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    • This article was downloaded by: On: 23 June 2010 Access details: Access Details: Free Access Publisher Psychology Press Informa Ltd Registered in England and Wales Registered Number: 1072954 Registered office: Mortimer House, 37- 41 Mortimer Street, London W1T 3JH, UK Journal of Clinical and Experimental Neuropsychology Publication details, including instructions for authors and subscription information: Memory Performance, but not Information Processing Speed, may be Reduced During Early Pregnancy R. H. M. de Groot; G. Hornstra; N. Roozendaal; J. Jolles To cite this Article de Groot, R. H. M. , Hornstra, G. , Roozendaal, N. and Jolles, J.(2003) 'Memory Performance, but not Information Processing Speed, may be Reduced During Early Pregnancy', Journal of Clinical and Experimental Neuropsychology, 25: 4, 482 — 488 To link to this Article: DOI: 10.1076/jcen.25.4.482.13871 URL: PLEASE SCROLL DOWN FOR ARTICLE Full terms and conditions of use: This article may be used for research, teaching and private study purposes. Any substantial or systematic reproduction, re-distribution, re-selling, loan or sub-licensing, systematic supply or distribution in any form to anyone is expressly forbidden. The publisher does not give any warranty express or implied or make any representation that the contents will be complete or accurate or up to date. The accuracy of any instructions, formulae and drug doses should be independently verified with primary sources. The publisher shall not be liable for any loss, actions, claims, proceedings, demand or costs or damages whatsoever or howsoever caused arising directly or indirectly in connection with or arising out of the use of this material.
    • Journal of Clinical and Experimental Neuropsychology 1380-3395/03/2504-482$16.00 2003, Vol. 25, No. 4, pp. 482–488 # Swets & Zeitlinger Memory Performance, but not Information Processing Speed, may be Reduced During Early Pregnancy R.H.M. de Groot1,2, G. Hornstra2, N. Roozendaal3, and J. Jolles3 1 Department of Human Biology, Maastricht University, The Netherlands, 2Nutrition and Toxicology Research Institute Maastricht (NUTRIM), Maastricht University, The Netherlands, and 3Department of Psychiatry & Neuropsychology, Division of Cognitive Disorders, Brain & Behaviour Institute, Maastricht University, The Netherlands ABSTRACT Several studies have investigated aspects of cognitive functioning during late pregnancy or in the period around delivery. The present paper describes a controlled study of neurocognitive functioning in an early phase of pregnancy (14 weeks). Seventy-one pregnant women and 57 control subjects matched for age and education were tested with a cognitive test battery. Intentional learning was tested with the Verbal Learning Test, retrieval from semantic memory with the Fluency Test, and speed of information processing with the Concept Shifting Test, the Stroop test, and the Letter Digit Substitution Test. Results show that performance Downloaded At: 14:45 23 June 2010 on tests measuring intentional learning and retrieval from semantic memory were lower in the pregnant group during early pregnancy as compared to a closely matched nonpregnant group. In contrast, speed of information processing was not different between the two groups. The differences observed in memory performance were not large and further research is needed to establish their clinical significance. In addition, the results should be interpreted with care, because our study has a cross-sectional design, which has limitations concerning the fact that preexisting performance differences might be possible. Therefore, longitudinal studies are essential to ascertain clear associations between pregnancy and cognitive performance. INTRODUCTION positive effect on some cognitive functions (Christensen, Poyser, Pollitt, & Cubis, 1999; for Forgetfulness and changed attentional functions review see Brett et al.; Brett & Baxendale, 2001). have frequently been reported by pregnant These discrepant findings may be due to differ- women (Condon, 1987). The majority of studies ences in the cognitive tasks used, or differences in have reported decreased performance on neuro- the stage of pregnancy of the subjects investi- cognitive tasks during pregnancy (e.g., Brindle, gated. Thus, there is no consistent answer to the Brown, Brown, Griffith, & Turner, 1991; question whether or not cognitive functioning is Buckwalter et al., 1999; Eidelman, Hoffmann, affected during pregnancy. & Kaitz, 1993; Parsons & Redman, 1991; Poser, Most of the above-mentioned studies investi- Kassirer, & Peyser, 1986; Sharp, Brindle, Brown, gated only one or some aspects of cognitive & Turner, 1993; Silber, Almkvist, Larsson, & functioning, and only two studies investigated Uvnas-Moberg, 1990), but some have found no whether cognitive functioning is altered in an effect of pregnancy (e.g., Morris, Toms, Easthope, early stage of pregnancy (Keenan, Yaldoo, Stress, & Biddulph, 1998; Schneider, 1989) or even a Fuerst, & Ginsburg, 1998; Sharp et al., 1993). The Address correspondence to: R.H.M. de Groot, Department of Human Biology, Maastricht University, P.O. Box 616, 6200MD Maastricht, The Netherlands. Tel.: þ 31 433881507. Fax: þ 31 433670976. E-mail: Accepted for publication: September 23, 2002.
