Neither soyfoods nor isoflavones warrant classification as endocrine disruptors: a technical review of the observational and clinical data

Figures & data

Table 1. Isoflavone intake in infants using soy infant formula and free-living Asian children and adolescents.

Group/Reference	N	Age (y) Mean ± SD or range	Country	Isoflavone exposure
				Intake (mg/d)	mg/kg/bw
Infants (Setchell et al. 1997, 1998)		4 months	US	28–47	6–9
Infants UK COT^a		0–4 months	UK		2.4–9.5
Infants UK COT^a		>4–6 months	UK		1.– 7.2
Boys (Wada et al. 2011)	230	5.12 ± 0.89	Japan	12.2	0.70
Girls (Wada et al. 2011)	198	5.14 ± 0.90	Japan	11.4	0.66
Boys/Girls (Surh et al. 2006)	NI	1–2	Korea	14.5	NC^b
Boys/Girls (Surh et al. 2006)	NI	3–6	Korea	8.9	NC
Boys/Girls (Surh et al. 2006)	NI	7–12	Korea	12.4	NC
Boys/Girls (Surh et al. 2006)	NI	13–19	Korea	10.1	NC
Boys/Girls (Hsiao and Lyons-Wall 2000)	66	8–9	Taiwan	36.6	1.13
Children/Adolescents (Hu et al. 2014)	174	0–14	China		0.53
Children (Messina, Nagata, and Wu 2006; Kato et al. 2014)	NI	1–6	Japan	∼14	∼1.0 ^c
Adolescents (Messina, Nagata, and Wu 2006; Hatena Blog)	NI	7–14	Japan	∼20	0.54^d

^a Estimates based on an isoflavone concentration of SIF of 18.0 to 46.7 mg/l and an intake of 800 or 1200 ml/d.

^b NC, not calculated.

^c 14 kg as bw.

^d 37 kg used as bw.

Table 2. Isoflavone intake reported in large prospective epidemiologic studies from China and Japan.

Sex/Ref.	Assumed bw (kg)	N	Age (y) range	Country	Isoflavone intake, mg/kg bw
					Intake quartile
					1	2	3	4
Men (Gu et al. 2006; Yu et al. 2014)	61 (Gu et al. 2006)	55,474	40-74	China	0.22	0.42	0.62	0.96
Men (Hara et al. 2012; Matsushita et al. 2008)	62.5 (Matsushita et al. 2008)	39,569	40-69	Japan	0.23	0.45	0.68	1.26
Women (Hara et al. 2012; Matsushita et al. 2008)	54 (Matsushita et al. 2008)	45,312	40-69	Japan	0.27	0.52	0.79	1.43
					Intake percentile
					Mean	8.8	51	28.1	10	2.2
Women (Yang et al. 2005; Ma et al. 2013)	61.4 (Ma et al. 2013)	45,694	40-70	China	0.66^4	0.12	0.43	0.87	1.39	2.37

Table 3. Selected examples of isoflavone exposure in intervention trials of at least approximately 2 years duration.

Sex	N	Age (y) Mean ± SD or 95% CI	Country	Duration	Isoflavone exposure
					mg/d	mg/kg/bw
Women (Hodis et al. 2011)	76	60.8 ± 7.2	US	3 years	91	1.31
Women (Alekel et al. 2010)	73	54.7 (52.0, 56.9)	US	3 years	120	1.80
Women (Tai et al. 2012)	200	55.8 ± 3.6	Taiwan	96 weeks	300	5.46
Women (Unfer et al. 2004)	154	49 ± 4.3	Italy	5 years	150	2.24* 1.34**
Men (Bosland et al. 2013)	53	61.3 ± 7.2	US	2 years	41	0.47
Men (Fleshner et al. 2011)	153	62.5	Canada	3 years	100	1.20

* Assumed dose refers to aglycone equivalent weight (unclear from text).

** Assumed dose refers to glycoside weight (unclear from text).

Table 4. Serum isoflavone levels in native Japanese adults.

