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nature publishing groupORIGINAL CONTRIBUTIONS

Preeclampsia is commonly defined as hypertension afer 20 ges-tational weeks combined with proteinuria. Maternal metabolicrisk actors are known to increase the risk o both early- andlate-onset preeclampsia, but there are also differences betweenthe two subgroups. Early-onset preeclampsia is believed to bemore o a placental disease and thus more dependent on under-lying abnormal placentation,1,2 while late-onset preeclamp-sia is thought to be a mainly maternal metabolic disease.14Especially, early-onset preeclampsia is a leading cause o mor-bidity and mortality among mothers and inants,5,6 due toincreased risks o maternal cardiovascular complications, intra-uterine growth restriction and preterm birth.4

Cardiovascular disease and preeclampsia share constitu-tional risk actors, such as obesity, hyperlipidemia, hyperten-sion, and increased blood glucose levels.7 Women who havehad preeclampsia are at increased risk o developing cardiovas-cular disease later in lie.810Long-term risk o cardiovascular

disease has been shown to be especially high i a woman hadrecurrent preeclampsia, early preeclampsia or i the diseaseappeared or the first time in a multiparous woman.11

High body mass index (BMI) is an important risk actor orboth preeclampsia12,13and cardiovascular disease.14,15Obesityprevalence is increasing at an alarming rate in both high- andlow-income countries.16Te prevalence o obesity in Europeanwomen ranges rom 1025%.16 Te risk o preeclampsia hasbeen shown to increase with an increasing BMI, with the lowestprevalence among underweight women.17 In a recent Britishstudy, extremely obese women were shown to have a ouroldincreased risk o developing preeclampsia, compared to womeno normal weight.18 Studies have shown that the incidence opreeclampsia is increasing in the United States,19,20which maybe attributed to an increase in underlying risk actors, such asobesity, diabetes, and chronic hypertension.19,21

Few have investigated the effects o maternal BMI on risks oearly and late preeclampsia separately.2225Tese studies showdiverging results, with some showing that obesity and over-weight are risk actors or late, but not early, preeclampsia.24,25It has shown that the risk o severe preeclampsia is increasedin women with a high pre-pregnancy BMI.17,26,27

Women o short stature are supposed to have an increasedrisk o cardiovascular disease.28Only a ew studies have inves-tigated i short stature also is a risk actor or preeclampsia,29,30

1Department of Womens and Childrens Health at Uppsala University, Uppsala,Sweden; 2Department of Medicine, Clinical Epidemiology Unit at KarolinskaInstitutet, Stockholm, Sweden; 3Department of Woman and Child Health,Division of Obstetrics and Gynecology, Karolinska University Hospital andInstitutet, Stockholm, Sweden. Correspondence: Sara Sohlberg([email protected])

Received 14 April 2011; first decision 22 May 2011; accepted 4 August 2011.

2012 American Journal of Hyper tension, Ltd.

Maternal Body Mass Index, Height, and Risks of

PreeclampsiaSara Sohlberg1, Olof Stephansson2,3, Sven Cnattingius2and Anna-Karin Wikstrm1,2

BACKGROUND

There is an association between maternal body mass index (BMI) and

preeclampsia, but if BMI has an effect on preeclampsia of all severities

is debated. If there is an association between maternal height and

preeclampsia of all severities is unknown.

METHODS

In this population-based cohort study including 503,179 nulliparouswomen, we estimated risks of preeclampsia of different severity in

short (

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ORIGINAL CONTRIBUTIONSMaternal BMI, Height, and Risks of Preeclampsia

and only one study has been able to show a correlation betweenheight and preeclampsia,30with only an increased risk o severepreeclampsia in short, compared to tall, multiparous women.

Based on the hypotheses o differences in underlying patho-physiology in early and late preeclampsia, we hypothesizedthat a high BMI and short stature are associated with both sub-

sets o disease, but with a stronger association between highBMI and late preeclampsia and between short stature and earlypreeclampsia.

In the present nationwide Swedish study, we included morethan 500,000 women with first births between 1992 and 2006.Using this data set, we estimated the effects o a high BMI andshort stature on risk o preeclampsia o different severity.

METHODS

We used inormation rom the population-based SwedishMedical Birth Register to define the study population. o increasethe homogeneity o the study population, we only included prim-iparous women born in the Nordic countries (Sweden, Norway,

Denmark, Finland, or Iceland) who delivered a singleton inantin gestational week 22 or later, without congenital malormation,during the years 19922006 (n= 503,179). We excluded womenwith gestational hypertension (n = 6,182). Te Birth Registercontains data on more than 98% o all births in Sweden31andincludes prospectively collected demographic data, inorma-tion on reproductive history and complications that occur dur-ing pregnancy, delivery, and the neonatal period. By means oeach individuals unique national registration number, the BirthRegister can be linked with other Swedish data sources.