    • MEMORY PERFORMANCE 483 possibility that early pregnancy is already char- normal health, that is, not suffering from any metabolic, acterized by cognitive changes is of importance as cardiovascular, renal, psychiatric, or neurological dis- there is not yet a profound change in psychosocial orders. Exclusion criteria were diastolic blood pressure higher than 90 mmHg, multiple pregnancy, consump- circumstances around the pregnant woman. Pos- tion of dietary supplements rich in polyunsaturated fatty sible changes in cognitive functioning could acids, and not being of Caucasian origin, in order to therefore more directly be ascribed to biological limit scatter of the measuring results due to large changes in the body brought about by hormones or differences in genetic, social, and cultural patterns. by a redistribution of nutrients essential for brain The nonpregnant women in the control group were functioning (e.g., long chain highly unsaturated friends or family members of the pregnant women, or were recruited by advertisements in local newspapers. essential fatty acids) in favor of the unborn child. All in- and exclusion criteria were the same as for the The present study investigated whether cogni- pregnant population with exception of the pregnancy- tive functioning is different during early preg- related criteria. Their last pregnancy, if any, was at least nancy (14 weeks after the last menstrual period) 32 weeks before study entry and if they had been and, if so, whether specific cognitive functions are pregnant before, they were not breastfeeding during the affected. A controlled design was chosen in which study. pregnant women were compared to carefully Seventy-one pregnant women and 57 control subjects volunteered to participate in this study. Groups matched controls, and where performance of were matched for age and education (measured on an 8- memory tasks was compared to performance on point scale, ranging from primary education to higher tests of information processing. The aspects of vocational training and university; Bie, 1987). All tests Downloaded At: 14:45 23 June 2010 cognition we measured in this study were were administered in the subject’s home, in a situation, focussed on memory and speed of information which enables testing under favorable conditions. processing. The reason for this choice was that The study was approved by the Medical Ethics pregnant women complain about concentration Committee of the University Hospital Maastricht and written consent was obtained from each participant. problems and everyday forgetting in particular (Baildam, 1991; Kane, Harman, Keeler, & Ewing, 1968; Parsons & Redman, 1991; Welch, 1991). Tests for Cognitive Functioning Sensitive tests are needed in order to detect changes in cognition during pregnancy with Visual Verbal Word Learning Task (WLT) reliability and validity, because such a study To assess learning capacity as well as recall and concerns a healthy population, where there is no retrieval from long-term memory, a visual verbal word learning task (Brand & Jolles, 1985) was completed by reason to expect profound changes in cognitive the subjects, according to the protocol of the MAAS performance. The tests we decided to use, have study (Jolles, Houx, van Boxtel, & Ponds, 1995). This already shown their effectiveness in earlier test is an improved version of a test originally devised research into neurocognitive functioning in by Rey (Rey, 1964). Fifteen words were presented one healthy subjects and in subjects with only mild after the other at 2-s intervals. After presentation, the cognitive complaints (Engelberts et al., 2002; participants were asked to recall as many words as Houx, 1991; van Boxtel et al., 1998). possible in any order. This procedure was repeated three times. After 20 min (within this time the tasks mentioned below were performed), delayed recall was measured. Dependent variables were the mean recall MATERIALS AND METHODS over three trials (WLTtot) and the delayed recall (WLTdr) after 20 min. Four different test versions were Subjects used across the population to prevent exchange of the Pregnant women were recruited by midwives in the words, used in the test between family and friends in region Maastricht, Heerlen, and Sittard, located in our test population. The test versions used in the Words the south-eastern part of the Netherlands, and by the Learning Test were parallel test versions. The words in Departments of Obstetrics and Gynecology of hospitals the lists consisted of frequently used meaningful in the same area (University Hospital Maastricht, monosyllabic nouns matched for word frequency. All Atrium Medical Center in Heerlen, and Maasland versions contained the same amount of living versus Hospital in Sittard). The selection criteria for study nonliving words, the words were emotionally neutral entry were a gestational age less than 14 weeks, and a and had on average the same amount of letters.
