Clinical value of combining transvaginal contrast-enhanced ultrasonography with serum human epididymisprotein-4 and the resistance index for early-stage epithelial ovarian cancer

Wu Meng; Wang Ying; Zheng Qichao; Li Ping; Tang Jie

doi:10.15537/smj.2017.6.19790

References

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1. Matulonis UA,
2. Oza AM,
3. Ho TW,
4. Ledermann JA
(2015) Intermediate clinical endpoints: a bridge between progression-free survival and overall survival in ovarian cancer trials. Cancer 121:1737–1746.
OpenUrl CrossRef PubMed
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1. Kim A,
2. Ueda Y,
3. Naka T,
4. Enomoto T
(2012) Therapeutic strategies in epithelial ovarian cancer. J Exp Clin Cancer Res 31:14.
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1. Bogani G,
2. Cromi A,
3. Serati M,
4. Di Naro E,
5. Casarin J,
6. Pinelli C,
7. et al.
(2014) Laparoscopic and open abdominal staging for early-stage ovarian cancer: our experience, systematic review, and meta-analysis of comparative studies. Int J Gynecol Cancer 24:1241–1249.
OpenUrl Abstract/FREE Full Text
↵
1. Hamed EO,
2. Ahmed H,
3. Sedeek OB,
4. Mohammed AM,
5. Abd-Alla AA,
6. Abdel Ghaffar HM
(2013) Significance of HE4 estimation in comparison with CA125 in diagnosis of ovarian cancer and assessment of treatment response. Diagn Pathol 8:11.
OpenUrl CrossRef
↵
1. Karlsen MA,
2. Sandhu N,
3. Høgdall C,
4. Christensen IJ,
5. Nedergaard L,
6. Lundvall L,
7. et al.
(2012) Evaluation of HE4, CA125, risk of ovarian malignancy algorithm (ROMA) and risk of malignancy index (RMI) as diagnostic tools of epithelial ovarian cancer in patients with a pelvic mass. Gynecol Oncol 127:379–383.
OpenUrl CrossRef PubMed
↵
1. Liu Z,
2. Yang F,
3. Zhang Y,
4. Yu H,
5. Zhu H,
6. Yang R,
7. et al.
(2016) Conventional, doppler and contrast-enhanced ultrasonography in differential diagnosis of ovarian masses. Cell Physiol Biochem 39:2398–2408.
OpenUrl
↵
1. Karlsen NS,
2. Karlsen MA,
3. Hogdall CK,
4. Hogdall EV
(2014) HE4 tissue expression and serum HE4 levels in healthy individuals and patients with benign or malignant tumors: a systematic review. Cancer Epidemiol Biomarkers Prev 23:2285–2295.
OpenUrl Abstract/FREE Full Text
↵
1. Ruggeri G,
2. Bandiera E,
3. Zanotti L,
4. Belloli S,
5. Ravaggi A,
6. Romani C,
7. et al.
(2011) HE4 and epithelial ovarian cancer: comparison and clinical evaluation of two immunoassays and a combination algorithm. Clin Chim Acta 412:1447–1453.
OpenUrl CrossRef PubMed Web of Science
↵
1. Szymanski M,
2. Socha MW,
3. Kowalkowska ME,
4. Zielinska IB,
5. Eljaszewicz A,
6. Szymanski W
(2015) Differentiating between benign and malignant adnexal lesions with contrast-enhanced transvaginal ultrasonography. Int J Gynaecol Obstet 131:147–151.
OpenUrl
↵
1. Hauptmann S,
2. Friedrich K,
3. Redline R,
4. Avril S
(2017) Ovarian borderline tumors in the 2014 WHO classification: evolving concepts and diagnostic criteria. Virchows Arch 470:125.
OpenUrl PubMed
↵
1. Chang X,
2. Ye X,
3. Dong L,
4. Cheng H,
5. Cheng Y,
6. Zhu L,
7. et al.
(2011) Human epididymis protein 4 (HE4) as a serum tumor biomarker in patients with ovarian carcinoma. Int J Gynecol Cancer 21:852–858.
OpenUrl Abstract/FREE Full Text
↵
1. Abdullah LS,