Author/Year/Reference		Genistein (nmol/l)				Daidzein (nmol/l)
	Sex/N	Mean	SD	Median	IQR*	Mean	SD	Median	IQR*
Nagata 2016 (Nagata et al. 2016)	M/56			317	146, 685			112	177, 268
Otokozawa 2015 (Otokozawa et al. 2015)
Minatoya 2015 (Minatoya et al. 2015)				185	75, 530			87	28, 266
Premenopausal	F/31	411	729			197	431
Postmenopausal	F/45	428	508			328	540
Michikawa 2015 (Michikawa et al. 2015)	M/121^c			239	116, 601			108	39, 263
	F/54^c			165	63, 608			85	21, 256
Sugiyama 2014 (Sugiyama et al. 2014)	M/28			219	118, 418			76	34, 124
Hara 2013 (Hara et al. 2013)	M/71, 81			826^a				111^a
	F/34, 39			710^a				102^a
Hozawa 2013 (Hozawa et al. 2013)	M/73, F/104				538, 996^d				302, 502^d
Shimazu 2011 (Shimazu et al. 2011)	F/252			268	110, 470			125	46, 242
Kurahashi 2008 (Kurahashi et al. 2008)	M/402			319	145, 722			140	55, 320
Fujimoto 2008 (Fujimoto et al. 2008)
Japanese	M/18^b	408	372	274	27, 1324	229	207	124	8, 593
Korean	M/20^b	429	423	229	28, 1512	379	780	142	15, 3676
Iwasaki 2008 (Iwasaki et al. 2008)	F/288			535	292, 946			70	22, 160
Nagata 2006 (Nagata et al. 2006)	F/194^e	117				50
Zhao 2006 (Zhao et al. 2006)	F/129	617	808	376	545	166	199	109	177
Takashima 2004 (Takashima et al. 2004)
Equol producers Non-producers	M/41			290	40, 2110			50	28, 1522
	M/47			262	27, 1432			78	11, 502
Ozasa 2004 (Ozasa et al. 2004)	M/151	368			185, 850	139			64, 320
Akaza 2004 (Akaza et al. 2004)	M/162			313				96
Morton 2002 (Morton et al. 2002)	M/102	493	601	288		283	375	149
	F/125	502	718	234		247	370	110
Nagata 2002 (Nagata et al. 2002)	F/87	414	644			162	204
Yamamoto 2001 (Yamamoto et al. 2001)	M,F/202	475	510			120	136
Adlercreutz 1993 (Adlercreutz, Markkanen, and Watanabe 1993)	M/14	276			116, 652	107			47, 237

* Interquartile range ^aMedian for third tertile ^bAged 50–59 years ^cSubjects with hepatitis virus infection ^dRange for third tertile ^eConcentration at delivery. For studies reporting values for cases and controls, only the latter were used.

Table 5. Serum isoflavone levels in men in response to varying isoflavone doses (Busby et al. 2002).

Formulation	Dose (mg/kg bw)		Genistein (µM)		Daidzein (µM)
	Genistein	Daidzein	Unconjugated	Total	Unconjugated	Total
A	1.0	0.11		0.929 ± 0.088
A	2.0	0.22		2.095 ± 0.451
A	4.0	0.44		4.418 ± 2.502		0.583 ± 0.279
A	8.0	0.89	0.131 ± 0.021	8.037 ± 2.203		0.906 ± 0.228
A	16.0	1.8	0.066 ± 0.031	7.594 ± 1.384		1.315 ± 0.057
B	1.0	0.49	0.074	2.729 ± 1.710	0.060	1.429 ± 0.767
B	2.0	0.98	0.069 ± 0.033	5.492 ± 1.516	0.040 ± 0.010	2.221 ± 0.640
B	4.0	2.0	0.084 ± 0.014	9.479 ± 2.053	0.070 ± 0.012	4.857 ± 0.384
B	8.0	3.9	0.258 ± 0.134	17.87 ± 2.426	0.139 ± 0.027	7.678 ± 1.961
B	16.0	7.8	0.363 ± 0.213	27.46 ± 15.38	0.315 ± 0.261	16.94 ± 8.711

Table 6. Mean (SD) of serum genistein and daidzein concentrations at each visit among postmenopausal women from three medical centers in Taiwan participating in a 2-year clinical trial in which participants received either 300 mg/d isoflavones or a placebo (Tai et al. 2012).

