CLINICIAN’S CORNERCLINICAL REVIEW

Pregnancy and FertilityFollowing Bariatric SurgeryA Systematic ReviewMelinda A. Maggard, MD, MSHSIrina Yermilov, MD, MPHZhaoping Li, MD, PhDMargaret Maglione, MPPSydne Newberry, PhDMarika Suttorp, MSLara Hilton, BAHeena P. Santry, MDJohn M. Morton, MD, MPHEdward H. Livingston, MDPaul G. Shekelle, MD, PhD

OBESITY HAS REACHED EPI-demic levels in the UnitedStates and is a leading causeof health-related disor-

ders.1-14 Rates of surgical weight loss pro-cedures have grown steeply and womenaccount for many of these patients.15

Large numbers of women in their child-bearing years may undergo bariatric sur-gery, which may change fertility follow-ing weight loss, alter nutritionalrequirements during pregnancy, or im-pact contraception to prevent preg-nancy. Our specific goals were to esti-mate the incidence of bariatric surgeryin women aged 18 to 45 years and per-form a systematic review to assess asso-ciations of bariatric surgery on preg-nancy outcomes, including maternal andneonatal outcomes, nutritional adverseevents, fertility, contraception, optimaltime to delay pregnancy, and surgicalcomplications during pregnancies.

CME available online atwww.jamaarchivescme.comand questions on p 2318.

Author Affiliations: Rand Corporation, Santa Monica,California (Drs Maggard, Newberry, and Shekelle andMss Maglione, Suttorp, and Hilton); Department ofSurgery, David Geffen School of Medicine, Univer-sity of California, Los Angeles (Drs Maggard, Yermi-lov, Li, and Shekelle, and Mss Maglione); VA GreaterLos Angeles Healthcare System, Los Angeles, Califor-nia (Drs Yermilov, Li, and Shekelle); Departmentof Surgery, Massachusetts General Hospital, Boston(Dr Santry); Department of Surgery, Stanford Schoolof Medicine, Palo Alto, California (Dr Morton); and

Department of Surgery, University of Texas South-western School of Medicine, Dallas (Dr Livingston).Corresponding Author: Melinda A. Maggard, MD,MSHS, Department of Surgery, David Geffen Schoolof Medicine, University of California, Los Angeles, CHS72-215, 10833 Le Conte Ave, Los Angeles, CA 90095(mmaggard@mednet.ucla.edu).Clinical Review Section Editor: Mary McDermott, MD.We encourage authors to submit papers for consid-eration as a Clinical Review. Please contact MaryMcDermott, MD, at mdm608@northwestern.edu.

Context Use of bariatric surgery has increased dramatically during the past 10 years,particularly among women of reproductive age.

Objectives To estimate bariatric surgery rates among women aged 18 to 45 yearsand to assess the published literature on pregnancy outcomes and fertility after surgery.

Evidence Acquisition Search of the Nationwide Inpatient Sample (1998-2005) andmultiple electronic databases (Medline, EMBASE, Controlled Clinical Trials Register Da-tabase, and the Cochrane Database of Reviews of Effectiveness) to identify articlespublished between 1985 and February 2008 on bariatric surgery among women ofreproductive age. Search terms included bariatric procedures, fertility, contraception,pregnancy, and nutritional deficiencies. Information was abstracted about study de-sign, fertility, and nutritional, neonatal, and pregnancy outcomes after surgery.

Evidence Synthesis Of 260 screened articles, 75 were included. Women aged 18to 45 years accounted for 49% of all patients undergoing bariatric surgery (�50 000cases annually for the 3 most recent years). Three matched cohort studies showed lowermaternal complication rates after bariatric surgery than in obese women without bar-iatric surgery, or rates approaching those of nonobese controls. In 1 matched cohortstudy that compared maternal complication rates in women after laparoscopic adjust-able gastric band surgery with obese women without surgery, rates of gestational dia-betes (0% vs 22.1%, P� .05) and preeclampsia (0% vs 3.1%, P� .05) were lower inthe bariatric surgery group. Findings were supported by 13 other bariatric cohort stud-ies. Neonatal outcomes were similar or better after surgery compared with obese womenwithout laparoscopic adjustable gastric band surgery (7.7% vs 7.1% for premature de-livery; 7.7% vs 10.6% for low birth weight, P� .05; 7.7% vs 14.6% for macrosomia,P� .05). No differences in neonatal outcomes were found after gastric bypass com-pared with nonobese controls (26.3%-26.9% vs 22.4%-20.2% for premature deliv-ery, P=not reported [1 study] and P=.43 [1 study]; 7.7% vs 9.0% for low birth weight,P=not reported [1 study]; and 0% vs 2.6%-4.3% for macrosomia, P=not reported [1study and P=.28 [1 study]). Findings were supported by 10 other studies. Studies re-garding nutrition, fertility, cesarean delivery, and contraception were limited.

Conclusion Rates of many adverse maternal and neonatal outcomes may be lowerin women who become pregnant after having had bariatric surgery compared withrates in pregnant women who are obese; however, further data are needed from rig-orously designed studies.JAMA. 2008;300(19):2286-2296 www.jama.com

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EVIDENCE ACQUISITIONAnalysis of Trendsin Surgery UtilizationThe Nationwide Inpatient Sample,16 aHealthcare Cost and Utilization Projectdata set, was used to produce nationalestimates of trends in bariatric surgi-cal procedures between 1998 and 2005,the latest year for which data are avail-able. The Nationwide Inpatient Sampleis a 20% stratified sample of all inpa-tient stays nationally and includes dataon 5 million to 8 million hospitaliza-tions from roughly 1000 hospitals.

A comprehensive list of Interna-tional Classification of Diseases, NinthRevision procedure codes was usedto identify patients who underwent bar-iatric surgery, accounting for changesin coding and types of procedures.17

Rates of bariatric cases were calcu-lated for each year. We determined thenumber of procedures among men andwomen aged 18 to 45 years. Percent-age change from 1998 was calculatedfor each subsequent year.

