Association between transabdominal uterine artery Doppler and small-for-gestational-age: a systematic review and meta-analysis

Zhi, Ruijuan; Tao, Xiangping; Li, Qingtao; Yu, Ming; Li, Honge

doi:10.1186/s12884-023-05968-w

Table 1 Characteristics of included studies

From: Association between transabdominal uterine artery Doppler and small-for-gestational-age: a systematic review and meta-analysis

Author	Year	Country	Study design	Group	Sample size	Age (years)	BMI (kg/m2)	Birth weight (g)	GA (weeks)	Complications	Smoking (number)	Doppler time (weeks)	QA
Arakaki	2020	Japan	Cohort	SGA (early-onset)	28	34 (20, 43)^a	19.9 (16.3, 25.0)^a	2298 (805, 2637)^a	38w6d (28w4d, 40w5d)^a	PIH	NA	11–13 weeks	7
				SGA (late-onset)	73	34 (22, 44)^a	19.6 (15.8, 27.7)^a	2493 (1703, 2943)^a	39w4d (33w6d, 41w4d)^a	PIH
				Non-SGA	1261	34 (18, 52)^a	20.1 (15.4, 43.8)^a	3032 (737, 4483)^a	39w2d (24w4d, 41w6d)^a	PIH
Arrue	2017	Spain	Cohort	Normal UtA	385	31.6 ± 4.6	23.03 ± 3.7	3293.8 ± 431.0	39.5 ± 1.4	NA	NA	Third trimester	8
				Abnormal UtA	56	32.7 ± 3.9	24.4 ± 4.5	3033.37 ± 689.7	38.5 ± 2.2	NA	NA	Third trimester	8
Borna	2019	Iran	Cohort	SGA	11	28(17, 43)^a	NA	3069.88 (1200, 4100)^a	NA	Severe hypertension, non-severe hypertension	NA	18–22 weeks	6
				Non-SGA	97	28(17, 43)^a	NA	3069.88 (1200, 4100)^a	NA	Severe hypertension, non-severe hypertension	NA	18–22 weeks	6
Carter	2015	USA	Cohort	Abnormal UtA	1192	31.5 (17–49)^a	26.4 (15.50, 67.67)^a	NA	NA	Preeclampsia, early preeclampsia, chronic hypertension, pregestational diabetes mellitus	NA	11–14 weeks	7
				Normal UtA	1192	31.5 (17–49)^a	26.4 (15.50, 67.67)^a	NA	NA		NA	11–14 weeks	7
Ciobanu	2019	UK	Cohort	SGA	1012	31.7 (27.2, 35.4)^b	NA	NA	36.1 (35.9, 36.4)^b	Chronic hypertension, diabetes mellitus type 1, diabetes mellitus type 2	NA	35–36 weeks	6
				Non-SGA	8592	32.2 (28.1, 35.7)^b	NA	NA	36.1 (35.9, 36.4) ^b	Chronic hypertension; diabetes mellitus type 1, diabetes mellitus type 2	NA	35–36 weeks	6
Drouin	2018	Canada	Cohort	SGA	486	28.9 (26.5, 31.5)^b	23.2 (21.4, 26.1)^b	2748 (2542, 2894)^b	39.7 (38.9, 40.6)^b	Chronic hypertension, diabetes mellitus; rheumatoid disease	NA	11–13 weeks	6
				Non-SGA	4149	28.7 (26.1, 31.3)^b	23.8 (21.7, 27.1)^b	3368 (3118, 3644)^b	39.9 (39.0, 40.7)^b	chronic hypertension, diabetes mellitus, rheumatoid disease	NA	11–13 weeks	6
Dugoff	2005	USA	Cohort	Abnormal UtA	1008	33 ± 5	23.3 ± 4.0	NA	38.8 ± 2	NA	61	10–14 weeks	7
				Normal UtA	1008	33 ± 5	23.3 ± 4.0	NA	38.8 ± 2	NA	61	10–14 weeks	7
El-Hamedi	2005	UK	Cohort	Abnormal UtA	98	NA	NA	NA	NA	NA	NA	Second trimester	5
				Normal UtA	232	NA	NA	NA	NA	NA	NA	Second trimester	5
Espinoza	2010	USA	Cohort	SGA	396	24 (15, 46)^a	NA	2770 (550, 3070)^a	39.3 (27.4, 41.9)^a	Preeclampsia	55	23–25 weeks	8
				Non-SGA	3153	26 (13, 46)^a	NA	3450 (870, 5350)^a	39.6 (25.6, 43)^a	Preeclampsia	334	23–25 weeks	8
