Int. J . Cancer: 45, 397-402 (1990) 0 1990 Wiley-Liss, Inc.

Publication of the Internstional Union Against Cancer Publication de I‘Union Internationals Contre le Cancer

ANTHROPOMETRIC VARIABLES AND RISK OF BREAST CANCER Fabio PARAZZINI’.~, carlo LAVECCHIA’.~, Eva NEGRI’.3, Pa010 BRUZZP,Domenico PALLI’and Peter B O Y L E ~ ‘Istituto di Ricerche Farmacologiche “Mario Negri” , 20157 Milan, Italy; 21nstitute of Social and Preventive Medicine, University of Lausanne, 1005 Lausanne, Switzerland; 31nter-University Consortium of Lombardy for Automatic Data Processing (CILEA), 20090 Segrate, Milan; 41stituto Nazionale per la Ricerca sul Cancro, Viale Benedetto XV 10, 16132 Genoa; 5Centroper la Prevenzione Oncologica (CSPO), USL I OIE, Florence, Italy; and 6Analytical Epidemiology Unit, International Agency for Research on Cancer, 69372 Lyon Cedex, France. The role of anthropometric variables in the risk of breast cancer has been investigated using pooled data from 2 hospital-based case-control studies conducted in Italy for a total data-set of 3,247 cases and 3,263 controls. No association was observed in pre-menopausal women between breast cancer risk and height, weight, indices of body mass (W/H2; W I H ’ 9 and surface area. In post-menopausal women, the risk of breast cancer was inversely related to height, being 0.8 in taller women (>I65 cm) compared with women 155 cm tall or less; the trend in risk, although not constantly decreasing, was statistically significant (p trend = 0.03). A direct, statistically significant association emerged with weight and indices of body mass and post-menopausal breast cancer risk. Considering 2 indices of body weight (W/H2 and W/H’.5) and relative to thinner women, the respective estimated risks of post-menopausal breast cancer increased to 1.4 and 1.3 for grossly obese women, and the corresponding p values for trend were respectively 0.002 and 0.02. The role of overweight was more evident in women with early age at menopause, thus suggesting a duration-risk effect.

There is convincing evidence that obesity increases the risk of breast cancer in post-menopausal women (de Waard, 1975; Boyle, 1988). The role of obesity in the pre-menopause, as well as the potential influence of other anthropometric variables on breast carcinogenesis, is, however, still largely undefined (Choi et al., 1978; Helmrich et al., 1983; Talamini et al., 1984; Lubin et al., 1985; Willett et al., 1985; La Vecchia et al., 1987; Le Marchand et al., 1988). Various studies have shown an inverse relation between measures of body weight and minimal or early breast cancer in the pre-menopause. This could be related to menstrual irregularities and frequent anovulation in obese women, which may reduce their breast cancer risk (La Vecchia et al., 1985; Key and Pike, 1988), but the possible influence of selection bias must be considered in this respect, since small breast lumps are obviously more easily detectable in thinner women (Brinton et al., 1983; Willett et al., 1985; Swanson et al., 1988). The hypothesis that the onset of menses is linked to the attainment of a certain body mass (and the suggestion that early menarche is a risk factor for breast cancer) led to the speculation that higher weight in adolescence and greater height might be related to the subsequent risk of breast cancer (de Waard and Trichopoulos, 1988). However, direct evidence from epidemiological studies only partially supports this hypothesis. Studies on migrants (Locke and King, 1980; Boyle, 1988) and cohorts of young athletes (Frisch et al., 1987) or ballet dancers (Warren, 1980) suggested that lower weight during adolescence and young adult life may reduce subsequent breast cancer incidence. However, the American Nurses Health Study (Willett et al., 1985) and a cohort investigation of Hawaiian women (Le Marchand et al., 1988) found an inverse association between adolescent body mass and pre-menopausal breast cancer, and a limited and inconsistent relation with earlier age at menarche, height or weight. The issue has important theoretical implications in order to