    • 484 R.H.M. DE GROOT ET AL. Concept Shifting Test (CST) in a random order. On the rest of the page, boxes are The Concept Shifting Test (CST) was used to measure presented with just letters. Subjects were asked to fill in visual conceptual and visuomotor tracking (Houx, as many corresponding numbers as possible within 1991; Vink & Jolles, 1985). This test consists of four 1 min. The total number of digits correctly related to a test sheets. On each test sheet, 16 small circles are letter was used as the dependent variable. grouped in a larger circle. On the first sheet, numbers appear in a fixed random order, on the second sheet Statistics letters, and on the third sheet both. Subjects were One pregnant subject did not have reliable test results, requested to cross out the items in the right order (1-2- because the conditions under which she performed the 3-4 (Subtask I), A-B-C-D (Subtask II), 1A-2B-3C cognitive tests were unacceptable. Data for this person (Subtask III), respectively); the time required to do this were excluded from the analyses. Individual data were was measured with a stopwatch. A fourth sheet with screened for extreme values based on normative data empty circles (Subtask IV), which had to be crossed out from the Maastricht Aging Study (van Boxtel et al., as fast as possible, was used to correct for motor speed. 1998); Five datapoints were considered outliers, with Mean speed for Subtasks I and II, corrected for motor values outside the range of þ /À 3*SD, and were speed (Subtask IV), was used as a measure of general excluded from the analyses. information processing speed. Subtask III, also cor- Subject characteristics were examined for statistical rected for motor speed, was used as a measure of differences between the two groups by unpaired t tests. concept shifting ability. The Mann–Whitney U-test analyzed the differences in education and number of pregnancies. The group Fluency (FLU) differences for the dependent variables were analyzed Downloaded At: 14:45 23 June 2010 The subjects completed a fluency task (Lezak, 1995) as by ANOVA with education and total number of a measure of retrieval from long-term semantic pregnancies as covariates. In the analysis of the WLT memory. Subjects had to name as many animals as a correction for test version was applied too. The CST possible within 1 min. Fluency is a measure of the was also analyzed by a two-way ANOVA for group  adequate, strategy-driven retrieval of information from repeated measures (two variables), to find out whether semantic memory. The number of animals named was there was a differential effect for concept shifting (CST used as dependent variable. III) or general speed (mean CST I/II). The same was done for the Stroop test. A p level of < .05 was con- Stroop Color-Word Interference Test sidered statistically significant. The Stroop Color-Word Interference Test was used to test selective attention (Klein, Ponds, Houx, & Jolles, 1997; Stroop, 1935). The test involves three cards RESULTS displaying 40 stimuli each: color names printed in black (Subtask I), colored patches (Subtask II), and color names printed in one of the other colors (Subtask III). Subject Characteristics For Subtask I subjects had to read aloud the printed Table 1 shows the subject characteristics. With an items, for Subtask II they had to name to color of the unpaired t test no statistically significant differ- patches and for Subtask III they had to name the ink ences were found between the two groups for age, color the words were printed in. The amount of extra height, and weight. The control subjects tended to time needed to discard irrelevant but very salient have attained a higher level of education information (reading) in favor of a less obvious aspect (p ¼ 0.0628). We therefore decided to use a sta- (color naming) was recorded. Mean speed for Subtasks I and II was used as a measure of general information tistical design in which education was controlled processing speed. Subtask III was used as a measure of for. The average total number