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					                                                             Life and Fitness

Some Thoughts on Body Mass Index, Micronutrient
Intakes and Pregnancy Outcome1
           Yasmin Neggers*2 and Robert L. Goldenbergy
           *University of Alabama, Department of Human Nutrition, University of Alabama,
           Tuscaloosa, AL 35487 and yUniversity of Alabama at Birmingham, Center for Research in
           Women’s Health, Birmingham, AL 35233

           ABSTRACT A low prepregnancy body mass index is one of strongest predictors of adverse pregnancy outcomes
           such as preterm birth and fetal growth retardation. A low body mass interacts with other risk factors such as smoking
           and stress to increase risk of these outcomes, whereas zinc supplementation and low-dose aspirin increase birth
           weight in thin but not normal-size women. The association between maternal thinness and adverse pregnancy
           outcomes may be mediated more by a low plasma volume than by decreased protein or energy status. Maternal
           micronutrient status may partially mediate plasma volume expansion in pregnancy. Therefore, improving maternal
           micronutrient status may reduce adverse outcomes through this mechanism. J. Nutr. 133: 1737S–1740S, 2003.

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           KEY WORDS:  body mass index  plasma volume  preterm birth  fetal growth
           retardation  micronutrients

   Maternal nutritional status both before and during preg-                               BMI and pregnancy outcomes: birth weight,
nancy is a well-recognized determinant of birth outcomes (1).                             intrauterine growth retardation and preterm delivery
Only two indicators of maternal nutritional status during
pregnancy have shown consistent positive association with                                     In developed countries an interaction between prepregnancy
infant birth weight: maternal prepregnancy weight for height                              weight and weight gain during pregnancy has been reported:
and weight gain during pregnancy (2). Body mass index                                     underweight women with weight gain in excess of 12 kg and
(BMI)3, defined as wt/ht2, is a simple, useful index for eval-                             overweight women with weight gains limited to 6–11 kg tend to
uating prepregnancy nutritional status in clinical settings.                              have the best pregnancy outcome (6). Spinillo et al. (7) reported
In 1990 the United States Institute of Medicine established                               a prepregnancy BMI , 19.5 and a second and third trimester
new weight gain recommendations for women during preg-                                    weight gain ,0.37 kg/wk to be associated with a significantly
nancy using BMI as the preferred way to classify women into                               increased risk of spontaneous preterm delivery. The risk of
prepregnancy weight categories (3). Although prepregnancy                                 spontaneous preterm delivery was associated with a low second
BMI has a genetic as well as nutritional component, a low                                 or third trimester weight gain with a BMI # 19.5 (odds ratio
prepregnancy BMI is considered a marker for minimal tissue                                [OR] 5.63; 95% confidence interval [CI]: 2.35–13.8) compared
nutrient reserves (4). Women with low prepregnancy weight for                             with those with BMI . 19.5 (OR 2.45; 95% CI: 1.60–3.75).
height or BMI are at increased risk for a number of adverse                               Similarly, Schieve et al. (4) reported that women with low
pregnancy outcomes, including preterm birth and intrauterine                              prepregnancy BMI were at increased risk of preterm delivery
growth retardation (IUGR) (5).                                                            only if they failed to gain weight at an adequate rate during
                                                                                          pregnancy. However, low prepregnancy BMI alone has also
                                                                                          been independently implicated as a risk factor for preterm
                                                                                          delivery. In a matched case-control study of idiopathic preterm
                                                                                          labor in Canada, Kramer et al. (8) reported an OR of 2.06 (95%
                                                                                          CI: 1.77–3.34) for preterm delivery in women with a pre-
      Manuscript prepared for the USAID-Wellcome Trust workshop on ‘‘Nutrition
as a preventive strategy against adverse pregnancy outcomes,’’ held at Merton             pregnancy BMI , 19.8. In a large cohort of Hispanic women in
College, Oxford, July 18–19, 2002. The proceedings of this workshop are                   the United States, Siega-Riz et al. (5) tested BMI cut points cited
published as a supplement to The Journal of Nutrition. The workshop was                   in the Institute of Medicine report (3) for their ability to predict
sponsored by the United States Agency for International Development and The
Wellcome Trust, UK. USAID’s support came through the cooperative agreement                preterm birth. Women with a prepregnancy BMI , 19.1 had
managed by the International Life Sciences Institute Research Foundation.                 a significantly increased risk of delivering preterm (relative risk
Supplement guest editors were Zulfiqar A. Bhutta, Aga Khan University, Pakistan,
Alan Jackson (Chair), University of Southampton, England, and Pisake Lumbiga-
                                                                                          1.7, p , 0.05; positive predictive value 10.4%). Although the
non, Khon Kaen University, Thailand.                                                      relative risks were not statistically significant, there was a trend
      To whom correspondence should be addressed. E-mail: yneggers@ches.                  toward a decreased risk of preterm birth with higher BMI.
      Abbreviations used: AOR, adjusted odds ratio; BMI, body mass index; CI,             Prepregnancy weight status based on BMI alone was an indicator
confidence interval; IUGR, intrauterine growth retardation; OR, odds ratio.                of preterm birth only for women with a low BMI.

