Immunohistochemical analysis of adipokine and adipokine receptor expression in the breast tumor microenvironment: associations of lower leptin receptor expression with estrogen receptor-negative status and triple-negative subtype

Llanos, Adana A. M.; Lin, Yong; Chen, Wenjin; Yao, Song; Norin, Jorden; Chekmareva, Marina A.; Omene, Coral; Cong, Lei; Omilian, Angela R.; Khoury, Thaer; Hong, Chi-Chen; Ganesan, Shridar; Foran, David J.; Higgins, Michael; Ambrosone, Christine B.; Bandera, Elisa V.; Demissie, Kitaw

doi:10.1186/s13058-020-1256-3

Table 2 Mean adipokine and adipokine receptor IHC expression, by select factors

From: Immunohistochemical analysis of adipokine and adipokine receptor expression in the breast tumor microenvironment: associations of lower leptin receptor expression with estrogen receptor-negative status and triple-negative subtype

Sociodemographic and clinical characteristics	LEP			LEPR			ADIPOQ			ADIPOR1			ADIPOR2
Sociodemographic and clinical characteristics	n	mean ± SD	P	n	mean ± SD	P	n	mean ± SD	P	n	mean ± SD	P	n	mean ± SD	P
Age at diagnosis (years)			0.53			0.05			0.69			0.11			0.45
20–45	181	112.2 ± 23.8		180	61.9 ± 26.2		200	73.4 ± 37.1		200	94.4 ± 38.5		200	61.8 ± 34.7
45–59	215	111.8 ± 24.2		208	61.2 ± 26.8		231	74.6 ± 35.7		231	95.5 ± 37.6		231	59.0 ± 35.8
60–75	179	109.4 ± 29.3		175	67.4 ± 27.8		189	76.5 ± 34.5		189	101.6 ± 32.6		189	63.2 ± 32.9
Menopausal status			0.41			0.01			0.54			0.54			0.45
Premenopausal	300	111.8 ± 23.4		301	60.2 ± 27.2		325	74.0 ± 35.8		325	95.7 ± 37.5		325	60.0 ± 35.8
Postmenopausal	350	110.2 ± 27.5		339	65.6 ± 26.3		374	75.6 ± 35.2		374	97.4 ± 35.2		374	62.0 ± 34.3
Race			0.51			< 0.0001			0.0003			0.68			0.03
Black/African American	500	110.6 ± 24.0		495	66.3 ± 24.8		540	77.5 ± 34.2		540	97.0 ± 35.8		540	62.7 ± 34.4
White	150	112.1 ± 30.6		145	52.1 ± 30.4		159	65.8 ± 38.3		159	95.6 ± 38.1		159	55.7 ± 36.6
Body mass index (kg/m²)			0.39			< 0.0001			0.36			0.17			0.09
18.5–24.99	163	112.9 ± 25.1		160	55.8 ± 27.6		177	71.0 ± 38.4		177	92.3 ± 40.3		177	54.9 ± 36.2
25.0–29.99	184	108.4 ± 25.1		182	58.9 ± 29.2		201	75.3 ± 33.9		201	98.5 ± 37.0		201	60.5 ± 34.4
30.0–34.99	166	112.0 ± 25.7		161	65.4 ± 26.8		176	77.6 ± 33.8		176	99.8 ± 33.3		176	64.1 ± 35.6
≥ 35.0	156	111.1 ± 26.3		154	71.7 ± 19.9		166	74.0 ± 36.2		166	94.1 ± 35.2		166	61.9 ± 34.4
Breast tumor clinicopathologic features
Tumor grade			0.63			0.27			0.84			0.65			0.07
Well differentiated	99	108.6 ± 29.9		94	65.4 ± 28.4		107	74.2 ± 36.6		107	95.8 ± 42.0		107	56.5 ± 37.5
Moderately differentiated	203	111.3 ± 24.6		199	64.2 ± 27.2		218	72.9 ± 35.9		218	94.9 ± 36.2		218	57.2 ± 35.3
Poorly differentiated	298	111.2 ± 24.8		291	61.1 ± 25.1		309	74.8 ± 35.7		309	63.3 ± 33.6		309	63.3 ± 33.6
Tumor size			0.48			0.08			0.03			0.22			0.003
< 1.0 cm	124	112.4 ± 23.3		129	58.5 ± 33.0		147	81.0 ± 33.4		147	101.0 ± 42.8		147	60.7 ± 36.0