2. Bondagji NS
(2012) Histopathological pattern of ovarian neoplasms and their age distribution in the western region of Saudi Arabia. Saudi Med J 33:61–65.
OpenUrl PubMed
↵
1. Suh DH,
2. Kim JW,
3. Kang S,
4. Kim HJ,
5. Lee KH
(2014) Major clinical research advances in gynecologic cancer in 2013. J Gynecol Oncol 25:236–248.
OpenUrl
↵
1. Liu JJ,
2. Li HX,
3. Chen ZB,
4. Yang WP,
5. Zhao SF,
6. Chen J,
7. et al.
(2015) Consistency analysis of contrast-enhanced ultrasound and contrast-enhanced CT in diagnosis of small hepatocellular carcinoma. Int J Clin Exp Med 8:21466–21471.
OpenUrl
↵
1. Szymanski M,
2. Socha MW,
3. Kowalkowska ME,
4. Zielinska IB,
5. Eljaszewicz A,
6. Szymanski W
(2015) Differentiating between benign and malignant adnexal lesions with contrast-enhanced transvaginal ultrasonography. Int J Gynaecol Obstet 131:147–151.
OpenUrl
↵
1. Fleischer AC,
2. Lyshchik A,
3. Jones HW Jr.,
4. Crispens M,
5. Loveless M,
6. Andreotti RF,
7. et al.
(2008) Contrast-enhanced transvaginal sonography of benign versus malignant ovarian masses: preliminary findings. J Ultrasound Med 27:1011–1018.
OpenUrl Abstract/FREE Full Text
1. Qiao JJ,
2. Yu J,
3. Yu Z,
4. Li N,
5. Song C,
6. Li M
(2015) Contrast-enhanced ultrasonography in differential diagnosis of benign and malignant ovarian tumors. PLoS One 10:e0118872.
OpenUrl
↵
1. Testa AC,
2. Ferrandina G,
3. Fruscella E,
4. Van Holsbeke C,
5. Ferrazzi E,
6. Leone FP,
7. et al.
(2005) The use of contrasted transvaginal sonography in the diagnosis of gynecologic diseases: a preliminary study. J Ultrasound Med 24:1267–1278.
OpenUrl Abstract/FREE Full Text
↵
1. Takayama S,
2. Watanabe M,
3. Kusuyama H,
4. Nagase S,
5. Seki T,
6. Nakazawa T,
7. et al.
(2012) Evaluation of the effects of acupuncture on blood flow in humans with ultrasound color Doppler imaging. Evid Based Complement Alternat Med 2012:513638.
OpenUrl PubMed
↵
1. Leinster DA,
2. Kulbe H,
3. Everitt G,
4. Thompson R,
5. Perretti M,
6. Gavins FN,
7. et al.
(2012) The peritoneal tumor microenvironment of high-grade serous ovarian cancer. J Pathol 227:136–145.
OpenUrl CrossRef PubMed Web of Science
↵
1. Huang W,
2. Cen S,
3. Kang XL,
4. Wang WF,
5. Wang Y,
6. Chen X
(2015) Doppler ultrasound measurement of resistance index in the diagnosis of prostate cancer. Tumor 101:644–649.
OpenUrl
↵
1. Shah CA,
2. Lowe KA,
3. Paley P,
4. Wallace E,
5. Anderson GL,
6. McIntosh MW,
7. et al.
(2009) Influence of ovarian cancer risk status on the diagnostic performance of the serum biomarkers mesothelin, HE4, and CA125. Cancer Epidemiol Biomarkers Prev 18:1365–1372.
OpenUrl Abstract/FREE Full Text
↵
1. Lee S,
2. Choi S,
3. Lee Y,
4. Chung D,
5. Hong S,
6. Park N
(2017) Role of human epididymis protein 4 in chemoresistance and prognosis of epithelial ovarian cancer. J Obstet Gynaecol Res 43:220–227.
OpenUrl CrossRef
↵
1. Schäberle W,
2. Leyerer L,
3. Schierling W,
4. Pfister K
(2016) Ultrasound diagnostics of renal artery stenosis: Stenosis criteria, CEUS and recurrent in-stent stenosis. Gefasschirurgie 21:4–13.
OpenUrl
↵
1. Maxim AR,
2. Badea R,
3. Tamas A,
4. Traila A
(2013) Contrast-enhanced ultrasound in ovarian tumors - diagnostic parameters: method presentation and initial experience. Clujul Med 86:31–35.
OpenUrl