0022-3166/03 $3.00 Ó 2003 American Society for Nutritional Sciences.

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    In a large prospective study of predominantly black indigent            smaller or of lower birth weight than infants born to women
women to examine the risk factors associated with IUGR and                  with either a normal or high BMI.
preterm delivery (9), except for a history of preterm delivery,                Studies conducted by Goldenberg et al. (11–13) have in-
a low prepregnancy weight (, 50 vs $ 85 kg) had the strongest               dicated an association between several risk factors for IUGR
relationship with preterm delivery with an adjusted odds ratio              and BMI. For example, smoking and psychosocial stress during
(AOR) of 2.72 (p , 0.05). Also, there was a 3-fold increase in              pregnancy and protective factors such as aspirin use and zinc
risk of IUGR (AOR 3.0, p , 0.05) in women with low                          supplementation during pregnancy were significantly associated
prepregnancy weight after adjustments were made for other                   with IUGR only in women with low BMI.
confounders. The risk of IUGR in women with low                                A poor psychosocial profile during pregnancy in both
prepregnancy weight was larger than all the other independent               smokers and nonsmokers was a significant predictor of IUGR
risk factors in the multiple regression model (Table 1). In                 only in thinner women (pregnancy BMI , 22). The risk of
a study to evaluate measures of maternal lean mass and fat                  IUGR was not significant in women with a poor psychosocial
reserves as predictors of infant birth size, the maternal                   profile in either smokers or nonsmokers with BMI $ 22 (13). In
prepregnancy weight was the best predictor for nearly every                 thinner women who smoked and had a poor psychosocial
neonatal measurement considered (2).                                        profile during pregnancy, the rate and the relative risk of IUGR
    In a comprehensive study to define a de facto reference BMI              was substantially higher (mean % IUGR 5 31.5; AOR 1.65;
for women in developing countries, Nestel and Rutstein (10)                 95% CI: 1.06–2.57) than for heavier women who smoked and
evaluated data from 46 national surveys in 36 developing                    had a poor psychosocial profile (mean % IUGR 5 11.1; AOR
countries for mothers aged 15–49 y. Four reproductive out-                  1.04; 95% CI: 0.50–2.15) (Table 2). Thus, a higher BMI seems
comes were compared according to BMI categories: neo-                       to protect against the adverse effect of stress and smoking in
natal and infant mortality, size at birth, birth weight and                 this population of poor and primarily black women.
miscarriage or stillbirth. Except for miscarriage or stillbirth,               In a randomized trial of low-dose aspirin (60 mg/d from 24