At the time o registration or antenatal care, which occursbeore the 15th week o gestation in more than 95% o the

pregnancies,31 inormation about demographic data, BMI,height, and smoking habits are collected by midwies. We useddata on maternal height and divided our population into quar-tiles and stated the shortest quartile as short and the highestquartile as tall. Te upper cutoff or the lowest quartile wasbetween 163 and 164 cm in our cohort, and the lower cutoffor the highest quartile was between 171 and 172 cm. We chose164171 cm as normal height in our model.

BMI (weight (kg)/height (m)2) was calculated and catego-rized into underweight (18.4); normal (18.524.9); over-weight (25.029.9); obese class I (30.034.9); and obese classIIIII (35.0) according to the definitions o the World HealthOrganization.32Inormation on maternal height was missingin 8% (n= 39,489) o the study population, and we were notable to calculate BMI in 16% (n= 81,337) o the women.

Complications during pregnancy and delivery were classifiedaccording to the International Classification o Diseases, ninthand tenth versions (ICD-9 and ICD-10), as noted by the respon-sible doctor at discharge rom hospital. Mild to moderate preec-lampsia was identified by the ICD-9 and ICD-10 codes 642 E,O140, and O149; and severe preeclampsia, including eclamp-sia, by the ICD-9 and ICD-10 codes 642G-F, O141-2, and O15.Te clinical definition o preeclampsia is a rise in blood pres-sure (140/90) combined with proteinuria (0.3 g/24 h), andthe disease is defined as severe i the diastolic blood pressure

rises above 110 mm Hg and/or the proteinuria exceeds 5 g/24 h.We classified women with preeclampsia by severity o dis-ease. First, we categorized pregnancies with preeclampsia intothree groups based on gestational length at birth. Te ollow-ing categories were used: term preeclampsia, including womenwith preeclampsia who gave birth afer 37 gestational weeks

or more; moderate early preeclampsia, including women withpreeclampsia who gave birth afer 3236 weeks; and very earlypreeclampsia, including women with preeclampsia who gavebirth beore gestational week 32. In Sweden, gestational age isassessed by ultrasound scans in 95% o women, usually aroundthe 17th week o gestation.33I no early second trimester ultra-sound scan was available, the last menstrual period was usedto calculate gestational age at delivery. Second, we categorizedpregnancies with preeclampsia as either mild/moderate orsevere preeclampsia according to the ICD codes. Te qualityo the diagnose preeclampsia has previously been validated: o148 pregnancies coded as preeclampsia in the birth registry, 137(93%) had the disease according to the individual records.31

We used inormation on amily situation, smoking habits,and chronic diseases rom the first antenatal visit. Tis inor-mation is recorded in a standardized manner, with check boxes.Family situation is categorized into living or not living withthe inants ather, and smoking habits into nonsmoker, lightsmoker (19 cigarette/day) and heavy smoker (10 cigarettes/day). Women with chronic disease were identified either by thecheck boxes rom the first antenatal visit and/or by diagnosesregistered at hospital discharge afer delivery by use o the ol-lowing ICD-9 and ICD-10 codes: hypertension 642A-C; 642H;O10; O11; diabetes mellitus 250; 648A; O240; O241; O243;chronic renal disease 581; 582; N03; N04; and systemic lupus

erythematosus 710A; M32. Inormation about maternal agewas collected when the woman was discharged rom the hospi-tal and categorized into 19 years or younger, 2024 years, 2529years, 3034 years, and 35 years or older. Te years o ormaleducation (categorized into up to 9 years, 1012 years, and 13years or more) and mothers country o birth were obtainedby linking the Birth Register to the Education Register and theRegister o otal Population, respectively, both held by StatisticsSweden. Te study was approved by the research ethics com-mittee at Karolinska Institutet, Stockholm, Sweden.

Statistical analysis. We examined the effects o maternal heightand BMI on the risk o developing preeclampsia o differentseverity. Odds ratios (OR) with 95% confidence intervals (CI)were estimated using multiple logistic regression, and normalheight (164171 cm) and BMI (18.524.9) were used as reer-ence. We adjusted the analysis or maternal age, years o ormaleducation, smoking habits and presence o chronic hyperten-sion, diabetes mellitus (pregestational or gestational), chronicrenal disease, and systemic lupus erythematosus. When calcu-lating effect o maternal height, we adjusted or maternal BMIand vice versa. We also calculated the effect on risks or di-erent types o preeclampsia per increasing BMI unit and perdecreasing height in cm by using BMI and height as continu-ous variables in the model, adjusting or the other variables as

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ORIGINAL CONTRIBUTIONS Maternal BMI, Height, and Risks of Preeclampsia

categorized variables. Further, within women with preeclampsia,we also calculated i risks related to maternal stature or mater-nal BMI were more associated with mild/moderate than severepreeclampsia, also adjusting or the other variables categorizedvariables. All analyses were perormed using the StatisticalAnalysis Sofware version 9.2 (SAS Institute, Cary, NC).

