hb maternal and pregnancy outcame

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Mean Maternal Second-Tr imesterHemoglobin Concentra t ion andOutcome of Pregnancy:A Pop ulat ion-B ased StudyGeorg-Friedrich von Tempelhoff, MD, FCATH, Lothar Heilmann, MD,Lothar Rudig, MD, Kunhard Pollow, PhD, MD, Gerhard Hommcl, PhD,and Jurgen Koscielny, M D

Cliniciii and .ApplieViilumc 14 NumlitT .l i inuan 2008 \'-)-2H

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Summary: Both anemia and the lack of physiologicalmaternal plasma volume expansion during the secondtrimester are associated with higher maternal morhidityand poor tetal outcome. Mean hemoglobin levelshetween the 14th and 30th gestational weeks were cal-culated in 4985 consecutive pregnant women and werecorrelated with outcome data of pregnancy. It was foundthat 9.4% of participants (n = 3959) had normal pregnancyoutcome. Mean maternal hemoglobin levels were signif-icantly lower in women with a normal pregnaney (11.96 0.94 g/dL) compared with women who had adverseoutcome events (preeelampsia, n - 4 2 3 , 12.5 1.0 g/dL,P < ,0001: early birth, n = 464, 12.2 1.01 g/dL, P < .0001;low birth weight newborn, n 473, 12.2 l.IO g/dL,

P < .0001; intrauterine growth retardation, n= 250, 12.2 1.0 g/dL, P < .0001). The risk for any adverse ou tcomevent was lowest with a mean hemoglohin hetween 11.0and 12.0 g/dL (odds ratio, 0.625; 95% confidence interval, 0.43-0.89) and highest hetween 13.0 and 15.0 g/dL(odds ratio, 2.24 ; 95% confidence inter\'al. 1.54-3.31). Inthis population-hased study from a community inWestern Germany, impaired plasma volume expansionwas an indepen dent risk factor for the developm ent of anadverse outcome of pregnancy.Keyw ords: plasma volume; hemoglobin, preeclampsialow birth weight; preterm delivery; intrauterine growthretardation; hemodilution

Over the past years, only anemia has heenrecognized as a risk factor for poor fetal out-come, whereas high hemoglohin concentra-tions have heen considered optimal for pregnancydevelopment. Meanwhile, it is well estahlished thathetween the second trimester and the middle of thethird trimester of pregnancy, plasma volume expandshy 25% to 80% of prepregnancy volumes.' Theincrease in red cell mass is restricted to about 30%,Address corresp ond ence to Georg-Friedrich von Tempelhoff, M D,Department of Obste tr ics and Gynecology, GP-Ruesselsheim,Augiist-Hebel Strasse 59. 65428 Ruesselsheim. Germany;e-mail: [email protected] of Obstetrics and Gynecology; Health and CareCenter Ruesselsheim. Ruesselsheim, Germany (GFVT. LH,LR); Institute for Fxpcrimcntal Endocrinolog); University ofMainz, Mainz. Germany (KP); Institute for Medical Biometrics,Epidemiology and Informatic; University of Mainz, Mainz,Germ any (GH); Institute for Transfusion Me dicine. Charit eHumboldt-University, Berlin. Germany (JK).

which results in a decrease of hematocrit of ahout 3%to 5% hetween gestational weeks 20 and 30^ withousuhstantial accompanying changes in mean corpuscular volume and hemoglohin content of the redblood cells.-^In large European studies, the majority of pregnant women with normal maternal and fetal outcomes had a range of hemoglobin concentrationduring the first and second trimester distinctly lowethan that of nonpregnant women. A prospective triafrom the northwest Thames region of London foundthe lowest perinatal mortality among 222 614women with their first singleton pregnancies, whohad the lowest recorded maternal hemoglobin concentration at the first antenatal checkbetween 9.0and lLOg/dL.-*In another large British population-hased studythat included 153 602 pregnant w omen, babies born


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20 Clinical m id Applied Thrombosis/Hemostasis / Vol. 14, No. 1, Janua ry 200 8

and 9.5 g/dL at approximately week 28' ' had thehighest mean birth weight. These results are of greatinterest hecause such values are considered torepresent anemia according to the World HealthOrganization.*"Such failure of plasma expansion between 20and 25 weeks may result in or favor the developmentof adverse outcome events during pregnancy.Inappropriate plasma volume expansion has heenassociated with the development of growth-retardedinfants, '" delivery of low hirth weight newhorns,^'^and placenta! infarction that may he caused byreduced uteroplacental perfusion at tr ibutable toincreased biood viscosity.'^ Finally, failure of plasmavolume expansion during the second trimester hasbeen held responsible for intrauterine fetal demise

in women with chronic hypertension. '"*In this population-based study from the middleregion of western Germany, we retrospectively ana-lyzed prenatal maternal records and evaluated anassociat ion between mean maternal hemoglobinconcentrat ions during the second trimester and theoutcome of pregnancy.