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women with a low BMI had worse outcomes in each outcome                     wk gestation) to reduce the incidence of preeclampsia (12), the
category than did women with a normal or high BMI. Women                    use of aspirin was associated with an 88 g (p 5 0.04) increase in
with a low BMI were more likely to have an infant that was                  birth weight after adjustment for other confounders. However,
                                                                            when the study population was divided by median BMI
                                                                            (median BMI 5 24.1), virtually the entire increase in birth
                             TABLE 1                                        weight associated with aspirin use (;140 g) was found in
                                                                            thinner women (BMI , 24.1). Sequential fetal ultrasound
   Adjusted odds ratios of some risk factors for intrauterine               measurements showed significant changes in the fetal abdom-
  growth retardation (IUGR) and preterm delivery calculated                 inal circumference (p , 0.001) at 27 wk and later associated
          from multiple logistics regression models                         with aspirin use, but these changes occurred only in thinner
                                                         Odds ratios           In a randomized, double-blind, placebo-controlled trial to
          Risk factors                   IUGR          Preterm delivery     evaluate the efficacy of zinc supplementation (25 mg zinc/d,
                                                                            starting at 19 wk gestation) on pregnancy outcome, infants of
Race                                                                        women in the zinc supplemented group had a significantly
  Black versus White                     1.70*               1.35*          higher birth weight (126 g, p 5 0.03) than did infants of women
  First versus second                    1.79                0.96           in the placebo group (11) (Table 3). However, in the thinner
  Third or more versus second            0.87                0.97           women (BMI , 26), zinc supplementation was associated with
Sex                                                                         a 248 g higher birth weight. Zinc supplementation had virtually
  Female versus male                     1.57*               1.07           no effect in heavier women (BMI $ 26).
Marital status
  Unmarried versus married               0.98                1.20
Education (y)                                                               Micronutrient intakes and pregnancy outcome
  ,12 vs. $12                            1.02                1.01
  12 vs. $12                             1.03                0.97              Considerable evidence suggests a role for micronutrients in
Maternal age (y)                                                            pregnancy outcomes (14–16). Even in a developed country
  $36 vs. 20–25                          1.95*               1.45*          like the United States, a substantial proportion of women of
Previous preterm delivery                                                   childbearing age consumes diets that provide less than the
  Yes versus no                          1.44*               2.92*          recommended amounts of micronutrients, particularly, zinc,
Maternal smoking
  Yes versus no                          2.00*               1.19*          folate, calcium and iron (17,18). In south Asia, iron deficiency
Maternal alcohol consumption                                                and anemia affect 50% or more of pregnant women. The
  Yes versus no                          1.04                0.97           prevalence of folic acid deficiency may be up to 30–50% and
Maternal drug use                                                           zinc deficiency is likely to be widespread (14). However,
  Yes versus no                          1.19                0.70           nutrition intervention studies have not provided unequivocal
Maternal weight (kg)                                                        evidence of an association between micronutrient intakes and
  ,50 vs. $85                            3.00*               2.72*
  50–60 vs. $85                          2.06*               2.33*          pregnancy outcomes such as birth weight, IUGR, preterm
  61–72 vs. $85                          1.55*               1.68*          delivery and pregnancy-induced hypertension (19,20). Study
  73–84 vs. $85                          1.14                1.23           population, sample size and study design showed considerable
Weight gain/wk (kg)                                                         methodological variation across these studies. Also, many of
  ,0.24 vs. 0.58–0.74                    2.24*               1.52*          these studies were conducted in women not at great risk for low
  0.24–0.57 vs. 0.58–0.74                1.55*               1.11           micronutrient intakes and were therefore less likely to
  $0.75 vs. 0.58–0.74                    1.25*               1.71*
                                                                            demonstrate a positive association between micronutrient
    * Significant (p , 0.05) differences in the rates of IUGR and preterm    intakes and pregnancy outcome.
delivery between the reference population and those with risk factor.          In a systematic review of randomized clinical trials to
   Data are from reference 9.                                               evaluate nutritional interventions to prevent IUGR, Onis et al.
                                   BODY MASS INDEX, MICRONUTRIENTS AND PREGNANCY OUTCOME                                                         1739S

                                                                          TABLE 2
                     Intrauterine growth retardation, mean birth weight, and relative risks of fetal growth retardation
                                                  according to maternal size in smokers

                         Good psychosocial profile                               Poor psychosocial profile
                                                                                                                      RR for IUGR
                   N              % IUGR                BW                N           % IUGR               BW        with poor profile          95% CI

BMI , 22          199             19.10                 3104              73            31.51              2994           1.65                1.06, 2.57
BMI $ 22          205             10.73                 3260              81            11.11              3294           1.04                0.50, 2.15

   Abbreviations: IUGR, intrauterine growth retardation; BW, birth weight; RR, relative risk; CI, confidence interval; BMI, body mass index.
   Data are from reference 13.

