined with anti-SSA antibody, 100% (81/81) fulfilled the ACR-EULAR criteria, 85 patients were negative SGUS and anti SSA antibody, and 60 patients(70.6%, 60/85) did not fulfil the ACR-EULAR criteria. SGUS positive group had higher antinuclear antibody(ANA) positive rate(83.1% vs. 98.1%, P < 0.001) in the patients with SS.

Conclusion

The OMERACT ultrasonic scoring system has high diagnostic value in SS. The combination of SGUS and anti-SSA antibody can improve the diagnostic value.

Keywords: Sjögren's syndrome, Salivary gland, Ultrasound

干燥综合征(Sjögren’s syndrome, SS)是一种以口干、眼干为主要表现的常见自身免疫性疾病，诊断基于多个参数的组合，目前最新的分类标准为2016年美国风湿病学会(American College of Rheumatology，ACR)/欧洲抗风湿病联盟(European League Against Rheumatism，EULAR)共识[1]，包括客观干燥症状(Schirmer试验、唾液流率、角膜染色评分)、自身抗体及唾液腺活检的灶性浸润。分类标准中部分条目虽然简单，但在临床工作中应用易受限制，如唾液流率易受外界影响、眼科检查需要眼科专科就诊等。唾液腺超声(salivary gland uhrasonography，SGUS)具备无创、便捷等优势，临床上已广泛用于SS的筛查、评估，由于其发展起步较晚，所以并没有被包括在最近的分类标准中。近年来对SGUS已提出了0~4分、0~16分、0~48分等多个评分系统[2-4]，它们对诊断SS均具有较好的敏感性和特异性，且已有多个研究提出了将SGUS纳入现有SS分类标准以提高其诊断性能[5-7]，但是由于对SS唾液腺病变缺乏统一的定义和分级系统，限制了SGUS在临床工作中的常规应用。2019年风湿病临床试验结果指标(outcome measures in rheumatology clinical trial，OMERACT)工作组提出了一个基于共识的评分系统以协调和标准化SGUS的评分[8]，该评分系统按半定量分级系统对SS患者中腮腺和颌下腺的实质异质性进行评估，评分范围为0~3分，0分：正常实质；1分：轻微病变，轻度回声不均，没有无/低回声区；2分：中度病变，中度回声不均，有局灶的无/低回声区；3分：重度病变，弥漫的回声不均，整个腺体表面均为无/低回声区，如果无法按半定量分级，可定性为脂肪化回声(轻微，1分)和纤维化回声(严重，3分)，两种方法得分≥2分定义为SS患者的唾液腺异常病变。本研究的目的是评估2019年OMERACT超声评分系统对SS诊断价值。

1. 资料与方法

1.1. 临床资料

本研究为回顾性研究，共收集2019年12月至2022年1月就诊于上海交通大学医学院附属第九人民医院风湿免疫科门诊及住院部的口干和(或)眼干患者246例，均完善SGUS检查。记录一般资料、未刺激唾液流率(unstimulated saliva flow rate, USFR)、Schirmer试验、唇腺活检(共193例)及血清学检查结果，包括抗核抗体(antinuclear antibody, ANA)、抗干燥综合征A(Sjögren’s syndrome A, SSA)抗体、抗干燥综合征B(Sjögren’s syndrome B, SSB)抗体、抗着丝点抗体、类风湿因子(rheumatoid factors, RF)、红细胞沉降率(erythrocyte sedimentation rate, ESR)、免疫球蛋白G(immunoglobulin G, IgG)等。

1.2. SGUS检查

选用PHIUPS iU22彩超诊断仪，高频线阵探头，频率范围5~12 MHz。依次检查双侧腮腺、颌下腺及周围组织。将患者4个唾液腺体测量结果按照2019年OMERACT超声评分系统进行评分，取单个腺体得分最高者计分。