Literature Search

Our literature search included Med-line, EMBASE, Controlled ClinicalTrials Register Database, and the Coch-rane Database of Reviews of Effective-ness and captured articles published be-tween 1985 and February 2008. Articleson bariatric surgery, including laparo-scopic adjustable gastric banding(LAGB), vertical-banded gastroplasty(VBG), Roux-en-Y gastric bypass (gas-tric bypass), and biliopancreatic diver-sion/duodenal switch (BPD), were in-cluded. We used various search termsfor each procedure (eg, Roux-en-Y gas-tric bypass: gastric bypass, RYGB, lapa-roscopic gastric bypass, and open gas-tric bypass). We also searched forfertility, contraception, pregnancy,weight management, neonatal out-comes, and nutritional deficiencies.

Study Inclusion

The literature search included review ar-ticles, randomized controlled trials, ob-servational studies, and case reports. Tobe included, studies had to be an origi-nal research article and discuss 1 of the

procedures and fertility or pregnancyoutcomes. Two reviewers (M.A.M. andZ. L.) reviewed each study. Disagree-ments were resolved by consensus.

Data Abstraction and Synthesisof Results

Study results were abstracted into datatables. Because of heterogeneity in thepatients, interventions, and out-comes, data pooling was not possible.Therefore, we summarized the data nar-ratively. Outcomes included maternalpregnancy outcomes (gestational dia-betes, hypertension, preeclampsia, ce-sarean delivery, nutritional deficien-cies, surgical complications, andmaternal weight gain), neonatal out-comes (premature delivery, birthweight, macrosomia, and perinatal mor-tality), fertility, the optimal time be-tween surgery and pregnancy, and con-traception efficacy.

Because we found no randomizedtrials, our evidence consisted of obser-vational studies. We discriminatedbetween studies based on how casesand comparison groups were identi-fied. We considered a study less proneto bias, and consequently gave it moreemphasis, if it enrolled a consecutiveor random sample of surgery casesor pregnancies and used a concurrentcomparison group that consistedof consecutive, random, or matchedpatients or pregnancies. Data pre-sented herein included all cohortstudies with a comparison group.Studies without a comparison group,case series, and case reports wereused for descriptions of surgical com-plications or rare adverse events or toprovide additional information aboutour study questions. Nutritionaloutcomes included both cohort andcase series studies. A RAND bio-statistician performed the statisticalanalyses (M.S.).

EVIDENCE SYNTHESISIncidence of Bariatric SurgeryAmong Women of Reproductive Age

The incidence of bariatric surgery in theUnited States increased by 800% be-tween 1998 and 2005 (from 12 480 to

113 500 cases). Women accounted for83% of procedures in the 18- to 45-year age group. Between 2003 and 2005,more than 50 000 women aged 18 to 45years underwent inpatient bariatric sur-gery procedures annually (49% of allbariatric surgery cases). The number ofinpatient bariatric procedures de-creased in 2005. Reasons for the lowersurgery rate in 2005 are unknown butcould include a shift to bariatric sur-gery in the outpatient setting, which isnot captured by the Nationwide Inpa-tient Sample.

Description of the StudiesIdentified by the Literature Search

Our search identified 1102 articles, ofwhich 260 were screened and of which75 were included in the review(FIGURE). One randomized controlledtrial comparing surgical procedures wastreated as a case series for pregnancyoutcomes. Of the 185 excluded ar-ticles, 88 did not study bariatric sur-gery, 60 did not study a procedure ofinterest or did not include pregnantwomen, and 37 were review articles.

Three cohort studies by Ducarme etal,18 Wax et al,19 and Patel et al20 com-pared outcomes for consecutive pa-tients with postsurgery pregnancies(bariatric surgery group) with out-comes for consecutive nonsurgical pa-tients (comparison group) who deliv-ered in the same period and werematched to 1 or more characteristics(eg, body mass index [BMI, calculatedas weight in kilograms divided by heightin meters squared], age). Because thesestudy designs are more rigorous, wepresent their results in detail.

The remaining cohort studies com-pared outcomes in selected pregnan-cies after bariatric surgery with out-comes in pregnancies before bariatricsurgery (same women before sur-gery), selected nonobese patients, orpopulation rates.

Risks for Pregnancies:Maternal Outcomes

Sixteen studies compared pregnanciesfollowing bariatric surgery with a com-parison group.18-33 The most com-

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monly reported maternal outcomeswere gestational diabetes, preeclamp-sia, pregnancy-induced hypertension,maternal weight gain, and cesarean de-livery (TABLE 1).

Laparoscopic Adjustable GastricBanding. Ducarme et al18 compared theoutcomes of 13 consecutive deliveriesfollowing LAGB surgery with out-comes of 414 consecutive patients whowere obese (BMI �30) who deliveredat the same practice between 2004 and2006. Gestational diabetes (0% vs22.1%, P� .05) and preeclampsia (0%vs 3.1%, P� .05) were lower in the bar-iatric surgery group than in the obesecomparison group, but there were nodifferences in pregnancy-induced hy-pertension or need for labor induc-tion. Maternal weight gain was re-duced in the surgical group (5.5 vs 7.1kg, P� .05).