	µmol/l/(n)
	Week 0	Week 4	Week 48	Week 96
Genistein
Isoflavone	0.34 ± 1.26/212)	6.85 ± 5.05/(210)	4.10 ± 4.34/(204)	3.30 ± 3.18/(200)
Placebo	0.23 ± 0.74/(211)	0.19 ± 0.71/(210)	0.20 ± 0.67/(203)	0.24 ± 0.80/(198)
Daidzein
Isoflavone	0.09 ± 0.36/(212)	1.44 ± 1.35/(212)	1.12 ± 1.16/(204)	0.73 ± 0.92/200
Placebo	0.05 ± 0.20/(211)	0.07 ± 0.35/(211)	0.10 ± 0.48/(203)	0.04 ± 0.23/(199)

Blood samples taken after an overnight fast.

Table 7. Relative binding affinity of isoflavones in comparison to estrogen (Kuiper et al. 1998).

Compound	RBA^a		RBA^b
	ERα	ERβ	ERα	ERβ
17β-estradiol	100	100	100	100
Genistein	4	87	0.7	13
Daidzein	0.1	0.5	0.2	1.0

^a Determined from solid-phase (Scintistrip) competition experiments.

^b Determined from solubilized receptor competition experiments Affinities are expressed as RBA values where the affinity of E2 for ERα or ERβ was set at 100%.

Table 8. RBA of isoflavones for ERα and ERβ and comparison with E2 (Jiang et al. 2013).

Compound	RBA (ERα)	RBA (ERβ)	β/α
17β-estradiol	100	100	1.0
Genistein	0.021	6.80	324
Daidzein	0.003	0.051	17
S-Equol	0.144	3.50	24

Binding affinities for human full-length ERα and ERβ were determined by

^a Radiometric competitive binding assay using tritiated 17β-E2 as tracer and E2 as standard.

Table 9. Search strategy.