understand the role of overweight (and its biological correlates) within the framework of the process of breast carcinogenesis, i.e., whether it has essentially a late-stage effect (like estrogens in endometrial cancer) (La Vecchia et al., 1984) or an early stage one, or both. The prospective study by de Waard and Baanders-van Halewijn (1974) found an independent effect of height on breast cancer risk, and an approximately multiplicative effect of height and weight: the relative risk rose to 3.6 for tallest/ heaviest women compared to the lowest heighvweight category. Subsequent studies (Willett et al., 1985; Kolonel et al., 1986; La Vecchia et al., 1987; Le Marchand et al., 1988; Swanson et al., 1988), produced inconsistent results, particularly for the relation with height, but, at least from an aetiological viewpoint, it is clearly important that the 2 factors (height and weight) are examined separately as well as in terms of combined indices. In this article, therefore, we examine the relation between various anthropometric variables and breast cancer risk, using data of a combined data-set from 2 large Italian case-control studies, i . e . , from a country with breast cancer mortality rates (28.1/100,000 in 1983) (Decarli and La Vecchia, 1989) intermediate between those of Great Britain and other Northern European countries and Japan, Central America and Africa (Boyle, 1988). The availability of comparable data in terms of collection methodology, drawn from 2 case-control studies conducted in the north and centre of Italy, offers the opportunity of analyzing the role of these factors in a large data-set, thus allowing investigation of such factors as menopausal status or age at menopause on meaningful numbers. SUBJECTS AND METHODS

The study design and methods of the 2 Italian case-control studies and their pooled analysis have been previously described (Toti et al., 1986; La Vecchia et al., 1987; Negri et al., 1988a). The first study (Toti et al., 1986) was a cooperative hospitalbased investigation carried out between 1980 and 1983 in 13 breast cancer clinics from 10 different Italian areas: 8 from Northern Italy (75% of the cases), I from Central Italy (20%) and 1 from the South (5%). Information was available on 1,227 newly diagnosed cases (histologically and/or cytologically confirmed) and 1,153 controls admitted for acute, orthopaedic, medical or surgical conditions, unrelated to known or suspected risk factors for breast cancer. Although matching was not strictly respected in the final series, the distribution of cases and controls according to province of residence was satisfactorily comparable. The second study (La Vecchia et al., 1987) was a hospital7To whom reprint requests should be sent, at the Istituto di Ricerche Farmacologiche “Mario Negri”, via Eritrea 62, 20157 Milan, Italy. Received: July 3, 1989 and in revised form November 29, 1989.

398

PARAZZINI ET AL.

based case-control study on a total of 2,020 histologically confirmed breast cancer cases below age 75 admitted from January 1983 to December 1988 to the National Cancer Institute, Milan, and the Ospedale Maggiore (which includes the 4 largest teaching and general hospitals in Milan). The comparison group consisted of 2, I 10 women admitted to the same network of hospitals for acute conditions (30% trauma, 25% other orthopaedics, 18% surgical, 27% other miscellaneous) comparable with the case series in terms of age and area of residence. In both studies less than 2% of cases and controls refused to be interviewed. Height and weight estimates were obtained, like other information, by interview. The distribution of cases and controls according to age and study is shown in Table I.

TABLE 11 - CORRELATION COEFFICIENTS’ FOR HEIGHT, WEIGHT, INDICES OF BODY MASS AND SURFACE AREA; ITALY, 198C-88

Height Weight win2 wtnl-5

1.00

0.30 1.00

-0.12 0.91 1.00

-0.01 0.95 0.99 1.00

w0.33/H

Surface area

-0.33 0.79 0.97 0.94 1.00

0.45 0.98 0.83 0.88 0.69 1 .OO

‘Pearson correlation coefficient.

surface area and risk of breast cancer is shown in Table 111. Height was inversely associated with the risk of breast cancer: Data analysis compared to women 155 cm tall or less, the risk decreased with The following information was obtained from the original increasing height, being 0.82 in women taller than 165 cm. data files of the 2 studies: age, height, weight, age at first The trend in risk, although not completely consistent, was full-term birth, parity, age at menarche, family history of statistically significant. No relation emerged with weight. Likewise, indices of body mass (W/H2 and W/H’.5) and surbreast cancer, menopausal status and age at menopause. face area were. unrelated to breast cancer risk (Table 111). Three different indices of body mass were calculated. W/H2 The role of anthropometric variables was further examined (Quetelet’s index), W/H1.5and W0.33/H.Body surface area [as potential indicator of metabolic rate (de Waard et al., 1977)] in strata of pre- and post-menopause. No association was found was computed as 0.0235 X H0.422(in cm) x W0.515(in kg). between pre-menopausal breast cancer risk and height, weight, As expected (Benn, 1971; Keys et al., 1972), W/H’.5, W/H2, indices of body mass or surface area (Table IV). In post-menopausal women, the risk of breast cancer was Wo33/H indices and surface area were closely correlated to weight, but W/H*.5was the least correlated to stature (Table inversely related to height. The trend was statistically signifi11). Nonetheless, W/H2 is probably the most appropriate body cant, but the estimated relative risks did not constantly demass index, as a moderate inverse association between body crease, being in subsequent strata of height, 1, 0.87, 1.07, mass and height is known to be real in this population, and due 0.76, 0.84. to the fact that shortest women tend to be more frequently A direct, statistically significant association emerged with obese. weight and indices of body mass. Considering W/H2 and Odds ratios as estimators of relative risks (RR) of breast W/H1.5indices, the estimated risks of breast cancer increased cancer according to height, weight, body mass indices and to 1.39 and I .34 for grossly obese women compared to thinner surface areas, together with their 95% approximate confidence women, and the corresponding p values for trend were 0.002 intervals (CI) were first computed from data stratified for age and 0.02 (Table V). The significance, however, was mainly only. Further, unconditional multiple logistic regression equa- due to the lowest risks among women in the lowest strata, since tions, fitted by the method of maximum likelihood (Baker and there was no real evidence of trend in subsequent strata. This Nelder, 1978; Breslow and Day, 1980), were used. Included in finding was confirmed when the relationship was analyzed in the regression equation were terms for age (as a cardinal term), wider ranges of body mass index: for example the relative risk study centre, age at menarche (S12, 13-14, 315), age at first of post-menopausal breast cancer was 1.41 in women reporting birth (162-165