RESULTS

Preeclampsia affected 4.8%. O the women who developedpreeclampsia, 3.7% developed term preeclampsia, 0.9% mod-erate early preeclampsia, and 0.2% early preeclampsia. Tecorresponding rates or mild/moderate and severe preeclamp-sia were 3.2% and 1.6%, respectively.

Every ourth woman in the study had a BMI above normal(i.e., 25.0); 17.7% were overweight (BMI 25.029.9), 4.8%obese class I (BMI 30.034.9), and 1.7% obese class IIIII(BMI 35.0) (Table 1).

Table 1presents the associations between maternal charac-teristics and term preeclampsia, moderate early preeclampsia,

and early preeclampsia. Te rates o preeclampsia o differ-ent gestational lengths increased with increasing maternalage and BMI. Increasing maternal height was associated withdecreasing rates o preeclampsia. Compared with women with12 years education or less, women with more years o ormaleducation had lower rates o preeclampsia. Smokers had lowerrates o preeclampsia, although smokers seemed less protectedrom early than late preeclampsia. Women with pregestationaland gestational diabetes, chronic renal disease, and systemiclupus erythematosus had increased rates o preeclampsia.Women with chronic hypertension had especially increasedrates o early preeclampsia.

Table 2 presents maternal height and BMI and risks opreeclampsia o different gestational lengths. Compared withwomen o normal height, women o short stature had higherrisks and women o tall stature had lower risks o term, mod-erate early, and early preeclampsia. Te association was espe-cially strong between maternal height and early preeclampsia.Te risks o term, moderate early, and early preeclampsiaincreased with increasing BMI. Compared with women withnormal BMI, women with obesity class IIIII aced a threeoldto a ourold higher risk o developing term, moderate early,and early preeclampsia.

Table 3presents maternal height and BMI and risks o mild/moderate and severe preeclampsia. Compared with women onormal stature, women o short stature had higher risks andwomen o tall stature had lower risks o both mild and severepreeclampsia. Tese associations were slightly stronger orsevere than or mild to moderate preeclampsia. Te risks oboth mild and severe preeclampsia increased with increasingBMI. Te associations between increasing BMI and preec-lampsia risks seemed stronger or mild to moderate than orsevere preeclampsia. Specifically, obesity class IIIII (BMI35.0) was associated with a ourold increased risk o mild tomoderate preeclampsia (adjusted OR 4.04; 95% CI 3.744.36)and a threeold increased risk o severe preeclampsia (adjustedOR 2.99; 95% CI 2.663.35).

Table 1 | Rates of term (37 weeks), moderate early (3236

weeks), and early preeclampsia (12 146,921 3.23 0.75 0.21 Missing 1,014 4.04 0.59 0.20

Smoking

No 409,174 3.88 0.87 0.23

19 cigarettes/day

46,124 2.81 0.61 0.21

10 cigarettes/day

17,828 2.40 0.61 0.18

Missing 30,051 3.37 1.18 0.47

Diabetes

No 497,651 3.63 0.82 0.24

Gestational 2,861 8.35 2.06 0.52

Pregestational 2,667 10.72 7.20 0.82

Chronic hypertension

No 500,293 3.66 0.84 0.23

Yes 2,886 10.53 4.26 2.08

Chronic kidney disease

No 501,000 3.69 0.85 0.24

Yes 2,179 4.82 1.97 0.69

Systemic lupus erythematosus

No 502,637 3.69 0.86 0.24

Yes 542 4.98 1.66 1.85aAt the time of registration for antenatal care, which occurs before the 15th week ofgestation in more than 95% of the pregnancies.
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Te risk o mild to moderate preeclampsia decreased 0.8%(95% CI 0.61.1) per cm and increased 9.5% (95% CI 9.19.8) per BMI unit, whereas the risk o severe preeclampsiadecreased 2.2% (95% CI 1.82.6) per cm and increased 7.0%(95% CI 6.57.5) per BMI unit.

Among women with preeclampsia, risk o severe preeclamp-sia increased with decreasing maternal height, while risk omild/moderate preeclampsia increased with increasing mater-nal BMI (P< 0.001 and P< 0.001, respectively). Tere was nostatistically significant interaction between maternal heightand BMI with respect to risk o preeclampsia (P= 0.21).

DISCUSSION

We ound that not only maternal BMI, but also maternalheight is associated with preeclampsia o all severities. A short

maternal stature was oremost associated with increased riskso the more severe types o preeclampsia, while overweightand obesity were closer associated with the milder orms opreeclampsia.