Three additional LAGB studies,21-23

which compared outcomes to selectedobese patients who did not undergo sur-gery or to historical presurgery preg-nancies, also found lower rates of ges-tational diabetes, preeclampsia, andmaternal weight gain, but in additionfound lower rates of pregnancy-induced hypertension in the bariatricsurgery group. One study21 reportedthat outcome rates for the surgery groupapproached rates in the community. Thefindings were supported by 6 case se-ries that reported low rates of these ma-ternal outcomes in pregnancies follow-ing LAGB.34-39

Gastric Bypass. Two cohort studiesreported on maternal outcomes follow-ing gastric bypass.19,20 Both reported onconsecutive deliveries following bariat-ric surgery in a single practice. Wax etal19 compared outcome rates for the bar-iatric surgery group with a comparisongroup consisting of the next 2 consecu-tive deliveries after the index case,matched for age and prior cesarean de-livery. Patel et al20 compared outcomesfollowing surgery with a comparisongroup consisting of the 5 consecutivenonsurgical women who delivered be-fore and the 5 consecutive nonsurgicalwomen who delivered after each indexcase, stratifying by obesity. Wax et al19

found a higher risk of pregnancy-induced hypertension in the bariatric sur-gery group compared with the nonsur-gical comparison group. However,women with bariatric surgery were moreobese than the comparison group, with68% and 26%, respectively, having a BMIof 30 or higher (P� .001). There wereno differences between the 2 groups inrates of gestational diabetes or weightgain. Patel et al20 found that rates of ges-tational diabetes, preeclampsia, and preg-nancy-induced hypertension did not dif-fer between the bariatric surgery andcomparison cohorts.

Two additional studies comparedoutcomes after gastric bypass surgerywith presurgery pregnancies from thesame patients or with patients matchedfor presurgery weight, parity, and yearof delivery.24,25 For all outcomes, thesestudies found no differences or found

lower outcome rates in the bariatric sur-gery group compared with the controlgroup.

Among case series on gastric by-pass, only 1 study40 reported data on thematernal outcomes of interest. Thisstudy identified no occurrences of ges-tational diabetes (n=100).

VBG and BPD. Two studies of ma-ternal outcomes after VBG proceduresfound similar results to the cohort stud-ies involving LAGB and gastric bypassprocedures. One study28 reported lowrates of gestational diabetes, pregnancy-induced hypertension, and preeclamp-sia among the surgery cohort and theother study27 reported a lower rate ofgestational diabetes in comparison withpresurgery historical pregnancies. Onecohort study29 on BPD reported a lowerpregnancy-induced hypertension rateamong patients who had surgery.

Mixed Procedures. Two studies31,32

assessed pregnancy outcomes follow-ing a variety of bariatric procedures.One study31 compared pregnancy out-comes for 298 patients who under-went bariatric surgery with commu-nity rates and found a higher rate ofgestational diabetes in the surgery group(9.4% vs 5.0%, P� .001), but no dif-ference in preeclampsia. Importantly,obesity was more prevalent among pa-tients who had surgery compared withthe community (10.7% vs 1.2%,P� .001). A second study32 found lowerrates of gestational diabetes, preeclamp-sia, and pregnancy-induced hyperten-sion following surgery.

In conclusion, 3 matched cohortstudies found that adverse maternal out-comes in pregnancies following LAGBand gastric bypass may be lower thanthose outcomes of obese comparisongroups and may approach rates in pa-tients who are not obese. Additional co-hort studies and case series studies sup-port these findings. Few studies haveassessed pregnancy outcome rates afterBPD.

Rates of Cesarean Delivery andOther Delivery Complications. Thir-teen studies18-20,22-25,27-31,33 compared ce-sarean delivery rates following bariat-ric surgery with a comparison group

Figure. Flow of Eligible Studies of BariatricSurgery Among Women of ReproductiveAge

75 Articles included28 Case reports26 Case series18 Cohort studies3 Matched cohort studies

1102 Titles and/or abstractsidentified in initial search1054 via literature search

48 via reference lists

260 Reviewed

278 Articles selected and ordered

824 Excluded (topic not bariatricsurgery, pregnancy, or originalresearch)

18 Excluded10 Based on review of abstract

5 Did not involve bariatricsurgery and pregnancy

3 Were reviews orguidelines

8 Not found

2 Discussed an obsoletesurgical approach

185 Excluded88 Did not study bariatric

surgery60 Did not focus on topic

of interest30 Were nonsystemic review

articles5 Were review or meta-

analysis articles2 Were background articles

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Table 1. Observational Studies on Maternal Pregnancy Outcomes Following Bariatric Surgery

Source andSurgery Type

Inclusion Criteria

% of Patients

BariatricSurgery

Comparison(Control)

GestationalDiabetes Preeclampsiaa

Pregnancy-Induced

Hypertension Cesarean Delivery

BariatricSurgery Control

BariatricSurgery Control

BariatricSurgery Control

BariatricSurgery Control

LAGBDucarme

et al,18

2007

13 Consecutivepregnancies(delivered2004-2006)

414 Obese (BMI �30)consecutive controls(delivered2004-2006)

0 22.1b 0 3.1b 7.7 8.2 15.3 34.4c

Dixon et al,21

200579 Consecutive first

postoperativepregnancies(1995-2003)

40 Consecutivepenultimatepreoperativepregnancies

79 Controls matched forparity, age, and BMI

61 000 Community controls

6.3 15

19b

5.5

5 28b

25b

NR

10 45b

38b

10-13

NR NR

Dixon et al,22

2001dSelected sample

of 22 pregnancies264 Preoperative

pregnancies4.5 9.4 NR NR 4.5 37b 13.6 30

Skull et al,23

200449 Pregnancies

from consecutivepatients

31 Consecutive historicalpreoperativepregnancies

8 27b 2 9.6e 8.1 22.5e 28.5 16.1

Gastric bypassWax et al,19

200838 Consecutive patients 76 Controls (next 2

deliveries after indexcase), matched forage and priorcesarean

5.3 4.0 NR NR 29.0 7.9b 65.8 64.5

Patel et al,20

200826 Consecutive

pregnancies(delivered2003-2006)

254 Controls (5 deliveriesbefore and afterindex case2003-2006)188 nonobese39 obese27 severely obese

3.8

1.65.1

14.8

3.8

3.77.77.4

3.8

3.72.67.4

61.5

36.2a

46.543.5

Richardset al,24

1987

57 Pregnanciesfrom 243of 580 surveys(1979-1983)

57 Preoperativepregnancies fromsame 243 surveys,matched on weight,parity, and year

5.3 10.5 NR NR 8.8 45.6f,g 24.6 15.8

Wittgroveet al,25

1998

17 Selected patientsidentified throughbariatric newsletter

Preoperative historicalpregnancies from thesame 17 patients

0 23.5b NR NR 0 41g 35.3 35.3

Landsbergeret al,26

2006h

19 Patients(delivered2004-2006)

38 Controls19 matched forpreoperative BMI19 matched forpostoperative BMI(2004-2006)

15.842.1

21.1

Trend towardpreeclampsiain bariatric cohort(P = .051) but nodata provided

No differencenoted (datanot given)