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[1] ↵
Matulonis UA,
Oza AM,
Ho TW,
Ledermann JA
(2015) Intermediate clinical endpoints: a bridge between progression-free survival and overall survival in ovarian cancer trials. Cancer 121:1737–1746.
OpenUrl CrossRef PubMed

[2] Matulonis UA,

[3] Oza AM,

[4] Ho TW,

[5] Ledermann JA

[6] ↵
Kim A,
Ueda Y,
Naka T,
Enomoto T
(2012) Therapeutic strategies in epithelial ovarian cancer. J Exp Clin Cancer Res 31:14.
OpenUrl CrossRef PubMed

[7] Kim A,

[8] Ueda Y,

[9] Naka T,

[10] Enomoto T

[11] ↵
Bogani G,
Cromi A,
Serati M,
Di Naro E,
Casarin J,
Pinelli C,
et al.
(2014) Laparoscopic and open abdominal staging for early-stage ovarian cancer: our experience, systematic review, and meta-analysis of comparative studies. Int J Gynecol Cancer 24:1241–1249.
OpenUrl Abstract/FREE Full Text

[12] Bogani G,

[13] Cromi A,

[14] Serati M,

[15] Di Naro E,

[16] Casarin J,

[17] Pinelli C,

[18] et al.

[19] ↵
Hamed EO,
Ahmed H,
Sedeek OB,
Mohammed AM,
Abd-Alla AA,
Abdel Ghaffar HM
(2013) Significance of HE4 estimation in comparison with CA125 in diagnosis of ovarian cancer and assessment of treatment response. Diagn Pathol 8:11.
OpenUrl CrossRef

[20] Hamed EO,

[21] Ahmed H,

[22] Sedeek OB,

[23] Mohammed AM,

[24] Abd-Alla AA,

[25] Abdel Ghaffar HM

[26] ↵
Karlsen MA,
Sandhu N,
Høgdall C,
Christensen IJ,
Nedergaard L,
Lundvall L,
et al.
(2012) Evaluation of HE4, CA125, risk of ovarian malignancy algorithm (ROMA) and risk of malignancy index (RMI) as diagnostic tools of epithelial ovarian cancer in patients with a pelvic mass. Gynecol Oncol 127:379–383.
OpenUrl CrossRef PubMed

[27] Karlsen MA,

[28] Sandhu N,

[29] Høgdall C,

[30] Christensen IJ,

[31] Nedergaard L,

[32] Lundvall L,

[33] et al.

[34] ↵
Liu Z,
Yang F,
Zhang Y,
Yu H,
Zhu H,
Yang R,
et al.
(2016) Conventional, doppler and contrast-enhanced ultrasonography in differential diagnosis of ovarian masses. Cell Physiol Biochem 39:2398–2408.
OpenUrl

[35] Liu Z,

[36] Yang F,

[37] Zhang Y,

[38] Yu H,

[39] Zhu H,

[40] Yang R,

[41] et al.

[42] ↵
Karlsen NS,
Karlsen MA,
Hogdall CK,
Hogdall EV
(2014) HE4 tissue expression and serum HE4 levels in healthy individuals and patients with benign or malignant tumors: a systematic review. Cancer Epidemiol Biomarkers Prev 23:2285–2295.
OpenUrl Abstract/FREE Full Text

[43] Karlsen NS,

[44] Karlsen MA,

[45] Hogdall CK,

[46] Hogdall EV

[47] ↵
Ruggeri G,
Bandiera E,
Zanotti L,
Belloli S,
Ravaggi A,
Romani C,
et al.
(2011) HE4 and epithelial ovarian cancer: comparison and clinical evaluation of two immunoassays and a combination algorithm. Clin Chim Acta 412:1447–1453.
OpenUrl CrossRef PubMed Web of Science

[48] Ruggeri G,

[49] Bandiera E,

[50] Zanotti L,

[51] Belloli S,

[52] Ravaggi A,

[53] Romani C,

[54] et al.