Ghi	2010	Italy	Cohort	Abnormal UtA	62	33.67 ± 5.34	21.66 ± 1.70	2408 ± 763	36.20 ± 3.45	NA	NA	26–28 weeks	6
				Normal UtA	42	32.64 ± 5.75	21.85 ± 1.97	3116 ± 463	38.59 ± 1.76	NA	NA	26–28 weeks	6
González-González	2017	Spain	Cohort	SGA	193	30.45 ± 6.37	26.4 ± 5.72	2421.1 ± 529.6	38.8 ± 3.3	Pregestational diabetes, chronic hypertension	64	11–13 weeks	7
				Non-SGA	795	31.11 ± 5.78	26.3 ± 5.29	3318.4 ± 520.9	39.5 ± 1.9	Pregestational diabetes, chronic hypertension	150	11–13 weeks	7
Groom	2009	New Zealand	Cohort	Normal UtA	2189	28.4 ± 5.7	25.2 ± 5.2	3403 ± 561	39.9 ± 1.9	NA	219 (at 15-wk visit); 227 (in pregnancy)	20–24 weeks	6
				Normal + abnormal UtA
				Abnormal + normal UtA
Hafner	2006	Austria	Cohort	SGA	2489	29.2 ± 5.2	23.7 ± 4.6	NA	NA	NA	NA	21–23 weeks	9
				Non-SGA	2489	29.2 ± 5.2	23.7 ± 4.6	NA	NA	NA	NA	21–23 weeks	9
He	2021	China	Cohort	SGA	76	29.6 ± 3.4	22.8 ± 1.5	1830 (920–2990)^a	34.0 (28.0–39.1)^a	Gestational diabetes mellitus, preeclampsia	NA	11–13 weeks	9
				Non-SGA	1720	30.5 ± 3.9	24.7 ± 1.7	3300 (2370–4640)^a	39.0 (36.0–41.0)^a	Gestational diabetes mellitus, preeclampsia	NA	11–13 weeks	9
Hershkovitz	2005	UK	Cohort	Normal UtA	55	NA	NA	3080(828, 4460)^a	39 (27, 42)^a	Preeclampsia	NA	20–24 weeks	7
				Abnormal UtA (unilateral)	11	NA	NA	2300(1282, 3820)^a	37 (32, 39.5)^a	Preeclampsia	NA
				Abnormal UtA (bilateral)	22	NA	NA	1892(828, 3610)^a	35 (27, 40)^a	Preeclampsia	NA
Kienast	2016	Germany	Cohort	SGA	40	25.8 ± 7.1	23 ± 1.7	2288.6 ± 479.1	36.6 ± 3.8	Chronic hypertension, systemic lupus erythematosus	NA	18–25 weeks	9
				Non-SGA	306	24.4 ± 5.0	22.9 ± 2.4	3088.6 ± 404.0	38.6 ± 2.7	Chronic hypertension, Systemic lupus erythematosus	NA	18–25 weeks	9
Konchak	1995	USA	Cohort	Normal UtA	103	27.1 ± 5.1	NA	3086 ± 690.8	NA	NA	NA	17–22 weeks	7
				Abnormal UtA	103	27.1 ± 5.1	NA	3086 ± 690.8	NA	NA	NA	17–22 weeks	7
Lobmaier	2021	Germany	Cohort	SGA	149	32.1 ± 4.5	22.5 ± 3.3	2630 ± 360	39.9 ± 1.2	PIH/PE, autoimmune disease, history of SGA	12	Third trimester	7
				Non-SGA	143	32.2 ± 4.3	22.0 ± 2.7	3488 ± 369	38.7 ± 1.3	PIH/PE, autoimmune disease, history of SGA	4	Third trimester	7
Maged	2017	Egypt	Cohort	Non-SGA	297	27.37 ± 3.66	24.49 ± 2.04	3277.07 ± 243.06	38.84 ± 1.98	NA	41	18–22 weeks	8
				SGA	52	28.54 ± 3.05	24.5 ± 2.15	2466.54 ± 306.1	37.35 ± 1.47	NA	18	18–22 weeks	8
Maroni	2011	Italy	Cohort	Abnormal UtA	66	34.42 ± 4.44	23.81 ± 2.82	2942 ± 583	38.2 ± 1.64	Late-onset pre-eclampsia	NA	34 weeks	7
				Normal UtA	66	34.12 ± 4.12	23.36 ± 2.38	3404 ± 469	38.9 ± 1.3	Late-onset pre-eclampsia	NA	34 weeks	7
McCowan	2010	New Zealand	Cohort	SGA	376	28.3 ± 5.9	26.2 ± 6.0	2573 ± 605	38.7 ± 3.8	NA	72	20 weeks	9
				Non-SGA	3137	28.1 ± 5.8	25.4 ± 5.1	3487 ± 514	39.6 ± 2.0	NA	315	20 weeks	9
Miranda	2017	Spain	Case–control	SGA	175	32 ± 5	22.4 ± 3.7	2421 ± 570	38.4 ± 2.8	Chronic hypertension, autoimmune disease, previous history of SGA	26	32–36 weeks	8