No differencenoted (datanot given)

VBGBilenka et al,27

199514 Deliveries

(1985-1990)Preoperative historical

deliveries (n = 18)from the same 9patients

0 16.7i 7.1 5.6 15.3 5.6 0 5.6

VBG/mixedDeitel et al,28

19887 Selected patients

(9 pregnancies)Selected sample of

86 preoperativepatients (274pregnancies)

0 7b 0 12.8g 0 26.7g 0 11.2 ofpreg-nanciesc

BPDFriedman

et al,29

1995

152 Consecutivepregnancies

77 Preoperative historicalpregnancies

NR 3.9 NR 9.1 0.7 2.6 44 31.2b

Kral et al,30

200679 Children from

primigravidpostoperativepregnancies

34 Children fromprimigravidpreoperativepregnancies

NR NR NR NR NR NR 19 34

(continued)

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(eg, nonobese women, obese women,presurgery pregnancies, or the generalpopulation). Rates ranged from 0% to65.8% for postsurgery pregnancies andfrom 5.6% to 64.5% for pregnancies incomparison groups (Table 1). Somestudies reported lower rates of cesar-ean delivery after surgery, whereas otherstudies reported higher rates or nodifference.

The 3 cohort studies did not reportconsistent findings. Ducarme et al18 re-ported an overall cesarean delivery rateafter LAGB procedures that was half thatof obese nonsurgical comparisons anda 0% cesarean delivery rate before startof labor. The 2 gastric bypass cohortstudies found high rates of cesarean de-livery in the surgery groups (�60%)that did not differ from obese compari-son groups, but exceeded those rates ofthe nonobese groups. Cesarean deliv-ery rates varied in the other cohort stud-ies (Table 1). Based on these data, bar-iatric surgery does not appear to havea strong relationship with cesarean de-livery rates.

Only 2 studies specifically reportedon rates of delivery complications, suchas blood loss or operative injury. These

studies18,19 found no differences in de-livery complications between surgerypatients and comparison groups.

Neonatal Outcomes

Fourteen studies compared neonataloutcomes following bariatric surgerywith a comparison group. The 4 mostcommonly noted outcomes were pre-mature delivery (�37 weeks’ gesta-tion), low birth weight (�2.5 kg), mac-rosomia (�4.0 or �4.5 kg), andperinatal mortality (TABLE 2).*

Laparoscopic Adjustable GastricBanding. Ducarme et al18 found no dif-ference in preterm birth rates or meanbirth weight after LAGB vs obese com-parisongroup.However,ratesoflowbirthweight(7.7%vs10.6%,P�.05)andmac-rosomia (7.7% vs 14.6%, P� .05) werelower among patients who had surgery.

Another study21 found that macroso-miarateswereloweramongpatientswhohadbariatricsurgerythanamongcontrolpatientswhowereobese(11.4%vs17.7%)and approached rates in the community(11.8%).Sixcaseseries34-39 onLAGBpro-cedures (n=162) found lowratesofneo-

natalcomplications,consistentwithfind-ings in the matched cohort study.

Gastric Bypass. In 2 matched co-hort studies,19,20 patients who under-went gastric bypass showed no differ-ences in premature delivery or low birthweight compared with patients who werenot obese. In both studies, there were nocases of macrosomia in the patients whohad surgery, whereas rates were 2.6% and4.3% in the nonobese comparisons(P =not reported [1 study] and P =.28 [1study]). Other cohort studies24,25 of gas-tric bypass found lower mean birthweightand lowermacrosomia rates in thepregnancies after surgery compared withrates in the obese comparison groups.

Relatively low neonatal complicationrates were also reported in 8 case seriesof pregnancy following gastric bypass(approximately 300 pregnancies).40,42-48

However, 2 studies43,44 reported higherthan expected rates of neural tube de-fects (1 study44 described 4 pregnanciesand the other study43 3 pregnancies, ofa total 110 pregnancies, resulting in in-fants with neural tube defects). Moth-ersinthesecaseswerereportedtobenon-adherent with recommended vitaminsupplementation.*References 18-21, 23-26, 28, 29, 31-33, 41.

Table 1. Observational Studies on Maternal Pregnancy Outcomes Following Bariatric Surgery (continued)

Source andSurgery Type

Inclusion Criteria

% of Patients

BariatricSurgery

Comparison(Control)

GestationalDiabetes Preeclampsiaa

Pregnancy-Induced

Hypertension Cesarean Delivery

BariatricSurgery Control

BariatricSurgery Control

BariatricSurgery Control

BariatricSurgery Control

Bariatric mixSheiner et al,31

2004298 Consecutive

deliveries(1988-2002)

158 912 Consecutivepopulation deliveries(1988-2002)

9.4 5.0g 5.7 4.7 5.4f 1.7f 25.2 12.2g

BariatricWeintraub

et al,32

2007h

507 Deliveries(1988-2006)

301 Preoperativedeliveries(1988-2006)

11.0 17.3f 1.0 4.0g 11.2 23.6f,g NR NR

Heinzen et al,33

2006h22 Consecutive

deliveries(1999-2006)

700 Computer-generated randomcontrol delivieries

No differencenoted (datanot given)

No differencenoted (datanot given)

NR NR No differencenoted (datanot given)

Abbreviations: BMI, body mass index, calculated as weight in kilograms divided by height in meters squared; BPD, biliopancreatic diversion/duodenal switch; LAGB, laparoscopic ad-justable gastric banding; NR, not reported; VBG, vertical-banded gastroplasty.

a Included eclampsia, if it was also reported.bP � .05.cP � .01.dDixon et al22 reported on 22 pregnancies that may be included in the other Dixon et al21 article, which compared postoperative pregnancies with all pregnancies in the state of Victoria

(61 000) and only had information on pregnancy-induced hypertension and gestational diabetes (not included in Table).eP = .06.f Included chronic hypertension.gP � .001.hAbstract available only.iP = .07.