1.3. 统计学分析

研究采用2016年ACR/EULAR共识作为SS诊断金标准。将SGUS结果与金标准对比，SGUS阳性且确诊SS人数为A，SGUS阳性且未确诊SS人数为B，SGUS阴性且确诊SS人数为C，SGUS阴性且未确诊SS人数为D，敏感度=A/(A+C)，特异度=D/(B+D)，阳性预测值=A/(A+B)，阴性预测值=D/(C+D)。采用SPSS20.0统计分析软件，计量资料用均数±标准差(x±s)、中位数(四分位距)[M(P25, P75)]表示，计数资料用百分比(%)表示。两组间比较采用χ2检验、t检验及Mann-Whitney U检验，用受试者工作特征(receiver operating characteristic，ROC)曲线评估SGUS诊断SS的准确性。

2. 结果

2.1. 临床资料

本研究入组246例患者，175例符合2016年ACR/EULAR共识，为SS组；余71例不符合2016年ACR/EULAR共识，为非SS组。SS组中，男性12例，女性163例；非SS组中，男性4例，女性67例。两组在年龄、性别及Schirmer试验阳性率中差异无统计学意义，相对于非SS组，SS组病程更长，USFR减低明显，唾液腺肿大发生率高，血清自身抗体(ANA、抗SSA抗体、抗SSB抗体、抗着丝点抗体、RF)阳性率更高，血IgG、ESR水平明显升高。共109例患者SGUS≥2分，为SGUS阳性组，余137例为阴性组。104例SGUS阳性患者符合SS诊断，5例SGUS阳性患者不符合SS诊断，这5例患者分别确诊为IgG4相关疾病、结节病、未分化结缔组织病、复发性腮腺炎及单纯口眼干燥症。SS组SGUS阳性者占59.4%(104/175)，显著高于非SS组7%(5/71)，P=0.000，见表 1。

表 1.

研究人群的基线特征

Baseline characteristics of the study population

Items Non-SS (n=71) SS (n=175) t/χ2/Z P
SS, Sjögren’s syndrome; USFR, unstimulated saliva flow rate; ANA, antinuclear antibody; SSA, Sjögren’s syndrome A; SSB, Sjögren’s syndrome B; RF, rheumatoid factors; IgG, immunoglobulin G; ESR, erythrocyte sedimentation rate; SGUS, salivary gland ultrasonography.
Age/years, x±s 54.2±11.8 53.4±14.9 0.860 0.391
Female, n (%) 67 (94.4) 163 (93.1) 0.005 0.946
Course of disease/months，M(P25, P75) 12 (3, 24) 36 (6, 96) -3.332 0.001
Enlargement of salivary gland, n (%) 3 (4.2) 33 (18.9) 8.656 0.003
Schirmer test, n (%) 52 (73.2) 147 (84.0) 3.784 0.052
USFR/(mL/15 min)，x±s 3.8±3.6 1.7±1.4 -5.716 < 0.001
ANA, n (%) 40 (56.3) 161 (92.0) 42.977 < 0.001
Anti-SSA antibody, n (%) 6 (8.5) 127 (72.6) 81.618 < 0.001
Anti-SSB antibody, n (%) 0 (0) 40 (22.9) 19.380 < 0.001
Anti-centrometric antibody, n (%) 5 (7.0) 31 (17.7) 4.605 0.032
RF，n (%) 8 (11.3) 71 (40.6) 19.895 < 0.001
IgG, n (%) 13 (18.3) 97 (55.4) 28.150 < 0.001
ESR/(mm/h), x±s 17.5±14.2 31.1±21.2 5.039 < 0.001
SGUS, n (%) 5 (7.0) 104 (59.4) 56.172 < 0.001
Lip biopsy (n =193), n (%) 4(6.7) (n=58) 112(83) (n=135) 97.894 < 0.001
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2.2. SGUS评分系统的诊断价值

根据SGUS评分结果，绘制ROC曲线，其曲线下面积为0.762(95%CI 0.701~0.823)，见图 1。SGUS评分与ACR/EULAR共识的绝对符合率为69.1%(170/246)，敏感性为59.4% (104/175)，特异性为93.0% (66/71)，阳性预测值为95.4% (104/109)，阴性预测值为48.2% (66/137)。

图 1.