Database and Search Period	MEDLINE Through January 2021	Embase Through January 2021	The Cochrane Library Through January 2021
Keywords	Soy.mp. Isoflavone.mp. soy isoflavones.mp. exp Isoflavones/ exp Soybeans/ soy protein.mp. exp Soybean Proteins/ exp Soy Foods/ exp Soy Milk/ (soy adj3 milk).mp. soybeans.mp. (soy adj3 bean$).mp. soy food$.mp. (soy adj3 beverage$).mp. or/1-14 Endocrine.mp. exp Reproductive Health/ exp Fertility/ (reproductive adj3 hormone$).mp. exp Spermatozoa/ exp Semen/ semen.mp. exp Prenatal Exposure Delayed Effects/ in utero.mp. exp Hypospadias/ hypospadias.mp. exp Menstrual Cycle/ menstrual cycle.mp. exp Leiomyoma/ (uterine adj3 fibroid$).mp. exp Endometriosis/ endometriosis.mp. exp Endometrial Neoplasms/ endometrial cancer.mp. exp Lactation/ exp Lactation Disorders/ lactation.mp. exp Breast Feeding/ (breast adj3 feeding).mp. exp Breast Neoplasms/ (breast adj3 cancer).mp. exp Sexual Maturation/ exp Puberty/ (puberty adj3 onset).mp. exp Growth Disorders/ exp Adrenal Insufficiency/ exp Pituitary-Adrenal System/ (adrenal adj3 function).mp. exp Thyroid Gland/ thyroid.mp. exp Mucocutaneous Lymph Node Syndrome/ (kawasaki adj3 disease).mp. or/16-52 15 and 53 limit 54 to animals 54 not 55 "randomized controlled trial".pt. (random$ or placebo$ or single blind$ or double blind$ or triple blind$).ti,ab. (retraction of publication or retracted publication).pt. or/57-59 (animals not humans).sh. ((comment or editorial or meta-analysis or practice-guideline or review or letter or journal correspondence) not "randomized controlled trial").pt. (random sampl$ or random digit$ or random effect$ or random survey or random regression).ti,ab. not "randomized controlled trial".pt. or/61-63 60 not 64 exp cohort studies/ cohort$.tw. controlled clinical trial.pt. epidemiologic methods/ limit 69 to yr = 1966-1989 exp case-control studies/ (case$ and control$).tw. (case$ and series).tw. case reports.pt. (case$ adj2 report$).tw. (case$ adj2 stud$).tw. or/66-68,70-76 meta-analysis.pt. meta-analysis.sh. (meta-analys$ or meta analys$ or metaanalys$).tw,sh. (systematic$ adj5 review$).tw,sh. (systematic$ adj5 overview$).tw,sh. (quantitativ$ adj5 review$).tw,sh. (quantitativ$ adj5 overview$).tw,sh. (quantitativ$ adj5 synthesis$).tw,sh. (methodologic$ adj5 review$).tw,sh. (methodologic$ adj5 overview$).tw,sh. (integrative research review$ or research integration).tw. or/78-88 65 or 77 or 89 56 and 90 89 or 76	Soy.mp. Isoflavone.mp. soy isoflavones.mp. exp isoflavone/ exp soybean/ (soy adj3 beans).mp. soy protein.mp. exp soybean protein/ exp soy food/ exp tofu/ miso.mp. exp soybean milk/ exp fermented soybean/ soybeans.mp. or/1-14 Endocrine.mp. exp reproductive health/ exp fertility/ (reproductive adj3 hormone$).mp. exp spermatozoon/ exp sperm/ semen.mp. exp Prenatal Exposure/ in utero.mp. exp hypospadias/ hypospadias.mp. exp menstrual cycle/ menstrual cycle.mp. exp leiomyoma/ (uterine adj3 fibroid$).mp. exp endometriosis/ endometriosis.mp. exp endometrium cancer/ endometri$ cancer.mp. exp lactation/ exp lactation disorder/ lactation.mp. exp breast feeding/ (breast adj3 feeding).mp. exp breast cancer/ (breast adj3 cancer).mp. exp puberty disorders/ (puberty adj3 onset).mp. exp growth disorder/ exp adrenal insufficiency/ exp adrenal function/ (adrenal adj3 function).mp. exp thyroid gland/ thyroid.mp. exp mucocutaneous lymph node syndrome/ (kawasaki adj3 disease).mp. or/16-51 15 and 52 limit 53 to human (random$ or placebo$ or single blind$ or double blind$ or triple blind$).ti,ab. RETRACTED ARTICLE/ or/55-56 (animal$ not human$).sh,hw. (book or conference paper or editorial or letter or review).pt. not exp randomized controlled trial/ (random sampl$ or random digit$ or random effect$ or random survey or random regression).ti,ab. not exp randomized controlled trial/ or/58-60 57 not 61 exp cohort analysis/ exp longitudinal study/ exp prospective study/ exp follow up/ cohort$.tw. exp case control study/ (case$ and control$).tw. exp case study/ (case$ and series).tw. case report/ (case$ adj2 report$).tw. (case$ adj2 stud$).tw. or/63-74 exp review/ (literature adj3 review$).ti,ab. exp meta analysis/ exp "Systematic Review"/ or/76-79 (medline or medlars or embase or pubmed or cinahl or amed or psychlit or psyclit or psychinfo or psycinfo or scisearch or cochrane).ti,ab. RETRACTED ARTICLE/ 81 or 82 80 and 83 (systematic$ adj2 (review$ or overview)).ti,ab. (meta?anal$ or meta anal$ or meta-anal$ or metaanal$ or metanal$).ti,ab. 84 or 85 or 86 62 or 75 or 87 54 and 88	Soy.mp. Isoflavone.mp. soy isoflavones.mp. exp Isoflavones/ exp Soybeans/ (soy adj3 bean$).mp. exp Soybean Proteins/ soy protein.mp. exp Soy Foods/ exp Soy Milk/ (soy adj3 milk).mp. soy food$.mp. (soy adj3 beverage$).mp. or/1-13 Endocrine.mp. exp Reproductive Health/ exp Fertility/ (reproductive adj3 hormone$).mp. exp Spermatozoa/ exp Semen/ semen.mp. exp Prenatal Exposure Delayed Effects/ in utero.mp. exp Hypospadias/ hypospadias.mp. exp Menstrual Cycle/ menstrual cycle.mp. exp Leiomyoma/ (uterine adj3 fibroid$).mp. exp Endometriosis/ endometriosis.mp. exp Endometrial Neoplasms/ endometrial cancer.mp. exp Lactation/ exp Lactation Disorders/ lactation.mp. exp Breast Feeding/ (breast adj3 feeding).mp. exp Breast Neoplasms/ (breast adj3 cancer).mp. exp Puberty/ Sexual Maturation/ (puberty adj3 onset).mp. exp Growth Disorders/ exp Adrenal Insufficiency/ (adrenal adj3 function).mp. exp Thyroid Gland/ thyroid.mp. exp Mucocutaneous Lymph Node Syndrome/ (kawasaki adj3 disease).mp. or/15-50 15 and 51 limit 52 to embase records 52 not 53