573

606

>165

551

618

XZl trend Weight (kg)

454 >54-60

656 775

753 789

>60-65

617

554

>65-72

595

562

604

605

xzI(trend)

12

0.89 (0.78-1.02) 1.06 (0.861.32) 0.85 (0.72-1.OO) 0.82 (0.72-1.96) p = 0.02 12

1.06 (0.91- 1.24) 1.18 (l.oCr1.39) 1.09 (0.92-1.28) 1.04 (0.88-1.22) p = N.S.3

WIP

c21.08 >21.08-23.05

578 653

725 654

B23.05-25.OO

681

620

>25.OG27.55

658

639

>27.55

677

625

xzItrend

12

1.15 (0.9S1.35) 1.23 (1 lwl.44) 1.11 (0.94-1.31) 1.20 ( 1.02-1.42) p = N.S.

WIH'.'

c26.68 >26.68-29.25

588 661

734 644

>29.25-31.72

679

609

>31.72-34.92

647

647

>34.92

672

629

12

1.18 (1 .oCr1.38) 1.23 ( 1.04- 1.44) 1.07 (0.91-1.27) 1.18 (1 .W1.39) p = N.S.

XzI (trend) Surface (mZ)

41.55 >1.55-1.64

622 649

680 650

>1.64-1.71

644

601

>1.71-1.82

691

689

>1.82

641

643

(trend)

Controls

_.._ .,\

Relative risk estimates .._cJ

._..

Height (em)

el55 >155-160

Y'.

I1 1 I l l P A S F S I 741 rnNTPnl C V I T A I Y 1 9 Q L Q Q

Controls

Height (cm)

>72

TABLE IV - RELATIVE RISK' OF PRE-MENOPAUSAL BREAST CANCER ACCORDING TO QUINTILES OF SELECTED ANTHROPOMETRIC VARIABLES

12

1.05 (0.9G1.24) 1.11 (0.94-1.31) 1 .oo (0.85-1.17) 0.99 (0.85-1.17) D =

N.S.

'Estimates from multiple logistic regression equations including terms for age, study centre, age at menarche, age at first birth, family history and menopausal status. -2Reference categ~ry.-~Notsignificant.

lead to underestimation of the association between anthropometric measures and breast cancer. It is, moreover, unlikely that the case/control status influenced reporting of height and weight; the possible relationship between obesity, height and breast cancer, in fact, has not gained widespread attention in the Italian population and was probably unknown to most of the subjects interviewed.

4155 >155-160

212 369

221 417

>la162

95

94

> 162-165

224

231

>165

210

278

12

0.92 (0.72-1.18) 1.03 (0.72-1.48) 1.02 (0.77-1.34) .81 (0.61-1.06) p = N.S.

X*I (trend) Weight (kg)

654 >54-60

310 302

373 330

>60-65

214

216

>65-72

161

156

1.06

166

(0.80-1.41) 0.72 (0.53-0.96)

>72

123

p = N.S.

XzI (trend) WIP

S21.08 >2 1.08-23.05

300 266

390 282

>23.05-25.OO

246

228

B25.OG27.55

156

187

B27.55

142

154

12

1.11 (0.87-1.41) 1.15 (0.89-1.48) 0.85 (0.64-1.12) 0.96 (0.71-1.29) p = N.S.

XZ1trend WIW.5

G26.68 >26.68-29.25

298 266

399 280

>29.25-31.72

251

219

B31.72-34.92

154

192

>34.92

141

151

12

1.14 (0.89-1.45) 1.24 (0.96-1.59) 0.85 (0.65-1.13) 0.99 (0.74-1.33) p = N.S.