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Table 2. Observational Studies on Neonatal Outcomes Following Bariatric Surgerya

Source andSurgery Type

Inclusion Criteria

% of Patients

Premature Delivery(�37 wk)

Low Birth Weight(�2.5 kg)

Macrosomia(�4.0 or �4.5 kg) Perinatal Mortality

BariatricSurgery

Comparison(Control)

BariatricSurgery Control

BariatricSurgery Control

BariatricSurgery Control

BariatricSurgery Control

LAGBDucarme

et al,18

2007

13 Consecutivepregnancies(delivered2004-2006)

414 Obese (BMI �30)consecutive controls(delivered2004-2006)

7.7 7.1 7.7 10.6b 7.7 14.6b NR NR

Dixon et al,21

2005c79 Consecutive first

postoperativepregnancies(1995-2003)

40 Consecutivepenultimatepreoperativepregnancies

79 From obese womenmatched for parity,age, and BMI

61 000 Communitycontrols

6.3 NR

12.7d,e

7.8

6.3 NR

8.9

6.9

11.4 NR

17.7d

11.8

1.3 0

Gastric bypassWax et al,19

200838 Consecutive

patients76 Controls (next 2

deliveries after indexcase), matched forage and priorcesarean

26.3 22.4 7.7 9.0 0 2.6 NR NR

Patel et al,20

200826 Consecutive

pregnancies(delivered2003-2006)

254 Controls(5 deliveries beforeand after index case2003-2006)188 nonobese39 obese27 severely obese

26.9 20.2

17.925.9

NR NR 0

4.37.7

18.5b

NR NR

Richardset al,24

1987f

57 Pregnanciesfrom 243of 580 surveys(1979-1983)

57 Preoperativepregnancies fromsame 243 surveys,matched on weight,parity, and year

12.3 7.0 NR NR 15.8 36.8b 3.5 3.5

Wittgroveet al,25

1998

17 Selected patientsidentified throughbariatric newsletter

Preoperative historicalpregnancies fromthe same 17patients

NR NR NR NR 5.6 30.4b 0 0

BPDMarceau

et al,41

2004

162 Full-termpregnancies from783 questionnaires

1236 Full-termpreoperativepregnancies

13.6 16.7 27.4 NR 7.7 34.8g 0.6 1.0

Friedmanet al,29

1995

152 Consecutivepregnancies

77 Preoperativehistoricalpregnancies

15.3 NR NR NR NR NR 2.6 2.6

Bariatric mixSheiner

et al,31

2004

298 Consecutivedeliveries(1988-2002)

158 912 Consecutivepopulation deliveries(1988-2002)

NR NR NR NR 9.4 4.6g 0.3 1.5

VBG/mixDeitel et al,28

19887 Selected patients Selected sample of 86

preoperative patientsNR NR NR NR NR NR 0 0

BariatricWeintraub

et al,32

2007

507 Deliveries(1988-2006)

301 Preoperativedeliveries(1988-2006)

NR NR NR NR 3.2 7.6h NR NR

Abbreviations: BMI, body mass index, calculated as weight in kilograms divided by height in meters squared; BPD, biliopancreatic diversion/duodenal switch; LAGB, laparoscopicadjustable gastric banding; NR, not reported; VBG, vertical-banded gastroplasty.

aThree additional studies reported only mean birth weight; therefore, data were not included in the table (Skull et al,23 Heinzen et al,33 Landsberger et al26), with the latter 2 reportedonly in abstract form. Landsberger et al26 reported no difference in preterm delivery or perinatal complications.

bP � .05.cAn additional study by Dixon et al22 was not included, which reported on 22 pregnancies; no comparison group data were provided in that article.dCompared with obese-matched patients rather than historical pregnancies.eP = .08.fLarge for gestational age.gP � .001.hP � .005.

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Biliopancreatic Diversion. Neona-tal outcomes following BPD wereassessed in 2 cohort studies (with�150 pregnancies)29,41 (Table 2) and4 case series.49-52 One cohort study41

found no difference in preterm birthrates, but lower mean birth weight

and macrosomia rates in the surgerygroup were found compared withcontrols who were obese (3 kg vs 3.5kg, P � .001; and 7.7% vs 34.8%,P � .001, respectively). The otherstudy29 found that after BPD, 22 of thesingleton pregnancies (15.3%) were

preterm deliveries compared with USestimates of 12.8% in 2005.53

A number of studies reported mis-carriage and perinatal mortality ratesfollowing BPD.29,41,49-52 In 1 cohort study(n=152), miscarriage rates were ap-proximately 20% before and after sur-gery and perinatal mortality was 2.6%for both groups.29 In another cohortstudy (n=251),41 miscarriage rates were21.6% before bariatric surgery vs 26.0%after bariatric surgery. The 4 case se-ries49-52 included 108 pregnancies fol-lowing BPD.

Mixed Procedures. A study31 thatcompared pregnancy outcomes be-tween 298 patients who underwent avariety of bariatric procedures and anonobese comparison group foundhigher labor induction rates (23.8% vs10.9%, P� .001), mean birth weights(P=.02), and macrosomia (P� .001),and no difference in perinatal mortal-ity among women with history of bar-iatric procedures.

Overall, following LAGB and gas-tric bypass procedures, there is nostrong evidence that adverse neonataloutcome rates are higher compared withobese groups. Following BPD, adverseneonatal outcomes may be lower; how-ever, miscarriage rates may be higher.