Figure 1. Flow of the literature search and study selection. *1 report included both an SRMA and an observational study (Wei, Y.L., J. Guo, Y. Bian, Z. Gao, M. Du, H. Yang, L. Chen, Y. Zhang, X. Wang, T. Chen, J. Chen, Z. Yu, C. Huo, D. Li, L. China Kadoorie Biobank Collaborative, Group, Soy intake and breast cancer risk: a prospective study of 300,000 Chinese women and a dose-response meta-analysis. European Journal of Epidemiology, 2019. 21: p. 21.). Abbreviation: SRMA-systematic review and meta-analysis.

Table 10. Selected characteristics and results of intervention studies evaluating the effects of isoflavone exposure on breast cell proliferation.

Author (year)	Group	N	Isoflavone dose (mg/d)	Participants	Intervention duration	Measure	Percentage positive cells
							Initial	Final
Hargreaves et al. (1999)	Control	53	0	Healthy premenopausal	14 days (8-14)	Ki67	3.16 ± 3.08^1	6.03 ± 4.27^1
	Soy	28	45				4.76 ± 6.16^1	6.17 ± 7.00^1
Palomares et al. (2004)	Placebo	9	0	Postmenopausal breast cancer survivors	11.7 months	Ki67	NA	−4.1 ± 9.0^1
	Isoflavones	9	100				NA	−4.9 ± 11.5^1
Sartippour et al. (2004)	Placebo	26	0	Postmenopausal breast cancer survivors^2	23 days (13-45)	AI/MI	6.5 ± 7.0^1	4.4 ± 4.7^1
	Isoflavones	17	120				3.3 ± 3.4^1	5.8 ± 8.3^1
Cheng et al. (2007)	Placebo	25	0	Healthy postmenopausal	12 weeks	Ki67	NA	No change
	Isoflavones	26	36				NA	No change
Khan et al. (2012)	Placebo	49	0	At risk pre- and post-menopausal	6 months	Ki67	0.97 (0.70-1.90)^3	0.92 (0.59-1.09)^3
	Isoflavones	49	235				1.17 (0.66-1.93)^3	1.09 (0.75-2.33)^3
Shike et al. (2014)	Control	50	0	Pre- and post-menopausal breast cancer survivors	6 months	Ki67	16.5 (0-80)^4	20.0 (1-72)^4
	Isoflavones	54	62				15.5 (1.6-80)^4	21.0 (4-80)^4

¹Mean ± SD. ²Isoflavone and placebo groups included 12% and 19% premenopausal breast cancer survivors, respectively. ³Median (interquartile range). ⁴Mean (range).

Table 11. Amniotic fluid and umbilical cord concentrations¹ (mean or geometric mean or median) of isoflavones and estrogen.