of pregnancies was color word interference susceptibility. statistically different between the two groups (p ¼ .0014). Therefore, we corrected for both Letter-Digit-Substitution-Test (LDST) education and total number of pregnancies. The Letter-Digit-Substitution-Test (LDST) is related to the Symbol-Digit Modalities Test developed by Smith Intentional Learning Task and Retrieval (Smith, 1968), which originates from the Digit Symbol Test developed by Wechsler (Wechsler, 1958). The from Semantic Memory LDST was used to measure the efficiency of operations The control group had a significantly higher score in working memory. At the top of the test sheet, a box is on the WLTtot (mean Æ SD 11.77 Æ 1.34, n ¼ 57) presented with nine numbers coupled with nine letters than the pregnant group (11.07 Æ 1.35, n ¼ 70,
    • MEMORY PERFORMANCE 485 Table 1. Subject Characteristics (Mean Æ SD). Characteristics Pregnant group Control group (n ¼ 71) (n ¼ 57) Age (year)1 29.5 Æ 3.7 30.5 Æ 4.2 Education2 3.9 Æ 1.5 4.4 Æ 1.2 Height (cm) 168 Æ 5 168 Æ 6 Weight (kg) 70.15 Æ 14.86 70.27 Æ 13.94 Number of pregnancies* n (%) n (%) 0 0 (0) 17 (29.8) 1 25 (35.2) 11 (19.3) 2 31 (43.7) 17 (29.8) 3 9 (12.7) 8 (14.0) >3 6 (8.4) 4 (7.1) Note. 1The age range is 21–39 years. 2 Education was measured on an 8-point scale. Ã Significant. Downloaded At: 14:45 23 June 2010 Table 2. Cognitive Test Performance in the Pregnant Group Versus the Control Group (Mean Æ SD). Tests Pregnant group Control group p n ¼ 71 n ¼ 57 WLTtot (# words recalled) 11.07 Æ 1.35 11.77 Æ 1.34 .015* WLTdr (# words recalled) 11.69 Æ 2.06 12.75 Æ 1.83 .006* Fluency (# words/min) 24.80 Æ 5.46 27.84 Æ 5.79 .006* CST (I þ II)/2 (s) 12.89 Æ 3.13 12.24 Æ 3.13 .421 CST (III) (s) 20.68 Æ 6.21 18.88 Æ 5.42 .303 Stroop (I þ II)/2 (s) 17.09 Æ 2.64 16.52 Æ 2.29 .872 Stroop (III) (s) 33.10 Æ 5.44 31.67 Æ 7.05 .491 LDST (# numbers filled in/min) 40.69 Æ 6.31 42.32 Æ 6.59 .624 Note. Differences between the pregnant group and the control group were corrected for education levels and total number of pregnancies. WLT was also corrected for test version. WLT ¼ Words Learning Test, tot ¼ total (mean of trial I, II and III) dr ¼ delayed recall, CST ¼ Concept Shifting Test, LDST ¼ Letter Digit Substitution Test. *Significant. p ¼ .015). The same was found for WLT delayed Speed of Information Processing recall task: 12.75 Æ 1.83 for the control group General speed of processing and concept shifting (n ¼ 57) versus 11.69 Æ 2.06 for the pregnant in the concept shifting test were not different group (n ¼ 70, p ¼ .006) (see Table 2). between the two groups (see also Table 2). Two With respect to retrieval from long-term scores on this test were analyzed; the mean of semantic memory, the pregnant group had a Version I and II as the general speed of informa- significantly lower score for the fluency test than tion processing (p ¼ .421) and the score of Ver- did the control group (24.80 Æ 5.46, n ¼ 70 vs. sion III as a measure of concept shifting ability 27.84 Æ 5.79, n ¼ 57; p ¼ .006 after correction for ( p ¼ .303). By two-way repeated measures education and number of pregnancies). ANOVA no differential effect was found for Analyses without correction for number of concept shifting. pregnancies revealed comparable results (WLTtot Likewise, there were no significant group p ¼ .013, WLTdr p ¼ .004, FLU p ¼ .020). differences in scores on the Stroop test (p ¼ .872
    • 486 R.H.M. DE GROOT ET AL. for the group differences concerning the mean of (Keenan et al., 1998; Sharp et al., 1993). In our Stroop Version I and II and p ¼ .491 for Ver- study, explicit memory (as measured by WLTtot sion III). Also, two-way ANOVA for repeated and WLTdr) was significantly impaired in the measures did not show any statistically significant pregnant group compared to the control group. differences. Finally, scores on the Letter Digit These results are consistent with those of Keenan Substitution Test were not statistically different et al. (1998), who, however, only found statisti- between the pregnant and the control