Nutritional Deficiencies

Dietary guidelines recommend supple-mentation with multivitamins and ironfollowing bariatric surgery.54,55 Obser-vational studies evaluating pregnancyafter LAGB or gastric bypass haveshown minimal evidence of nutri-tional adverse events; however, mostmonitored supplement adherence. Of22 studies that addressed the issues ofnutritional deficiencies, 13 were com-parison studies or case series (TABLE 3)and 9 were case reports.

Laparoscopic Adjustable GastricBanding. One study21 of women who be-came pregnant after LAGB reported nonutritional problems; 84% of the 79 preg-nant women reported adherence withsupplementation. However, among 4studies,23,35,37,38 approximately 19% ofpregnant women had their adjustableLAGB deflated or removed for various

Table 3. Observational Studies of Nutritional Outcomes in Pregnancy Following BariatricSurgery

Source andSurgery Type

No. ofPregnanciesAfter Surgery Selection Criteria Findings

LAGBDixon et al,21

200579 Selected sample

(consecutivepregnancies)

No adverse nutritional events; 84%adherent with vitaminsupplementation

Gastric bypassPatel et al,20

200826 Selected sample

(consecutivepregnancies)

11.5% Had anemia treated withparenteral iron, anemia was foundto be 1.1% in nonobese controls(P = .001); adherence with vitaminsupplementation unknown

Wittgrove etal,25 1998

36 Volunteers frommediaadvertisement

No clinically significant anemia;adherence with vitaminsupplementation unknown

Martin et al,43

1988110 Survey and review of

records to identifyinfants with neuraltube defects

3 Women had infants with neural tubedefects; all were nonadherent withvitamin supplementation

Haddowet al,44

1986

3 Not reported 3 Women had infants with neural tubedefects; all were nonadherent withvitamin supplementation

Printen andScott,45

1982

54 Not reported 4.4% Required parenteral iron;adherence with vitaminsupplementation unknown

Dao et al,47

200634 Selected sample 1 Woman had mild anemia that

resolved with supplementation;adherence with vitaminsupplementation unknown

BPDFriedman

et al,29

1995

152 Consecutive patients 21% Required parenteral nutrition; allother patients received “usualsupplementation”

Marceauet al,41

2004

166 Survey of patientsand review ofprenatal records

4 Women required parenteral nutrition;unknown adherence with vitaminsupplementation

Cools et al,49

20069 Not reported 4 Women had iron deficiency requiring

transfusion or supplements; 1 alsorequired parenteral nutrition; 3were adherent with vitaminsupplementation and 5 were not;unknown whether 1 was adherent

Gerrits et al,50

20034 Study of

contraceptionfollowing BPD;reviewed 4unplannedpregnancies

1 Woman had anemia despite ironsupplementation; 1 hadunspecified vitamin deficiency whilenot taking any supplementation;remaining 2 were adherent withvitamin supplementation

Adami et al,51

199264 Not reported 20% Required parenteral nutrition;

adherence with vitaminsupplementation unknown

Friedmanet al,52

1989

48 Not reported 15% Required inpatient parenteralnutrition and 17% requiredoutpatient parenteral nutrition; allother patients received “usualsupplementation”

Abbreviations: BPD, biliopancreatic diversion/duodenal switch; LAGB, laparoscopic adjustable gastric banding.

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reasons, including nausea and vomit-ing and patient preference.

Gastric Bypass. Gastric bypass wasassociated with few nutritional ad-verse outcomes during pregnancy(Table 3). Four studies20,25,45,47 re-ported low rates of anemia, rangingfrom 0% to 11%. Two other studies43,44

reported neural tube defects in preg-nancies (6 neonates) following gastricbypass; however, none of the motherswere adherent with supplements. Fourcase reports56-59 following gastric by-pass reported nutritional deficiencies (2had adherence and 2 did not have ad-herence with supplementation).

Biliopancreatic Diversion. Obser-vational studies29,41,51,52 show that par-enteral nutrition is used in approxi-mately 20% of pregnancies followingBPD. Several small case series of preg-nancies following BPD reported nutri-tional deficiencies among women tak-ing nutritional supplements, those nottaking supplements, and some in whomadherence was unclear.49,50,60-62

There are few studies of adverse nu-tritional outcomes in pregnancies fol-lowing LAGB or gastric bypass surger-ies when nutritional supplementationwas maintained. Severe nutritional de-ficiencies requiring parenteral nutri-tion have been reported in pregnan-cies following BPD. Many, but not all,of the studies attributed the defi-ciency to nonadherence. Of concernwere several studies of neural tube de-fects, particularly in neonates of womenwho had undergone gastric bypass andbeen nonadherent. However, these stud-ies were not designed to specifically as-sess nutritional outcomes.

Bariatric Surgery and Fertility. Weidentified 6 studies27,28,31,41,63,64 that ad-dressed fertility outcomes in patients af-ter bariatric surgery and most of thesecompared pregnancy rates before andafter surgery (TABLE 4). Three smallstudies27,28,41 reported improvements infertility and 1 study63 noted no change.

One study (n=298) found that afterbariatric surgery, the need for fertilitytreatment in women was low (6.7%) butexceeded that of the community (2.3%,P� .001).31 Similar results were found

for patients after surgery with gesta-tional diabetes compared with a non-surgery control population with gesta-tional diabetes.64 Five additional caseseries (n=21 to 48)22,25,35,37,52 found thatinfertility rates before surgery rangedfrom 15% to 44%.

Six studies28,50,63,65-67 found evidenceof normalization of hormones and men-strual cycles and lessening of polycys-tic ovarian syndrome following bariat-ric surgery. One study65 prospectivelyfollowed up 17 women who had BPDor gastic bypass surgery and founddecreases in hirsutism, testosterone,androstenedione, and dehydroepi-androsterone sulfate and also found nor-malization of menstrual cycles, ovula-tion,orboth inallwomen.Aprospectivecase series50 of women before and afterBPD surgery demonstrated normaliza-

tion of hormones. The postsurgery nor-malization of menstrual cycles wasobserved in a cohort study of 109women (P� .001).28 A retrospective sur-vey63 reported that menstrual cycles nor-malized in71.4%(95%confidence inter-val, 62.3%-80.5%) of 98 previouslyanovulatory women and that resump-tion of ovulation was associated withgreater weight loss following surgery.Another study66 showed resolution ofpolycystic ovarian syndrome follow-ing gastric bypass surgery: all 24 womenresumed normal menstrual cycles, 5conceived without clomiphene, and hir-sutism resolved in more than 50%. Astudy67 following VBG surgery (n=38)found improvements in hormone lev-els and normalization of menstrualcycles among all 5 women with abnor-mal cycles.