[55] ↵
Szymanski M,
Socha MW,
Kowalkowska ME,
Zielinska IB,
Eljaszewicz A,
Szymanski W
(2015) Differentiating between benign and malignant adnexal lesions with contrast-enhanced transvaginal ultrasonography. Int J Gynaecol Obstet 131:147–151.
OpenUrl

[56] Szymanski M,

[57] Socha MW,

[58] Kowalkowska ME,

[59] Zielinska IB,

[60] Eljaszewicz A,

[61] Szymanski W

[62] ↵
Hauptmann S,
Friedrich K,
Redline R,
Avril S
(2017) Ovarian borderline tumors in the 2014 WHO classification: evolving concepts and diagnostic criteria. Virchows Arch 470:125.
OpenUrl PubMed

[63] Hauptmann S,

[64] Friedrich K,

[65] Redline R,

[66] Avril S

[67] ↵
Chang X,
Ye X,
Dong L,
Cheng H,
Cheng Y,
Zhu L,
et al.
(2011) Human epididymis protein 4 (HE4) as a serum tumor biomarker in patients with ovarian carcinoma. Int J Gynecol Cancer 21:852–858.
OpenUrl Abstract/FREE Full Text

[68] Chang X,

[69] Ye X,

[70] Dong L,

[71] Cheng H,

[72] Cheng Y,

[73] Zhu L,

[74] et al.

[75] ↵
Abdullah LS,
Bondagji NS
(2012) Histopathological pattern of ovarian neoplasms and their age distribution in the western region of Saudi Arabia. Saudi Med J 33:61–65.
OpenUrl PubMed

[76] Abdullah LS,

[77] Bondagji NS

[78] ↵
Suh DH,
Kim JW,
Kang S,
Kim HJ,
Lee KH
(2014) Major clinical research advances in gynecologic cancer in 2013. J Gynecol Oncol 25:236–248.
OpenUrl

[79] Suh DH,

[80] Kim JW,

[81] Kang S,

[82] Kim HJ,

[83] Lee KH

[84] ↵
Liu JJ,
Li HX,
Chen ZB,
Yang WP,
Zhao SF,
Chen J,
et al.
(2015) Consistency analysis of contrast-enhanced ultrasound and contrast-enhanced CT in diagnosis of small hepatocellular carcinoma. Int J Clin Exp Med 8:21466–21471.
OpenUrl

[85] Liu JJ,

[86] Li HX,

[87] Chen ZB,

[88] Yang WP,

[89] Zhao SF,

[90] Chen J,

[91] et al.

[92] ↵
Szymanski M,
Socha MW,
Kowalkowska ME,
Zielinska IB,
Eljaszewicz A,
Szymanski W
(2015) Differentiating between benign and malignant adnexal lesions with contrast-enhanced transvaginal ultrasonography. Int J Gynaecol Obstet 131:147–151.
OpenUrl

[93] Szymanski M,

[94] Socha MW,

[95] Kowalkowska ME,

[96] Zielinska IB,

[97] Eljaszewicz A,

[98] Szymanski W

[99] ↵
Fleischer AC,
Lyshchik A,
Jones HW Jr.,
Crispens M,
Loveless M,
Andreotti RF,
et al.
(2008) Contrast-enhanced transvaginal sonography of benign versus malignant ovarian masses: preliminary findings. J Ultrasound Med 27:1011–1018.
OpenUrl Abstract/FREE Full Text

[100] Fleischer AC,

[101] Lyshchik A,

[102] Jones HW Jr.,

[103] Crispens M,

[104] Loveless M,

[105] Andreotti RF,

[106] et al.