(19) concluded that perhaps with the exception of balanced                         Prepregnancy BMI, birth weight and
protein and energy supplementation, no effective nutritional                       micronutrient intakes
intervention has been demonstrated. However, they
recommended that interventions such as with zinc, folate and                           The mechanisms of association between prepregnancy BMI
magnesium supplements during pregnancy merit further re-                           and IUGR and preterm delivery are not clear, but throughout
search.                                                                            the literature there is an assumption that the relationship

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   Ramakrishan et al. (20) published an extensive review of the                    between a low prepregnancy BMI and adverse pregnancy
relationship between micronutrient status and pregnancy                            outcomes is mediated by protein-energy availability. However,
outcome. This review was not restricted to randomized                              there are reasons to believe protein-energy malnutrition may
controlled trials and also included cross-sectional, prospective,                  not provide the full explanation (21,22). For example, the
case-control studies. Their key conclusions were that 1)                           effect of reduced prepregnancy weight on fetal growth was still
significant evidence, mostly from developed countries, shows                        present when underweight women were able to gain weight at
improved pregnancy outcomes from supplementation with zinc,                        a normal rate throughout pregnancy (23,24). It is likely that
calcium and magnesium; 2) vitamin A supplements may be                             a normal gestational weight gain indicates a positive energy
associated with reduced maternal mortality and increased                           balance. If maternal energy intake directly affects fetal growth,
birthweight; 3) although the prevention of neural tube defects                     then it is hard to explain why similar weight gains result in
with folate supplementation and increases in hemoglobin with                       larger infants in women with a normal prepregnancy weight
iron supplementation are well documented, evidence demon-                          than in women with a low prepregnancy weight. One ex-
strating whether folic acid and iron supplementation reduce                        planation for the lower mean infant birth weight in women
other adverse pregnancy outcomes is limited; 4) vitamin C                          with low prepregnancy weight may be that the fetus was
deficiency may have a role in the etiology of preterm delivery;                     prevented from receiving an adequate supply of nutrients from
and 5) severe maternal iodine deficiency results in mental                          the mother because of changes in maternal hemodynamic
retardation and cretinism but evidence is weak in the case of                      status (22).
marginal iodine deficiency.                                                             In a study comparing the plasma volume in underweight,
   Because in developing countries the prevalence of both poor                     normal-weight and overweight women with similar weight
pregnancy outcome (20% of infants are low birth weight                             gains during pregnancy, underweight women had smaller total
compared with 6% in developed countries) and multiple                              plasma volume than did normal and overweight women both
micronutrient deficiencies are common, well-designed random-                        early and late in pregnancy (22). As expected, the mean birth
ized clinical trials in high risk women with low prepregnancy                      weight of infants of underweight women was significantly lower
BMI are needed to evaluate the role of micronutrients related                      than those of the other two groups. During pregnancy no
to poor pregnancy outcomes.                                                        differences in plasma volume expansion were observed between
                                                                                   underweight and normal-weight women. It was concluded that
                                                                                   because weight gain was similar in all groups, maternal weight
                                                                                   and plasma volume increased proportionately. The authors
                              TABLE 3                                              suggest that this supports a key role for maternal plasma volume
                                                                                   in fetal growth. Based on the results of their clinical studies,
 The effect of maternal zinc supplement on infant birth weight                     Rosso et al. (22) proposed that in underweight women,
             by body mass index (BMI) categories                                   a low plasma volume during early pregnancy will result in
                                                                                   a proportionately reduced cardiac output. A lower cardiac
             Zinc supplement            Placebo                                    output would result in a lower uteroplacental blood flow and
                  group                  group               Difference            hence a decrease in transfer of nutrients to the fetus and
  BMI              Birthweight,          Birthweight,    Birthweight,              a reduction in fetal growth.
category    No.         g         No.         g               g           p            Some evidence shows that in underweight women, micro-
                                                                                   nutrient intake during pregnancy may be associated with
,19.8        20        2997        23         23               425        .11      maternal plasma volume and infant birth weight. In a supple-
19.8–26.0   116        3224       109        109               186        .04      mentation study conducted in Chile by Mardones-Santander et
26.1–29.0    46        3279        37         37                52        .74
.29         108        3223       108        108               ÿ44        .60
                                                                                   al. (25) in underweight women (mean BMI 5 20.2), infant birth
                                                                                   weight was significantly higher in the group that received
   BMI calculated as kg/m2.                                                        energy (milk powder) and a micronutrient supplement than the
   Used with permission from reference 11.                                         group that received energy supplement alone. Also, the
1740S                                                        SUPPLEMENT