Patients And MethodsPregnant WomenFrom January 1990 to the end of December 1996,498 S consecutive women with singleton pregnancywbo delivered in our department were eligible to beincluded in this retrospective investigation. Toassess the maternal data, we photocopied the mater-nity records (Mutterpass). These records includeinformation on previous pregnancies and deliveriesand the current pregnancy (eg, results of routine phys-ical examination and ultrasound fetometry documentedby the external obstetrician), in addition to systolic

and diastolic blood pressures, hemoglobin concen-trat ions, and urine and immunologic/hematologicresults. Moreover, the personal, medical, and socialhistories with particular emphasis on risk factors ofpregnancy and delivery such as obesity, smoking,comorbidity, and drug use are documented. Todetermine mean hemoglobin concentrat ions dur ingthe second trimester, values between the 14' ' ' and30'^ weeks of gestation were adopted and calculatedfrom the maternity records. The following maternaland tetal data were assessed: geographic origin, birthweight, week of gestation at the time of delivery,small-for-date newb orns (in the absence of congenital

malformations or chromosomal abnormali t ies), tpre se nc e and tyjie of preeclampsia (hemolysis, elevatliver enzymes, low platelet syndrome), abruptio plcentae, fetal death and perinatal mortality, venopH in the umbilical cord, and 1-minute, 5-miniand 10-minute Apgar scores.To stratify normal and abnormal, we defined thterms similarly for all subjects:

Low birtb weight:


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M a te r n a l S e c o n d - T r ime s t e r H e mo g lo b in - Co n c e n t r a t i o n /Von Temjielhoff ct ul 21

Table 1. Characteristics of Women With Normal Pregnancy Outcome and Patients With Preeclampsia, Eariy Birth(Before Week 37), Low Birth Weight (


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22 Clinical and Applied Titrombosis/Hemostasis / \/o\. 14, No. 1, Januiiry 2008

Table 2. Ou tcom e Data of Wom en Witb Normal Pregnancy and Patients With Preeclam psia, Early Birth(Before wk 37), Low Birth Weigbt (


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Maternal Second-Trimester Hemoglobin-Concentration / Von Tenifelhojf et al 23

13,5 hemotobln [g/dL] ROC-curve "Preeclampsia

p < 0.0001 vs normal pregnancy25- 75 % Inter quartlle


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24 Clinical and Applied Thrombosis/Hemostasis / \o\. 14, No. 1, January 2008

Hemoglobin II trim.

Weight before pregn.Proteinuria II tr im.

RRsys>140 l l t r lm .

RR dias > 90 II tr im.Smoking

Number of cigVcJayBMI (Kg/m2}

iower risk

Chi - Squfire

higher risk

BHemoglobin il trim.

Weight before pregn.Proteinuria il trim.

RR sy s> 140 il trim.RR dias > 90 il trim.

SmokingNumber of cig./day

AgeBMi {Kg/m2)

lower riskChi - Square *: p


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Maternal Second-Trimester Hemoglobin-Concentration / Von Tem pelhoff et al 25

eHemoglobin II trim.

Weight before pregn.Proteinuria II trim.

RR sys > 140 II t r im.RRdias>90 II t r im.

SmokingNumber of cig./day

AgeBMI (Kg/m2)

Hemoglobin II trim.Weight before pregn.

Proteinuria II t r im.RR sys > 140 H t r im.RR dias > 90 II t r im.

Smoking

Number of cig./dayAge

BMI (Kg/m2)

lower risk

Chi Square : p


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26 Clinical and Applied Thrombosis/Hemostasis / Vol. 14, No. 1, January 200 8

9 5% C l, 0.951 -0.9 84; P < .0001), maternal age (OR,1.044; 95% Cl , 1 .005-1 .024; P = .005). and smok-ing (OR, 1.748; 95% C l, 1.177-2.597; P = .006)were statistically significant independent prognosticma rkers for the delivery of low birth weight child ren.Th e risk for delivery of a growth-retarde d new bornwas significantly associated with increasing meanmaternal hemoglohin concentration and pathologicalBP during the second trimester, smoking, the numherof cigarettes per day, and a lower weight hefore preg-nancy (Fig. 4C). Mean maternal second trimesterhemoglobin (OR, 1.352; 95 % Cl, 1.175-1.556; P