图 1

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唾液腺超声诊断干燥综合征的受试者工作特征曲线

Receiver operating characteristic curve of salivary gland ultrasonography scores in diagnosis of Sjögren's syndrome

2.3. SGUS评分与抗SSA抗体联合的诊断价值

共81例患者SGUS、抗SSA抗体双阳性，81例均符合ACR/EULAR共识，阳性符合率为100%(81/81)；28例患者SGUS阳性并抗SSA抗体阴性，23例(82.1%，23/28))符合ACR/EULAR共识；52例患者SGUS阴性且抗SSA抗体阳性，46例(88.5%，46/52)符合ACR/EULAR共识；85例患者SGUS阴性且无抗SSA抗体，60例未达到ACR/EULAR共识，阴性符合率为70.6% (60/85)。

2.4. SGUS评分与SS疾病临床特征之间的关联

SS患者中，SGUS阳性组和阴性组ANA阳性率差异有统计学意义，但是在年龄、性别、抗SSB、抗SSA阳性率、RF、IgG、USFR、Schirmer试验阳性率和唇腺活检阳性率等方面差异无统计学意义，见表 2。

表 2.

SS患者中SGUS阳性组与阴性组临床特征

Clinical characteristics of SGUS positive and negative groups in patients with SS

Items SGUS negative (n=71) SGUS positive (n=104) t/χ2/Z P
SGUS, salivary gland ultrasonography; SS, Sjögren’s syndrome; ANA, antinuclear antibody; SSA, Sjögren’s syndrome A; SSB, Sjögren’s syndrome B; RF, rheumatoid factors; IgG, immunoglobulin G; ESR, erythrocyte sedimentation rate; USFR, unstimulated saliva flow rate.
Age/years, x±s 53.9±15.1 53.0±14.9 0.396 0.693
Female, n (%) 66 (93.0) 97 (93.3) 0.000 1.000
Course of disease/months，M(P25, P75) 36 (6, 120) 36 (12, 60) -0.087 0.931
Schirmer test, n (%) 58 (81.7) 89 (85.6) 0.474 0.491
ANA, n (%) 59 (83.1) 102 (98.1) 12.862 < 0.001
Anti-SSA antibody, n (%) 46 (64.8) 81 (77.9) 3.635 0.057
Anti-SSB antibody, n (%) 12 (16.9) 28 (26.9) 2.403 0.121
Anti-centrometric antibody, n (%) 9 (12.7) 22 (21.2) 2.081 0.149
RF, n (%) 30 (42.3) 41 (39.7) 0.140 0.708
IgG, n (%) 35 (49.3) 61 (59.6) 1.819 0.177
ESR/(mm/h), x±s 20.8±18.2 31.2±23.1 -0.118 0.906
USFR/(mL/15 min)，x±s 1.8±1.5 1.7±1.3 0.574 0.567
Lip biopsy, n (%) (n=135) 50/61 (82) (n=61) 62/74 (83.8) (n=74) 0.780 0.780
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3. 讨论

唾液腺超声是一种简便的、非侵入性的技术，临床上广泛用于评估疑似SS的患者。迄今为止，已经提出多种SGUS评分系统，2018年的一项荟萃分析显示[9]，不同超声评分系统诊断SS的灵敏度分别为75% (0~4评分系统)、84% (0~16评分系统)、75%(0~48评分系统)；特异性分别为93% (0~4评分系统)、88% (0~16评分系统)、95%(0~48评分系统)，其后，Ramsubeik等[10]对一项纳入6 087例患者的荟萃分析显示，唾液腺超声诊断SS的综合敏感度为80%(95%CI 77~83)，特异性为90% (95%CI 87~92)，这些研究中使用了不同的超声评分系统，评估了腺体大小、实质不均性、边界的清晰性和血流改变等多个项目[11]。然而，研究显示实质回声不均性是SS最相关的超声征象，且具有良好的观察者间信度[12-13]。2019年OMERACT工作组发表了对SS病变定义的共识和分级系统，将SS中腮腺和颌下腺的异常病变定义为局限或弥漫的无/低回声灶，且制定出明确的病变分级系统(0~3级)[8]。SGUS评分系统能否在SS的诊断中发挥作用，首先要评估其可信度。经测评，2019年OMERACT超声评分系统对SS患者唾液腺结构的评估是可靠的，具有优秀的观察者内信度及良好的观察者间信度[8, 14]。多个研究显示，其诊断SS的敏感性为52%~72%，特异性为81%~91%[5, 15-17]。将SGUS加入2016年ACR/EULAR分类标准后，分类标准的敏感性上升，特异性略有下降[5-6, 17]；将SGUS分别替换分类标准中角膜染色评分、Schirmer试验和唾液流率等3个项目后，该标准的诊断性能无显著变化[6]，这些研究均体现出SGUS对SS的诊断具有重要价值。