Xzl Surface (m2)

a1.55 >1.55-1.64

274 271

310 299

>1.64-1.71

220

244

>1.71-1.82

203

209

>1.82

142

179

Y z n(trend)

12

0.97 (0.77-1.22) 0.98 (0.75-1.27)

12

0.94 (0.74-1.21) 0.87 (0.67-1.13) 0.96 (0.73-1.25) 0.73 (0.5M.98) D

= N.S.

'Estimates from multiple logistic regression equations includin terms for age, study centre, age at menarche, age at first birth, family history.-2Reference category.

Likewise, it is in our opinion improbable that the present results were severely affected by other sources of bias. Although data were collected in more than 10 different centres and had some intrinsic limitations, including for instance the absence of information on stage, cases and controls were drawn from hospitals and institutions covering comparable catchment areas and DarticiDation rate was almost comulete. Further, these findings' could hardly be explained by c o n f k d -

400

PARAZZINI E T A L .

TABLE V - RELATIVE RISK' OF POST-MENOPAUSALBREAST CANCER ACCORDLNG TO QUINTILES OF SELECTED ANTHROPOMETRY VARIABLES (2.137 CASES. 2.022 CONTROLS): ITALY. 198LL88 Breast cancer

Controls

Height (cm) GI55 > 155-160

560 722

468 708

>160-162

165

131

>162-165

349

375

> I65

341

340

TABLE VI - RELATIVE RISK1 OF POST-MENOPAUSAL BREAST CANCER ACCORDING TO QUINTILES OF WEIGHT AND W/H2 IN STRATA OF AGE AT MENOPAUSE; ITALY, 198LL88

Relative risk estimates (95% confidence interval)

Aee at menopause >52 4549 5&52 145 (362 cases/ (61 1 cases/ (730 cased (425 cases/ 434 controls) 629 controls) 635 controls) 319 controls)

~

xzI@end) Weight ( k g ) s 54 >54-60

346 473

380 459

>6M5

403

338

>65-72

434

406

>72

481

439

Wlff S21.08 B21.08-23.05

278 387

335 372

>23.05-25.OO

435

392

>25 SKL27.55

502

452

>27.55

535

471

x21(trend)

xZ1trend

12

0.87 (0.74-1.03) 1.07 (0.82-1.40) 0.76 (0.63-0.93) 0.84 (0.69-1.03) p = 0.03 12

1.15 (0.94-1.40) I .34 (1.08-1.65) 1.16 (0.94-1.43) 1.24 (1.01-1.52) p = 0.05 12

1.22 (0.97-1.52) 1.33 (1.07-1.66) 1.29 (1.05-1.60) 1.39 ( 1.13-1.71) p = 0.002

WIH' G26.68 >26.68-29.25

290 395

335 364

>29.25-31.72

428

390

>31.72-34.92

493

455

>34.92

531

478

< I .55 s 1.55-1.64

348 378

370 35 1

S1.64-1.71

424

357

S1.71-1.82

488

480

>1.82

499

464

xzI (trend)

12

1.24 (l.oCrl.55) 1.28 (1.03-1.59) 1.21 (0.98-1.49) 1.34 (1.09-1.65) p = 0.02

Surface (m2)

, ' Y

Itrend)

12

1.17 (0.95-1.45) 1.30 ( 1.05-1.60) 1.08 (0.88-1.32) 1.19 (0.98-1.46) D =

N.S.

IEstimates from multiple logistic regression equations including terms for age, study centre, age at menarche, age at first birth, family history and age at menopause. -2Reference category.

ing, since allowance for age, centre and major potential distorting factors, including well-known risk factors for breast cancer, did not appreciably change the estimated relative risks. The choice of hospital controls for a study of the association between weight and various diseases may lead to an underestimation of the true association, since overweight is related to cardiovascular, metabolic and orthopaedic diseases (Lew and Garfinkel, 1979; Negri et al., 19886). However, in our study

Weight (kg)

534 >54-60 >6M5 >65-72 >72

XzI(trend) WIH2 621.08 >21.08-23.05 B23.05 >25.00-27.55 >27.55 Y 2 a (trend)

12

12

1.51 1.41 1.14 1.64

1.12 1.11 1.35 1.46 p = N.S. p = 0.02 p 12

1.85 1.80 1.42 1.92 D=N.S. ~

12

12

1.13 1.54 1.10 0.94 = N.S. p 12

12

0.90 1.35 1 .00 1.18 = N.S 12

0.92 1.27 1.14 I .42 1.13 1.29 1.19 1.25 1.33 1.33 1.21 1.41 = 0 . 0 4D = N . S . D = N . S .