Author/Location/ Reference	Participant number/ Sampling time (gestation)	Estradiol (nM)	Estriol (nM)	Estrone (nM)
Amniotic Fluid
Hill/Czech Republic/ (Hill et al. 2010)	12/28-41 wk	2.1	90.5	12.3
Adlercreutz/Finland/ (Adlercreutz et al. 1999; Adlercreutz and Luukkainen 1970)	7/At delivery	Unconjugated low Conjugated 5.1	Unconjugated 195 Conjugated 3232	Unconjugated 20.7 Conjugated 29.6
Cho/Korea// (Cho et al. 2006)	22/8–15 wk .		3-sulfate, 18.9 ± 11.2 3-glucuronide, 8.4 ± 3.6 16-glucuronide, 19.8 ± 11.2
van de Beck/USA/ (van de Beek et al. 2004)	75/2^nd trimester 78/2^nd trimester	0.89 ± 0.003 (from males) 1.01 ± 0.004 (from females)
Robinson/USA/ (Robinson et al. 1977)	48 male/14–20 weeks 72 female/14–20 weeks	64 ± 4 pg/ml (M) (235 pM) 96 ± 9 pg/ml (F) (352 pM)		353 ± 33 pg/ml (M) (1306 pM) 331 ± 28 pg/ml (F) (1224 pm)
Cord Levels
Adlercreutz/ (Adlercreutz et al. 1999; Adlercreutz and Luukkainen 1970)	7/At delivery	Unconjugated 27.2 Conjugated 12.4	Unconjugated 475 Conjugated 4369	Unconjugated 89.8 Conjugated 96.9
Nagata/Japan/ (Nagata et al. 2006)	194/Delivery	17.1 nmol/l geometric	7109 nmol/l geometric	Not reported
Troisi/USA /China/ (Troisi et al. 2008)	87, 96/Delivery 110, 120/Delivery	34.4 44.9	541 829
Troisi/USA/ (Troisi et al. 2003)	86/Delivery	34.9	774	113
Shibata/USA/ (Shibata, Harris, and Billings 2002)	57 Caucasian/Delivery 22 Hispanic/Delivery 22 Asian/Delivery	24.7 20.7 27.0		34.1 28.9 43.6
Troisi/USA/ (Troisi et al. 2003)	86/ (38–39 gestation wk)	35.0	0.81	116.5
Faupel-Badger/ (Faupel-Badger et al. 2009)	75/ (2nd tertile for pregnancy wt gain)	32.1	708	121.1
Savarese/USA/ (Savarese et al. 2007)	289/Delivery	34.2	1,149 (unconjugated)
van de Beck/USA/ (van de Beek et al. 2004)	18 mothers with males 18 mothers with females	45.9 ± 4.49 32.4 ± 2.99
Lagiou/USA /Shanghai/ (Lagiou et al. 2011)	92 USA 110 Shanghai	129.9 292.5	1328.6 1411.9
		Genistein	Daidzein	Equol
Cord blood
Adlercreutz/Japan/ (Adlercreutz et al. 1999; Adlercreutz and Luukkainen 1970)	7/Delivery	165	58.8	50.9
Todaka/Japan/ (Todaka et al. 2005)	51/Delivery	71.9	19.9	3.7
Nagata/Japan/ (Nagata, Oba, and Shimizu 2006)	194/Delivery	126.9	38.6	4.2
Dalais/Indonesia (Dalais, Meliala, and Wahlqvist 2000)	30/Delivery	91.7 ± 12.5	33.9 ± 5.62
Jarrell/Canada/ (Jarrell, Foster, and Kinniburgh 2012)	300/2^nd trimester	9.93	9.01
Mustafa/Malaysia/ (Mustafa et al. 2007)	103	57.0	13.8
Amniotic Fluid (nmol/l)
Adlercreutz/Japan/ (Adlercreutz et al. 1999; Adlercreutz and Luukkainen 1970)	7/At delivery	64.0	67.8	68.0
Foster/USA/ (Foster et al. 2002)	53/15-23 wk gestation	6.3	5.7
Engel/USA/ (Engel et al. 2006)	21/<20 wks gestation	5.1	37.5
Jarrell/Canada/ (Jarrell, Foster, and Kinniburgh 2012)	300/2^nd trimester	2.85	2.36

Conversions: Estrone pg/ml × 3.699 = pmol/l, estradiol pg/ml × 3.67 = pmol/l, estriol ng/ml × 3.47 = nmol/l (Robinson et al. 1977).

Table 12. Estrogen and isoflavone concentrations in breast milk and plasma of Korean women (Choi et al. 2002).

	Concentration (ug/l)/nmol/l
Molecule	Breast milk	Plasma
17β-estradiol	7.9–18.5/29.0–67.9	3.5–8.4/12.8–30.8
Genistein	6.3–28.7/23.3–106.2	8.4–86.5/31.1–320.1
Daidzein	3.2–44.9/12.6–176.6	15.3–322/60.2–1266.6

Table 13. Isoflavone concentrations (nmol/L, mean ± SD) in human breast milk samples before (day 1), during (days 3 and 6), and after (day 7) intervention with soy drink (Jochum et al. 2017).

	Study day 1	Study day 4	Study day 7	Study day 8
Daidzein	Not detected	9.3 ± 4.2	9.1 ± 4.8	7.3 ± 3.3
Genistein	Not detected	4.9 ± 7.2	4.3 ± 2.7	3.5 ± 2.3

Detection limit: daidzein: 6.25 nmol/L; genistein: 2.5 nmol/L.

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