Tis is to our knowledge the first study showing an associa-tion between maternal height and preeclampsia o all sever-ity. One previous study has shown an association betweenmaternal height and the risk o severe preeclampsia, but onlyin multiparous and not in primiparous women.30 Since theassociation both in our and in their study is not that strong,the difference in cohort size (60,000 vs. 500,000) might at leastin part explain why we in our study were able to show corre-lation between maternal height and all types o preeclampsiain primiparous women. Inants born small or gestational agehave an increased risk o short final stature, although most o

Table 2 | Risks of term, moderate early, and early preeclampsia based on maternal height or BMI

Term preeclampsia(>37 weeks) (N= 15,894)

Moderate early preeclampsia(3236 weeks) (N= 3,598)

Early preeclampsia(

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ORIGINAL CONTRIBUTIONS Maternal BMI, Height, and Risks of Preeclampsia

them catch up in height during childhood.34According to thehypothesis o Developmental Origins o Health and Disease,a poor nutrition in uterocan result in etal adaptation whichleads to survival gains in uteroand in inancy, but also to long-term increased risks o metabolic and cardiovascular diseases,including pregnancy complications such as preeclampsia in

adulthood.

3537

Tis can be a reason why both short womenand women with preeclampsia have an increased risk o uturecardiovascular disease.9,10,28In a recent study by Zhang et al.,it has been shown that inants born by short statured womenhave an increased risk o perinatal mortality which is partlymediated through small or gestational age birth.38Both smallor gestational age birth and early preeclampsia are associatedwith abnormal placentation and thereore, the study by Zhanget al.and our study both support an association between shortmaternal stature and abnormal placentation.

Being overweight or obese is a well-known risk actor orpreeclampsia12,13,17,18,23,29and the risk increases with increas-ing BMI.13,17,23,29 Te associations between overweight and

obesity and preeclampsia o different severity are less stud-ied.17,22,23,26,27 We ound positive associations betweenincreasing BMI and risks o preeclampsia o different severityand gestational lengths, and risks related to a high BMI wereslightly higher or the milder orms o preeclampsia. Tis is inagreement with two recent reports,22,23while two other reportsound that a high BMI was only a risk actor or late24,25 ormild preeclampsia.24Another study ound a stronger associa-tion between increasing BMI and severe than mild preeclamp-sia.13Limited sample sizes24,25or a broader definition o severepreeclampsia24 may have contributed to these findings. Ourfinding, that BMI seems to have a stronger association to late

or mild preeclampsia, is compatible with the two stage modelo preeclampsia, in which early and or severe preeclampsia isthought to originate to a larger extent in abnormal placenta-tion, and less by maternal metabolic actors such as BMI, whilelate/mildmoderate preeclampsia is thought to be more o amaternal, metabolic disease.2,29

Te strengths and limitations o the present study are con-stituted in the registry-based design. Te included variablesrom the Swedish Medical Birth Register have been validatedand have been shown to be reliable.31o increase the homoge-neity o the study population (and reduce the risks o residualconounding), we restricted the study to primiparous womenborn in Nordic countries. Te large nationwide cohort enabledus to look at preeclampsia o different gestational lengths anddifferent severity. Since maternal care is provided ree o chargeor all women in Sweden and home deliveries are very rare,selection bias is unlikely. Further, since data were collectedprospectively, recall bias is precluded. In contrast to previousstudies, our data are relatively recent,13 and the gestationallength was based on a routine ultrasound examination in earlysecond trimester and not the last menstrual period.13,23A limi-tation o the study is that the diagnoses o mild/moderate andsevere preeclampsia have not been validated in the SwedishMedical Birth Register, though the diagnosis o preeclampsiahas, with high accuracy. Further, adult height is influenced by

environmental and socioeconomic actors. We adjusted orsmoking and years o education, but an effect o unmeasuredactors cannot be excluded.

In conclusion, we ound an association between shortmaternal stature and preeclampsia, especially early preeclamp-sia. We urther ound an association between a high BMI and

preeclampsia o all severities, but especially with the milderorms o preeclampsia. Tese findings correspond well withthe hypothesis o two subsets o preeclampsia, the early-onsetdisease with a predominantly placental and genetic origin andthe late-onset disease with a stronger metabolic origin.

Acknowledgments: This study was funded by Gillbergska foundation,Regional Research Council in the Uppsala-rebro region (project No.25531), Swedish Society of Medicine (project No. 101291 and 97321).The study was approved by one of the Regional Ethical Review Boards inStockholm, Sweden. Reference number: 2008/1182. Date of approval: 3September 2008.

Disclosure: The authors declared no conflict of interset.

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