percentage of IUGR infants was significantly lower in the group                               LITERATURE CITED
that received energy plus a micronutrient supplement than the
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supplement (26). These investigators suggested that in              Gynecol. 96: 194–200.
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                                                                    Hispanic population. Obstet. Gynecol. 84: 565–573.
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    In a recent prospective study conducted in India in             weight. Obstet. Gynecol. 86: 163–169.
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consumption of foods rich in micronutrients (vitamins A and                8. Kramer, M. S., Coates, A. L., Michoud, M. C., Dagenais, S., Hamilton, E. F.
C, folacin, calcium and iron) whereas energy and protein            & Papageorgiou, A. (1995) Maternal anthropometry and idiopathic preterm
                                                                    labor. Obstet. Gynecol. 86: 744–748.
intakes were not associated with birth size (27). Women who                9. Wen, S. W., Goldenberg, R. L., Cutter, G. R., Hoffman, H. J. & Cliver,
consumed green leafy vegetables, fruits or milk products 3–4        S. P. (1990) Intrauterine growth retardation and preterm delivery: prenatal risk
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                                                                          10. Nestel, P. & Rutstein, S. (2002) Defining nutritional status of women in
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weight (green leafy vegetables: 2742 vs. 2601 g, fruits: 2721 vs.         11. Goldenberg, R. L., Tamura, T., Neggers, Y., Copper, R. L., Johnston,
2598 g, milk products: 2704 vs. 2618 g). Because the mean           K. E., Dubard, M. B. & Hauth, J. C. (1995) The effect of zinc supplementation on
birth weight in this study was low (mean 5 2665, SD 6 358 g),       pregnancy outcome. JAMA 274: 463–468.
                                                                          12. Goldenberg, R. L., Hauth, J. C., DuBard, M. B., Copper, R. L. & Cutter,
an increase in birth weight of 139, 122 and 86 g with increased     G. R. (1995) Fetal growth in women using low-dose aspirin for the prevention of
consumption of micronutrient-rich green leafy vegetables, fruits    preeclampsia: effect of maternal size. J. Matern. Fetal Med. 4: 218–224.
and milk products, respectively, is of biological significance.            13. Cliver, S. P., Goldenberg, R. L., Cutter, G. R., Hoffman, H. J., Copper,
                                                                    R. L., Gotlieb, S. J. & Davis, R. O. (1992) The relationships among psychosocial
Thus, in undernourished women with low prepregnancy BMI,            profile, maternal size, and smoking in predicting fetal growth retardation. Obstet.
a lack of association of birth weight with energy and protein       Gynecol. 80: 262–267.
intakes but a strong association with micronutrient intakes               14. Seshadri, S. (2001) Prevalence of micronutrient deficiency particularly
                                                                    of iron, zince and folic acid in pregnant women in South East Asia. Br. J. Nutr. 85:
suggests that micronutrients may be one of the limiting factors     S87–S92.
for fetal growth.                                                         15. Black, R. E. (2001) Micronutrients in pregnancy. Br. J. Nutr. 85: S193–
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                                                                          16. Bendich, A. (2001) Micronutrients in women’s health and immune
prepregnancy BMI is a significant predictor of fetal growth.         function. Nutrition 17: 858–867.
The effect of some protective factors (aspirin use and zinc               17. Scholl, T. O., Hediger, M. L., Schall, J. I., Woolcott, K. S. & Krueger, P. M.
supplements) on IUGR and preterm birth is largely present in        (1997) Use of multivitamin/mineral prenatal supplements: Influence on the
                                                                    outcome of pregnancy. Am. J. Epidemiol. 146: 134–141.
women with a low prepregnancy BMI. By contrast, a higher                  18. Block, G. & Abrams, B. (1993) Vitamin and mineral status of women of