在我们的研究中，根据2019年OMERACT超声评分系统，SGUS诊断SS的敏感性为59.4%，特异性为93.0%，SS患者的SGUS评分明显高于非SS组。我们的结果与上述文献[5, 15-17]结果基本一致。总体来说，根据2019年OMERACT超声评分系统，SGUS对SS的诊断非常特异，但敏感性略低，缺乏敏感性似乎并不能用疾病病程来解释，我们的研究显示，在SS患者中，SGUS阴性组与阳性组病程差异无统计学意义(P=0.524)，这与之前的研究结果[17]一致。另有研究显示，SS患者SGUS实质异常在2年内无显著变化[18]。SS患者中，SGUS正常者与低疾病活动度相关[19]，因此，我们推测SGUS较低的敏感性可能与SS的异质性相关，未来SGUS特征性改变可能成为某一类型SS的标记。

本研究中，SGUS、抗SSA抗体双阳性的患者中，阳性符合率为100%(81/81)。在SGUS、抗SSA抗体双阴性的患者中，阴性符合率为70.6% (60/85)，表明SGUS联合抗SSA抗体阳性预测诊断，但SGUS、抗SSA抗体双阴性不能排除诊断。既往有研究显示[20]，在SGUS与抗SSA抗体双阳性的患者中，97% (35/36)符合ACR/EULAR共识，在SGUS与抗SSA抗体双阴性的患者中，98% (44/45)未达到ACR/EULAR共识；另一项研究显示在抗SSA抗体阴性患者中，SGUS评分阴性符合率达92%，提示SS的诊断几乎是不可能的，因此，可以避免此类人群进一步行唇腺活检[15]。本研究结果与此前研究[20]阳性符合率类似，阴性符合率略低，可能与研究样本人群、样本量差异及应用不同的SGUS评价系统等因素相关。

此外，我们发现SGUS评分与临床和实验室结果有很好的相关性，在SS患者中，SGUS阳性组有更高的ANA阳性率，这与Kim等[21]的研究基本一致，唾液腺超声实质不均性的严重程度与抗SSA抗体的阳性率、唾液流率及唾液腺活检的灶性评分显著相关；另一项研究表明[22]，利妥昔单抗治疗后唾液腺的实质不均性可能得到改善，这可能间接证实了该疾病中腺体受累、免疫学参数和B淋巴细胞过度活跃之间的重要相关性，因此，2019年OMERACT超声评分的建立除了对SS的诊断价值之外，可能对其预后发挥重要作用，比如，提示患者有因B淋巴细胞过度活化(如冷球蛋白血症或B细胞淋巴瘤等疾病)而导致系统性并发症的风险[23]，未来仍需大样本、多中心的临床研究进一步证实。

根据2019年OMERACT超声评分，SGUS对SS的诊断非常特异，且评分简便，易于临床应用，联合抗SSA抗体可进一步提高诊断性能。此外，未来仍需大样本、多中心的临床研究进一步证实SGUS在SS病情评估及预后中的作用。

Funding Statement

上海市浦江风湿青年医师培育计划(SPROG202005)

Supported by the Shanghai Pujiang Young Rheumatologists Traning Program(SPROG202005)

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