				Non-SGA	875	31 ± 5	22.8 ± 4.1	3381 ± 396	39.7 ± 1.3	Chronic hypertension, autoimmune disease, previous history of SGA	75	32–36 weeks	8
Mitsui	2016	Japan	Cohort	Abnormal UtA	24	33.3 ± 6.2	24.3 ± 5.8	2450.4 ± 768.1	37.6 ± 3.1	PIH	NA	Second trimester	7
				Normal UtA	13	34.3 ± 5.6	29.1 ± 6.4	2982.0 ± 576.6	39.3 ± 1.6	PIH	NA	Second trimester	7
Miyakoshi	2001	Japan	Cohort	Abnormal UtA	28	32.6 ± 4.16	NA	2,934 ± 417.3	38.9 ± 1.8	PIH	NA	21–24 weeks	8
				Normal UtA	331	32.6 ± 4.16	NA	2,934 ± 417.3	38.9 ± 1.8	PIH	NA	21–24 weeks	8
Običan	2020	USA	Cohort	Abnormal UtA	200	27 (23, 31) ^b	25 (20.9, 31.4) ^b	NA	NA	Chronic hypertension,	20	Third trimester	6
				Normal UtA	200	27 (23, 31) ^b	25 (20.9, 31.4) ^b	NA	NA	Chronic hypertension,	20	Third trimester	6
Ohkuchi	2000	Japan	Cohort	SGA	15	28.1 ± 3.7	NA	2438 ± 276	39.6 ± 1.5	NA	NA	16–23 weeks	8
				Non-SGA	264	28.7 ± 4.0	NA	3105 ± 744	39.1 ± 2.2	NA	NA	16–23 weeks	8
Paules	2019	Spain	Case–control	Non-SGA	202	33.6 (30.5, 36.5)^b	22.8 (20.5, 25.3)^b	3020 (2510, 3420) ^b	39.0 (35.7, 40.1) ^b	Chronic hypertension, pregestational diabetes	23	35–37 weeks	7
				SGA	184	33.4 (29.0, 36.4)^b	21.6 (19.8, 23.4)^b	2337 (1935, 2613)^b	37.7 (37.0, 39.4)^b	Chronic hypertension, pregestational diabetes	48	35–37 weeks	7
Phupong	2003	Thailand	Cohort	Abnormal UtA	58	26.4 ± 4.8	NA	NA	NA	preeclampsia	NA	22–28 weeks	5
				Normal UtA	264	26.4 ± 4.8	NA	NA	NA	preeclampsia	NA	22–28 weeks	5
Quant	2016	USA	Cohort	SGA	40	31 (27–35)^b	26.0 ± 7.01	NA	NA	Chronic hypertension	NA	18–24 weeks	7
				Non-SGA	333	31 (27–35)^b	26.0 ± 7.01	NA	NA	Chronic hypertension	NA	18–24 weeks	7
Rial-Crestelo	2019	Spain	Cohort	SGA	155	34 ± 5.1	23 ± 3.6	2733 ± 250	40 ± 1.3	Maternal disease, previous FGR	25	32–34 weeks	9
				Non-SGA	875	34 ± 5.4	24 ± 4	3423 ± 384	40 ± 1.3	Maternal disease, previous FGR	79	32–34 weeks	9
Rodríguez	2018	Chile	Cohort	Abnormal UtA	33	28.2 ± 7.47	34.5 ± 5.02	2533 ± 561.3	36.4 (35.7, 37.7)^b	Chronic hypertension, systemic lupus erythematosus, diabetes mellitus type-2	0 (0)	34 weeks	7
				Normal UtA	53	26.0 ± 7.04	32.7 ± 5.47	3227 ± 447.9	38 (37.0, 38.1)^b	Chronic hypertension, systemic lupus erythematosus, diabetes mellitus type-2	3	34 weeks	7
Roeder	2014	USA	Cohort	Normal UtA	108	32.2 ± 5.3	24.2 (22.1, 27.8)^b	NA	NA	Prior preeclampsia, chronic hypertension, prior IUGR, pregestational diabetes	NA	24–26 weeks	6
				Abnormal UtA	24	32.2 ± 5.3	24.2 (22.1, 27.8)^b	NA	NA		NA	24–26 weeks	6
Rueangjaroen	2021	Thailand	Cohort	SGA	24	29.5 ± 5.2	23.4 ± 4.3	2256 ± 551	37.3 ± 2.8	NA	NA	11–14 weeks; 18–22 weeks	8
				Non-SGA	311	29.7 ± 5.1	23.1 ± 4.5	3076 ± 455	38.2 ± 2.1	NA	NA	11–14 weeks; 18–22 weeks	8
Schwartz	2014	USA	Cohort	SGA	56	29.6 ± 5.8	26.2 ± 7.7	NA	NA	Chronic hypertension	9	11–14 weeks	9
				Non-SGA	522	30.8 ± 5.8	27.1 ± 6.8	NA	NA	Chronic hypertension	48	11–14 weeks	9