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Maternal Second-Trimester Hemoglobin-Concentration / Von Tempelhoffet al

trial. Alth oug h co rrec tion of iron deficiency in preg-nancy^which is a com m on cau se oF ane m ia indeveloping countriescan produce a s ignificantincrease in hemoglobin concentrations, it does notincrease hemoglobin higher than the optimal con-centration needed for oxygen delivery,^^ Therefore,iron supplementation is not likely a cofactor forhigher hemoglobin concentrations in patients withadverse outcome events during pregnancy.

In most developing co untries, ane mia is a leadingcause (or symptom) in women with adverse outcomeevents during pregnancy. Such low hemoglobin con-centrations in pregnant women often are tbe conse-quence of common environmental influences andconditions"^ (eg, malnutrition, comorhidity, injury,or inadequate management of bleeding complica-tions), which themselves potentially interfere withtbe normal outcome of pregnancy. Apart from verylow hemoglobin concentrations (


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28 Clinical and Applied Thrombosis/Hemostasis / Voi. 14, No. I, January 2008

by chronic hypertension and intrauterine fetal demise,Obstet Gynecol. 1982:60:174-178.15. Stephansson O, D ickman PW, Johansson A, Cnattingius S.Maternal hemoglobin-concentration during pregnancyand risk of stillbirth. JAMA. 2000;284:2611 -2617,16. Lao I'V, Tam K-F, Ch an LY. Third trimester iron status

and pregnancy outcome in non-anaemic women; preg-nancy unfavourably affected by maternal iron excess.Hum Reproditd. 2OOO;I5,1843-1848.17. Lu ZM, Goldenberg RL, Oliver SP, Cutter G, BlanksonM, The relationship between maternal hematocrit andpregnancy outcome. Obstet Gynecol 199 I ;77:190-194.18. Uosso P, Donoso E, Braun S, Espinoza R, Fcrnadez C,Salas SP. Maternal hemodynamic adjustment in idio-pathic fetal growth retardation. Gynecol Obstet Invest.I993;35:I62-165.19. Ortner A, Zech H, Humpeler E, Mairbaeurl H, Mayhigh oxygen affinity of maternal hemoglobin cause fetal

growth retardation?. Oynecology. 1983;234:79-85.20. Troeger C , Holzgreve W, Ladewig A, Zhong XY, Hah n S.Examination of maternal plasma erythropoietin andactivin A concentrations with regard to circulalorv' cry-throblast levels in normal and preeclamptic pregnan-cies. Fetal Diagn Ther. 2OO6;21:I66-16O.21. Daniel SS, Jam es LS, Stark R l, Iro pper PJ. Preventionof the normal expansion of maternal plasma volume: amodel for chronic fetal hypoxaemia. J Dev Physiol.1989;! 1:225-233.

22 , Barton D P, Joy MT, Lappin TR, et al. Matern al erythpoietin in singleton pregnancies: a randomized trial the effect of oral hematinic supplementation. AmObstet Gynecol. 1994;170:896-901.23, Bodnar LM. Scanlon KS, Freedman DS , Siega Riz ACogswell ME. High prevalence of postpartum anem

among low-income women in the United States. AmObstet Gynecol. 2001; 185:438-443,24, Rush D. Nutrition and maternal mortality in developing world. Am J Glin Nutr. 2000;72(supp212S-240S,25, Meis PJ. Miehielutte R, Peters TJ, et al. Factors assoated with prcterm birth in Cardiff, Wales. I. Univariaand muhivariable analysis. Am J Obstet Gynec1995;172:590-596.26 , Meis PJ, Miehielutte R, Peters TJ, et ak Factors assoated with preterm birth in Cardiff, Wales. 11. Indieaand spontaneous preterm hirth. Am J Obstet Gynec

1995:172:597-602.27, Ganzevoort W, Rep A, Bonsel GJ, De Vries JI, WolfPETRA investigators. A randomized trial of plasma vume expansion in hypertensive disorders of pregnaninfluence on the pulsatility indices of the fetal umbiliartery and middle cerebral artery. Am J Obstet Gynec2005; 192:233-239.28 , von Tempelhoff G-F, Heilmann L. The effect of plasvolume e.xpansion on the utero-placental perfusion. CHemorheol. 1993; 19:729-736.


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hb maternal and pregnancy outcame

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