IEstimates from multiple logistic regression equations including terms for age, study centre, age at menarche, age at first birth and family history.-*Reference category.

the estimated relative risks were similar when a comparison was made with different categories of controls (trauma, other orthopaedic, surgical and other). Obesity may increase the risk of post-menopausal breast cancer by increasing the level or availability of estrogens (Ota et al., 1986; Trichopoulos et al., 1987), through increased conversion of androgens in the adiopose tissue (Siiteri, 1978) or decreased levels of sex-hormone-binding globulin (Nisker et al., 1980). At pre-menopausal ages the contribution of nonovarian estrogens is low, and this could explain the lack of relation between body mass and pre-menopausal breast neoplasia. The significantly decreased pre-menopausal breast cancer risk observed in our study for the upper quintile of weight (but not of body mass indices) can be, at least in part, explained in terms of irregular menstrual periods, amenorrhea and luteal phase progesterone deficiency associated with obesity (Key and Pike, 1988), although the potential role of diagnostic bias ( i . e . ,easier detection of small breast lumps in thinner women) is difficult to dismiss. Furthermore, the observation that the relation between weight or indices of body mass and post-menopausal breast cancer risk is more evident in strata of early age at menopause can be explained in terms of longer time of exposure to high levels of endogenous estrogens in overweight women. This is consistent with a duration-risk relationship, although direct investigation of time since menopause is complicated by the predominant effect of age and potential interaction with it. Greater height and weight in adolescence have been considered to be related to subsequent risk of breast cancer (de Waard and Trichopoulos, 1988), since over-nutrition early in life may increase breast cellularity (Albanes and Winick, 1988). However, if this hypothesis were true, the risk should be increased both in pre- and post-menopausal age groups. Likewise, if over-nutrition in childhood and adolescence affects the risk of breast cancer, leading to earlier menarche (de Waard and Trichopoulos, 1988), the effect of height and weight should be more evident in pre-menopausal women, when age at menarche appears to be a more relevant factor (Negri et al., 1 9 8 8 ~ ) . Confirmation of the absence of any important role of nutritional status (specifically over-nutrition) early in life on subsequent breast cancer risk comes from a cohort survey in Hawaii (Le Marchand et al., 1988) which found that weight during adolescence was inversely related to subsequent breast cancer risk. In these data, there was no clear relationship between height and breast cancer risk and, if anything, an inverse trend was

ANTHROPOMETRIC VARIABLES AND BREAST CANCER RISK

observed in post-menopausal women. Chance might explain this finding, since there is no evident aetiological mechanism or obvious bias which may explain this apparent difference between pre- and post-menopausal women. In general, evidence from these and previous data of a positive (de Waard and Baanders-van Holewijn, 1974; Brinton et al., 1983; Swanson et al., 1988; Tretli, 1989), inverse or no relationship (Adami et al., 1977; Willett et al., 1985; Le Marchand et al., 1988; Albanes et al., 1988) are far from indicating a clear and convincing association between height and risk of breast cancer. The differences in various studies, moreover, might be due to differences in the nutritional status of various populations at subsequent time periods which are reflected in the corresponding sequence of the general increase in height over the last few decades (de Waard, 1975; Kolonel et al., 1986; London and Willett, 1988). Surface area has been positively associated with risk of breast cancer in 2 case-control studies (de Waard et al., 1977; Kolonel et al., 1986). This relationship was explained in terms of metabolic rate; however, no relationship emerged in our study between surface area and breast neoplasia.

40 1

In conclusion, this combined analysis of 2 case-control studies from Northern Italy confirmed, in a sample larger than previously available, that overweight is consistently associated with breast cancer in post-menopausal women possibly with a direct duration-risk relationship. Although the association was, in terms of relative risk, moderate, it could account for about 10% of post-menopausal breast cancers in this population. Data on height from this study were not in agreement with most published evidence, and cast some doubt on the consistency of this association, or its applicability in different populations.

ACKNOWLEDGEMENTS

This study was conducted within the framework of heCNR (Italian National Research Council) Applied Project “Oncology”. The contributions of the Italian League Against Tumors and of the Italian Association for Research on Cancer, Milan, Italy, are gratefully acknowledged. The authors thank Ms. I. Garimoldi, Ms. S . Bidoli, Ms. J . Baggott and the G.A. Heiffer Memorial Library Staff for editorial assistance.

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Anthropometric variables and risk of breast cancer.

The role of anthropometric variables in the risk of breast cancer has been investigated using pooled data from 2 hospital-based case-control studies c...
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