Seravalli	2014	USA	Cohort	SGA	172	28 (22, 35)^b	27.5 (23.5, 34.4)^b	NA	NA	History of diabetes, history of preeclampsia, history of hypertension, prior IUGR	NA	18–22 weeks	7
				Non-SGA	1810	30 (24, 35)^b	27.6 (24.2, 32.6)^b	NA	NA	history of diabetes, history of preeclampsia, history of hypertension, prior IUGR	NA	18–22 weeks	7
Shwarzman	2013	Israel	Cohort	Normal UtA	144	29.35 ± 5.8	NA	NA	34.33 ± 2.99	Diabetes mellitus, hypertensive disorders	NA	34–37 weeks	8
				Abnormal UtA (unilateral pathologic waveforms)	37	27 .30 ± 6.44	NA	NA	34.08 ± 2.80	Diabetes mellitus, hypertensive disorders	NA
				Abnormal UtA (bilateral pathologic waveforms)	17	30.12 ± 5.3	NA	NA	34.33 ± 3.70	Diabetes mellitus, hypertensive disorders	NA
Triunfo	2017	Spain	Case–control	SGA	46	32.4 ± 4.7	23.9 ± 3.1	2215.1 ± 576.9	37.4 ± 3.1	Chronic hypertension, gestational diabetes, autoimmune disease, coagulation disorders, neurological disorders, endocrinological disorders	23 (< 10 cigarettes/day); 12 (≥ 10 cigarettes/day)	First trimester; Second trimester; Third trimester	8
				Non-SGA	92	31.7 ± 4.8	24.0 ± 3.5	3374.2 ± 404.2	39.7 ± 1.2	Chronic hypertension, gestational diabetes, autoimmune disease, coagulation disorders, neurological disorders, endocrinological disorders	< 10 cigarettes/day: 8(8.7%);≥ 10 cigarettes/day: 6(6.5%)	First trimester; Second trimester; Third trimester	8
Valiño	2016	UK	Cohort	SGA	379	37.7 (26.9, 35.3)^b	NA	NA	40.0 (39.1, 40.9)^b	Chronic hypertension, diabetes mellitus, SLE/APS	365	35–37 weeks	8
				Non-SGA	3509	37.7 (26.9, 35.3)^b	NA	NA	40.0 (39.1, 40.9)^b	Chronic hypertension, diabetes mellitus, SLE/APS	365	35–37 weeks	8
Ventura	2015	Peru	Cohort	Abnormal UtA	91	33 (28, 36)^b	NA	2840 (2370, 3320)^b	39 (37, 40)^b	Hypertension, diabetes mellitus	32	28 weeks	8
				Normal UtA	174	33 (28, 36)^b	NA	3090 (2795, 3400)^b	39 (38, 40)^b	Hypertension, diabetes mellitus	32	28 weeks	8
Viola	2014	USA	Cohort	SGA	191	28 (22, 35)^b	26.1 (22.9, 33.7)^b	2605 (2281, 2736)^b	39 (37.4, 40)^b	Diabetes, hypertension, prior preeclampsia, prior IUGR	28	11–14 weeks	8
				Non-SGA	2076	30 (25, 35)^b	26.6 (23.1, 32)^b	3320 (3045, 3604)^b	39.3 (38.3, 40)^b	Diabetes, hypertension, prior preeclampsia, prior IUGR	192	11–14 weeks	8
Zarean	2018	Iran	Cohort	Normal UtA	60	30.53 ± 5.51	NA	3236.50 ± 592.64	37.93 ± 1.96	Preeclampsia, gestational diabetes, hypertension, hypertension with preeclampsia	NA	30–34 weeks	7
				Abnormal UtA	40	28.50 ± 6.03	NA	2422.75 ± 473.95	36.49 ± 2.51	Preeclampsia, gestational diabetes, hypertension, hypertension with preeclampsia	NA	30–34 weeks	7

Abbreviation: BMI body mass index, GA gestational age, QA quality assessment, SGA small-for-gestational age, PIH pregnancy-induced hypertension, NA not applicable, UtA uterine artery Doppler, GH gestational hypertension, PE pre-eclampsia
^a Data are presented as the median (range)
^bData are presented as the median (IQR)

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