Table 4. Observational Studies Reporting Fertility Outcomes for Patients Following BariatricSurgery

Source andSurgery Type

Inclusion Criteria

FindingsBariatric Surgery Comparison

Bariatric mixSheiner et al,31

2004298 Consecutive

postoperativedeliveries(1988-2002)

158 912Consecutivegeneralpopulationdeliveries(1988-2002)

6.7% Required fertility treatment aftersurgery vs 2.3% of population(P � .001)

Sheiner et al,64

2006b28 Postoperative

deliveries inwomen withgestationaldiabetes

7986 Deliveries inwomen withgestationaldiabetes

21.4% after surgery with gestationaldiabetes required fertility treatmentvs 5.5% of patients frompopulation with gestationaldiabetes (P � .001

Gastric bypass/mixedTeitelman

et al,63

2006

Postoperative data on195 questionnaires(51% response)

Preoperative dataon 195questionnaireresponders

17.5% With menstrual irregularities aftersurgery vs 49.5% before (P � .001);no significant difference in fertilitymedication usea

VBGBilenka et al,27

199514 Postoperative

deliveries18 Preoperative

deliveries11.1% Received fertility treatment after

surgery vs 83% (5/6) before(P � .001)a

VBG/mixDeitel et al,28

1988Selected sample of 7

women withpostoperativedeliveries

Selected sample of86 women withpreoperativedeliveries

88.9% Able to get pregnant aftersurgery vs 25.2% before(P � .001)a

BPDMarceau

et al,41

2004

162 Postoperativepregnancies from783 patientquestionnaires(85% response)

1236 Full-termpreoperativepregnancies

46.9% (15/32) who were unable to getpregnant before surgery were ableto get pregnant after surgerya

Abbreviations: BPD, biliopancreatic diversion/duodenal switch; LAGB, laparoscopic adjustable gastric banding; VBG, vertical-banded gastroplasty.

aMay have selection bias because it is unknown how many patients overall desired and attempted pregnancy after sur-gery.

bSubset of Sheiner et al.31

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Most observations on fertility fol-lowing bariatric surgery lack com-plete data on the total number ofwomen attempting to get pregnant andpregnancy rates. Most studies presentconvenience samples of women whowere able to get pregnant, in whom pre-surgery fertility histories were avail-able. With these significant limita-tions in mind, data suggest that surgerymay have a beneficial influence on fer-tility, which is supported by the nor-malization of hormones in polycysticovarian syndrome and correction of ab-normal menstrual cycles.

Contraceptive Use. No random-ized trials have assessed the efficacy ofcontraception after bariatric surgery.Theoretical concerns exist about ab-sorption of oral contraceptive pills inpatients following a malabsorptive pro-cedure, such as BPD. One case series50

identified 2 failures for oral contracep-tive pills out of 40 women after BPD sur-gery. No firm conclusions can be drawnabout the effectiveness of contracep-tive methods following bariatric sur-gery.

Evidence on Time to Delay ofPregnancy After Bariatric Surgery

We identified 5 studies comparing preg-nancy outcomes within the first year upto 18 months following surgery withlater pregnancies. One study42 in-cluded 18 women with 21 successfulpregnancies after gastric bypass sur-gery. Of these women, 10 conceivedwithin 1 year after surgery. No differ-ences were found in rates of cesareandelivery, delivery complications, lowbirth weight, or congenital abnormali-ties. Another study47 found no differ-ences in outcomes between pregnan-cies within the first year followinggastric bypass surgery vs pregnanciesoccurring more than 1 year after sur-gery. In a study comparing 20 preg-nancies in which conception occurredwithin the first year after LAGB,21 ma-ternal weight gain was lower in theseearly postsurgery pregnancies, birthweight was unchanged, and there wereno differences in pregnancy complica-tions or preterm deliveries. Another

study68 found a higher spontaneousabortion rate among pregnancies oc-curring within 18 months of havingBPD surgery compared with those preg-nancies occurring after 18 months ofhaving BPD surgery (31% vs 18%). Ina matched cohort study, Patel et al20

stratified the postoperative cohort of 26patients by time to conception from sur-gery and found that 4 women (15.4%)were pregnant within the first year, 12(46.1%) were pregnant between 13 and24 months, and 10 (38.5%) becamepregnant after more than 2 years. Earlypregnancies were associated with morepreterm deliveries (50% for �12months, 25% for 13-24 months, and20% for �24 months). A study that in-vestigated pregnancies within 2 yearsafter gastric bypass surgery found a highrate of premature births (18%), but thisstudy included no comparison group.45

A study of pregnancies within 2 yearsof LAGB surgery found spontaneousabortion rates to be 29%.36

In conclusion, few data are avail-able to support recommendations re-garding the ideal timing for pregnan-cies following surgery. However, thereare reports of successful pregnancieswithin 1 or 2 years of surgery.

Surgical Complicationsin Pregnancies FollowingBariatric Surgery

We identified 20 reports of complica-tions requiring surgical interventionduring pregnancy following bariatricsurgery. Maternal complications in-cluded 14 bowel obstructions (11 in-ternal hernias), 1 gastric ulcer, 4 bandevents, and 1 staple-l ine stric-ture.20,23,69-83 Gestational age at ad-verse event ranged from 13 to 37 weeks(median, 26 weeks). Most women pre-sented with nonspecific abdominalcomplaints and delays often occurredbefore therapeutic intervention. In 7 of20 cases (35%), an emergent cesareandelivery or premature rupture of mem-branes occurred. Five neonates died(25%) and 10 were delivered full-term(50%). There were 3 maternal deaths(15%). The case reports indicate the po-tential for complications in pregnan-

cies following bariatric surgery, includ-ing maternal and fetal death.