1.0–2.0 cm	265	111.9 ± 25.8		256	65.0 ± 26.5		281	71.5 ± 36.8		281	95.2 ± 36.7		281	55.1 ± 36.1
> 2.0 cm	280	109.6 ± 26.2		272	62.6 ± 23.8		292	74.1 ± 35.1		292	95.0 ± 32.9		292	65.1 ± 33.4
AJCC stage			0.56			0.40			0.44			0.18			0.24
Stage 0	62	111.1 ± 27.7		51	67.3 ± 28.7		61	78.9 ± 34.5		61	91.3 ± 47.4		61	62.7 ± 37.7
Stage I	241	112.1 ± 24.7		237	61.1 ± 29.8		256	75.1 ± 35.0		256	100.9 ± 35.6		256	57.0 ± 35.1
Stage II	256	111.3 ± 23.1		246	64.0 ± 23.6		271	73.9 ± 35.5		271	94.1 ± 35.2		271	61.4 ± 35.5
Stage III	91	106.9 ± 32.7		89	60.1 ± 25.3		96	69.8 ± 37.3		96	95.2 ± 34.2		96	65.1 ± 32.4
Stage IV	6	106.8 ± 25.8		6	55.6 ± 28.6		6	88.6 ± 10.7		6	98.8 ± 10.0		6	45.6 ± 41.7
Lymph node status			0.61			0.30			0.89			0.77			0.07
Negative	372	110.5 ± 26.5		368	61.8 ± 28.6		406	74.1 ± 35.4		406	96.7 ± 37.0		406	59.0 ± 35.2
Positive	252	111.5 ± 25.4		244	64.2 ± 24.0		266	74.4 ± 36.1		266	95.8 ± 35.5		266	64.0 ± 34.4
Ki67 status			0.09			0.12			0.05			0.34			0.64
Ki67−/favorable	326	110.0 ± 23.9		320	68.1 ± 25.5		348	79.0 ± 34.3		348	100.4 ± 37.1		348	61.8 ± 33.8
Ki67+/unfavorable	147	113.8 ± 19.0		143	64.4 ± 22.4		155	72.6 ± 35.4		155	97.1 ± 32.9		155	63.3 ± 35.8
ER status			0.45			< 0.0001			0.61			0.49			0.17
ER−	205	110.1 ± 23.8		198	55.4 ± 27.2		215	75.7 ± 34.3		215	97.9 ± 33.1		215	63.2 ± 34.1
ER+	463	111.7 ± 25.8		459	65.9 ± 26.2		503	74.3 ± 35.9		503	96.0 ± 37.6		503	59.3 ± 35.6
PR status			0.36			< 0.0001			0.57			0.46			0.04
PR−	307	110.2 ± 26.4		302	57.9 ± 27.0		333	73.8 ± 36.0		333	95.3 ± 36.3		333	63.2 ± 34.0
PR+	361	112.0 ± 24.1		355	66.8 ± 26.2		386	75.3 ± 35.1		386	97.4 ± 36.6		386	57.9 ± 36.1
HER2 status			0.15			0.24			0.35			0.37			0.42
HER2−	538	110.6 ± 25.6		521	63.4 ± 26.5		573	74.2 ± 36.3		573	96.1 ± 36.1		573	60.0 ± 35.0
HER2+	121	114.2 ± 20.1		124	60.2 ± 27.4		130	77.2 ± 31.9		130	99.3 ± 36.3		130	62.8 ± 35.6
Breast cancer subtype^a			0.24			< 0.0001			0.71			0.58			0.12
Luminal A	393	110.6 ± 26.5		383	66.2 ± 26.1		420	73.9 ± 36.6		420	95.3 ± 37.2		420	58.5 ± 35.7
Luminal B	55	117.7 ± 13.2		56	66.3 ± 26.1		60	79.3 ± 28.4		60	98.8 ± 35.7		60	58.3 ± 35.5
HER2-E	66	111.2 ± 34.1		68	55.3 ± 27.7		70	75.4 ± 34.7		70	99.7 ± 37.1		70	66.5 ± 35.5
TN	145	110.6 ± 23.3		138	55.8 ± 26.3		152	75.7 ± 35.3		152	99.1 ± 31.9		152	64.6 ± 32.7

IHC expression scores reflect quantitative expression of LEP, LEPR, ADIPOQ, ADIPOR1, and ADIPOR2 as analyzed through an automated/unsupervised scoring (quantitative) methodology. The scores estimate the effective staining intensity (ESI) within the effective staining area (ESA) of the biomarker in question
^aBreast cancer subtypes were classified based on IHC expression of ER and PR, and overexpression or amplification of HER2 (by IHC or FISH) as reported in pathology records

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