[107] Qiao JJ,
Yu J,
Yu Z,
Li N,
Song C,
Li M
(2015) Contrast-enhanced ultrasonography in differential diagnosis of benign and malignant ovarian tumors. PLoS One 10:e0118872.
OpenUrl

[108] Qiao JJ,

[109] Yu J,

[110] Yu Z,

[111] Li N,

[112] Song C,

[113] Li M

[114] ↵
Testa AC,
Ferrandina G,
Fruscella E,
Van Holsbeke C,
Ferrazzi E,
Leone FP,
et al.
(2005) The use of contrasted transvaginal sonography in the diagnosis of gynecologic diseases: a preliminary study. J Ultrasound Med 24:1267–1278.
OpenUrl Abstract/FREE Full Text

[115] Testa AC,

[116] Ferrandina G,

[117] Fruscella E,

[118] Van Holsbeke C,

[119] Ferrazzi E,

[120] Leone FP,

[121] et al.

[122] ↵
Takayama S,
Watanabe M,
Kusuyama H,
Nagase S,
Seki T,
Nakazawa T,
et al.
(2012) Evaluation of the effects of acupuncture on blood flow in humans with ultrasound color Doppler imaging. Evid Based Complement Alternat Med 2012:513638.
OpenUrl PubMed

[123] Takayama S,

[124] Watanabe M,

[125] Kusuyama H,

[126] Nagase S,

[127] Seki T,

[128] Nakazawa T,

[129] et al.

[130] ↵
Leinster DA,
Kulbe H,
Everitt G,
Thompson R,
Perretti M,
Gavins FN,
et al.
(2012) The peritoneal tumor microenvironment of high-grade serous ovarian cancer. J Pathol 227:136–145.
OpenUrl CrossRef PubMed Web of Science

[131] Leinster DA,

[132] Kulbe H,

[133] Everitt G,

[134] Thompson R,

[135] Perretti M,

[136] Gavins FN,

[137] et al.

[138] ↵
Huang W,
Cen S,
Kang XL,
Wang WF,
Wang Y,
Chen X
(2015) Doppler ultrasound measurement of resistance index in the diagnosis of prostate cancer. Tumor 101:644–649.
OpenUrl

[139] Huang W,

[140] Cen S,

[141] Kang XL,

[142] Wang WF,

[143] Wang Y,

[144] Chen X

[145] ↵
Shah CA,
Lowe KA,
Paley P,
Wallace E,
Anderson GL,
McIntosh MW,
et al.
(2009) Influence of ovarian cancer risk status on the diagnostic performance of the serum biomarkers mesothelin, HE4, and CA125. Cancer Epidemiol Biomarkers Prev 18:1365–1372.
OpenUrl Abstract/FREE Full Text

[146] Shah CA,

[147] Lowe KA,

[148] Paley P,

[149] Wallace E,

[150] Anderson GL,

[151] McIntosh MW,

[152] et al.

[153] ↵
Lee S,
Choi S,
Lee Y,
Chung D,
Hong S,
Park N
(2017) Role of human epididymis protein 4 in chemoresistance and prognosis of epithelial ovarian cancer. J Obstet Gynaecol Res 43:220–227.
OpenUrl CrossRef

[154] Lee S,

[155] Choi S,

[156] Lee Y,

[157] Chung D,

[158] Hong S,

[159] Park N

[160] ↵
Schäberle W,
Leyerer L,
Schierling W,
Pfister K
(2016) Ultrasound diagnostics of renal artery stenosis: Stenosis criteria, CEUS and recurrent in-stent stenosis. Gefasschirurgie 21:4–13.
OpenUrl

[161] Schäberle W,

[162] Leyerer L,

[163] Schierling W,

[164] Pfister K

[165] ↵
Maxim AR,
Badea R,
Tamas A,
Traila A
(2013) Contrast-enhanced ultrasound in ovarian tumors - diagnostic parameters: method presentation and initial experience. Clujul Med 86:31–35.
OpenUrl

[166] Maxim AR,

[167] Badea R,

[168] Tamas A,

[169] Traila A

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Clinical value of combining transvaginal contrast-enhanced ultrasonography with serum human epididymisprotein-4 and the resistance index for early-stage epithelial ovarian cancer

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Clinical value of combining transvaginal contrast-enhanced ultrasonography with serum human epididymisprotein-4 and the resistance index for early-stage epithelial ovarian cancer

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