COMMENTMore than 150 000 women of repro-ductive age underwent bariatric pro-cedures in the most recent 3 years forwhich inpatient data are available. Thisfigure is likely an underestimate be-cause many patients undergo outpa-tient bariatric surgical procedures (eg,LAGB surgery) that would not havebeen reported in the Nationwide Inpa-tient Sample. A growing number ofwomen of child-bearing age have un-dergone these procedures and need in-formation and guidance about fertil-ity, pregnancy, and contraception.

The available evidence suggests thatrisks for maternal complications, suchas gestational diabetes and preeclamp-sia, may be lower following surgically in-duced weight loss than the risks in obesewomen and may approach communityrates. Similarly, neonatal complica-tions, such as premature delivery andlow birth weight, may be lower in preg-nancies following bariatric surgery. Re-sults from large cohorts of consecutivepatients with pregnancies are needed toconfirm these findings. The effect of bar-iatric surgery on need for cesarean de-livery is unclear as reported rates be-fore and after surgery vary widelybetween studies. Nutritional problemsduring pregnancy following LAGB orgastric bypass surgeries appear uncom-mon and many are attributed to supple-ment nonadherence. Studies of consecu-tive patients that systematically monitoradherence and nutritional status areneeded. The relationship of bariatric sur-gery to fertility has not been well stud-ied. Reports of normalization of sex hor-mones, menstrual irregularities, andimprovement in polycystic ovarian syn-drome following surgery suggest that fer-tility may improve, which would be con-sistent with that observed in obesewomen after nonsurgically inducedweight loss. However, most of thesestudies may have selection bias, limit-ing their ability to reach valid conclu-sions. Although rare, complications ofbariatric surgery can manifest during

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pregnancy. The most commonly re-ported complication is internal herniacausing bowel compromise. There is nostrong evidence to guide how long to de-lay pregnancy following bariatric sur-gery. The typical recommended periodis 1 year, coinciding with the end of theperiod of most rapid weight loss. Thereis no convincing evidence to support orrefute concerns about the use of oralcontraceptive pills following bariatricsurgery.

Our review is limited by the qualityof the original studies. Three matchedcohort studies assessed consecutive pa-tients and compared these with con-current control groups and provided themain evidence in support of our con-clusions. However, sample sizes weremodest (77 surgical cases and 744 com-parison controls) and there may havebeen differences in women electing toundergo surgery compared with womenwho did not have surgery. Because ran-domized controlled trials will not be fea-sible for assessing pregnancy out-comes, these types of studies representthe best available evidence for assess-ing the effect of surgically inducedweight loss on future pregnancies. How-ever, inherent limitations in the iden-tified studies preclude us from draw-ing strong conclusions. Some of theseclinical questions addressed in our re-view, such as optimal contraception,will be best answered by randomizedclinical trials or prospective cohort stud-ies. Because clinicians must still makedecisions regarding these patients, weassessed the best evidence available inan attempt to help guide clinicians.

Research is needed to better delin-eate the extent to which surgery andsubsequent weight loss improve fertil-ity and pregnancy outcomes. Optimiz-ing success for contraception and pro-ducing healthy neonates followingsurgery will require a multidisci-plinary effort by surgeons, primary carephysicians, reproductive fertility spe-cialists, obstetricians, and patients.

Author Contributions: Dr Maggard had full access to allof the data in the study and takes responsibility for theintegrityof thedataandtheaccuracyof thedataanalysis.Study concept and design: Maggard, Li, Maglione,Hilton, Santry, Livingston, Shekelle.

Acquisition of data: Maggard, Yermilov, Li, Suttorp,Santry, Livingston, Shekelle.Analysis and interpretation of data: Maggard,Yermilov, Li, Maglione, Newberry, Suttorp, Hilton,Santry, Morton, Livingston, Shekelle.Drafting of the manuscript: Maggard, Yermilov, Li,Hilton, Santry, Shekelle.Critical revision of the manuscript for important in-tellectual content: Maggard, Yermilov, Li, Maglione,Newberry, Suttorp, Santry, Morton, Livingston,Shekelle.Statistical analysis: Maggard, Yermilov, Li, Suttorp,Hilton.Obtained funding: Maglione, Shekelle.Administrative, technical, or material support:Yermilov, Maglione, Newberry, Hilton.Study supervision: Maggard, Maglione, Shekelle.Financial Disclosures: None reported.Funding/Support: This project was funded under con-tract 290-02-0003 from the Agency for HealthcareResearch and Quality, US Department of Health andHuman Services to the Southern California EvidenceBased Practice Center. Dr Maggard’s time was sup-ported in part by a grant from the Robert WoodJohnson Physician Faculty Scholars program. This workwas requested by the American College of Obstetri-cians and Gynecologists.Role of the Sponsor: The Agency for Healthcare Re-search and Quality had input into the general designand conduct of evidence reviews conducted by theEvidence Based Practice Centers, but not this evi-dence review in specific. The sponsors were not in-volved in the collection, management, or analyses ofthe data, but did review and provide comments onthe evidence report upon which this article is based.Disclaimer: The authors of this article are responsiblefor its content. Statements in the article should not beconstrued as endorsement by the Agency for Health-care Research and Quality or the US Department ofHealth and Human Services. All data used for this studyare accessible for review.Also Available: A more detailed clinical review of preg-nancy and fertility following bariatric surgery will beavailable at http://www.ahrq.gov/downloads/pub/evidence/pdf/bariatricrep/barirep.pdf.

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2296 JAMA, November 19, 2008—Vol 300, No. 19 (Reprinted) ©2008 American Medical Association. All rights reserved.

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