prepregnancy BMI seems to protect against factors such as           childbearing potential. Ann. N. Y. Acad. Sci. 678: 244–254.
smoking and stress that reduce birth weight.                              19. Onis, M., Villar, J. & Gulmezoglu, M. (1998) Nutritional interventions to
    In developing countries, where deficiencies of multiple          prevent intrauterine growth retardation: evidence from randomized controlled trail.
                                                                    Eur. J. Clin. Nutr. 52: S83–S93.
micronutrients are common, some evidence indicates that                   20. Ramakrishnan, U., Manjrekar, R., Rivera, J., Gonzales-Cossio, T. &
increasing micronutrient intakes, either by supplementation         Martorell, R. (1999) Micronutrients and pregnancy outcome: A review of the
or by increased consumption of micronutrient-rich foods, is         literature. Nutr. Res. 19: 103–159.
                                                                          21. Rosso, P., Donoso, E., Braun, S., Espinoza, R. & Salas, S. P.
associated with significant increase in birth size and a reduction   (1992) Hemodynamic changes in underweight pregnant women. Obstet.
of IUGR in women with a low prepregnancy BMI. It is plausible       Gynecol. 79: 908–912.
that in these undernourished women both low prepregnancy                  22. Rosso. P. & Salas, S. P. (1994) Mechanisms of fetal growth re-
                                                                    tardation in the underweight mother. In: Nutrient regulation during pregnancy,
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micronutrient status. This combination may thus result in           Plenum Press, New York.
a decreased transfer of nutrients from mother to fetus and may            23. Rosso, P. (1985) A new chart to monitor weight gain during pregnancy.
                                                                    Am. J. Clin. Nutr. 41: 644–649.
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    In conclusion, there is need for                                and birth weight. Am. J. Obstet. Gynecol. 154: 503–509.
                                                                          25. Mardones-Santander, F., Rosso, P., Stekel, A., Ahumada, E., Llaguno, S.,
 research to further clarify the mechanism of association          Pizarro, F., Salinas, J., Vial, I. & Walter, T. (1988) Effect of milk-based food
  between prepregnancy BMI and IUGR and preterm delivery            supplement on maternal nutritional status and fetal growth in underweight Chilean
                                                                    women. Am. J. Clin. Nutr. 47: 413–419.
  and                                                                     26. Mardones-Santander, F. (1999) Nutritional intervention to prevent
 well-designed randomized controlled trials in high-risk           intrauterine growth retardation: evidence from randomized controlled trials. Letter
  women with low prepregnancy BMI, preferably in de-                to the editor. Eur. J. Clin. Nutr. 53: 970–971.
  veloping countries (where multiple micronutrient deficien-               27. Rao, S., Yajnik, C. S., Kanade, A., Fall, C. H. D., Margetts, B. M., Jackson,
                                                                    A. A., Shier, R., Joshi, S., Rege, S., Lubree, H. & Desai, B. (2001) Intake of
  cies are common) to evaluate the role of micronutrients           micronutrient-rich foods in rural Indian mothers is associated with size of their
  related to poor pregnancy outcomes.                               babies at birth: Pune maternal nutrition study. J. Nutr. 21: 1217–1224.

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Description: BMI (body mass index, referred to as body mass index, also known as body mass index, referred to as BMI), is the weight in kilograms divided by height with the number of squares that the number of meters, is commonly used to measure the international level, and whether the body fat, thin, healthy a standard. Mainly used for statistical purposes, when we need to compare and analyze a person's body weight for different heights of people about the health effects, BMI value is a neutral and reliable indicators.