groups cally significant differences in explicit memory in (p ¼ .624). the third trimester of pregnancy. Their group sizes, however, were small (10 pregnant women and 10 women in the control group). Sharp et al. DISCUSSION (1993) detected deficits in explicit memory in all trimesters of pregnancy. Studies performed later The aim of this study was to investigate whether in pregnancy have yielded conflicting data. Casey, memory and/or information processing speed is Huntsdale, Angus, and Janes (1999), as well as different in early pregnancy as compared to the McDowall and Moriarty (2000) did not find any nonpregnant state and, if so, which specific effect of pregnancy on different memory func- aspects are different. Our results show a clear tions. Brindle et al. (1991) found that implicit difference between women in early pregnancy memory was significantly impaired in primigra- and their matched controls with regard to perfor- vidae, while explicit memory was unimpaired in Downloaded At: 14:45 23 June 2010 mance on the WLTtot, its delayed recall, and the contrast to our findings. fluency test. These findings suggest that inten- In our study, speed of information processing tional learning and retrieval from semantic mem- did not differ between the pregnant women and ory are compromised. In contrast, speed of the control women. In contrast, Buckwalter et al. information processing under simple and more (1999) showed a lower performance on tasks complex conditions was not different. Thus, requiring speed of cognitive processing and memory functions in particular are affected in conceptual tracking during pregnancy as com- early pregnancy without consequences for atten- pared with performance after delivery. However, tion and speed tasks. However, the differences in they administered the tasks late in pregnancy cognitive performance between the two groups, (19.8 days prior to delivery), in contrast to our although statistically significant, are not large and study, and it may be that these cognitive functions may not be clinically important. Nevertheless, are only affected later in pregnancy. Thus, in early there is a possibility that these differences are pregnancy performance on intentional learning relevant, since they may cause suboptimum tests may be a more sensitive indicator of changed functioning. Therefore, further research is needed cognitive functioning than performance on speed to establish the clinical significance of the tasks. This is especially since women in the observed differences. In addition, it should be earlier phases of pregnancy may still have noted that our study had a cross-sectional design, sufficient attentional ‘resources’ to cope with the the results of which can be influenced by selec- demands of speed tasks. tion-bias. This implies that preexisting perfor- There is uncertainty about the mechanisms mance differences could have been present underlying the performance deficits seen in between the groups. Although the careful match- pregnancy. Changes in mood and even depres- ing between the groups makes it improbable that sion, as well as biological factors, or a combina- there is a systematic difference between the tion of biological and psychosocial factors have groups, a longitudinal study is needed in order been mentioned. Concerning the correlation to rule out this possibility. Till then the results of between mood during pregnancy and cognitive this cross-sectional study should be interpreted functioning, Harris, Deary, Harris, Lees, and with caution. Wilson (1996) observed that, after they corrected As far as we know, there are only few studies, for depression pregnancy was no longer asso- which investigated cognition in early pregnancy ciated with cognitive dysfunction. However,
    • MEMORY PERFORMANCE 487 Keenan et al. (1998) found that although pregnant factors, and hormones. A change in LC-PUFA women scored higher on both depression and availability could, therefore, explain our findings. anxiety scales, the pregnancy-related decline in During pregnancy, accretion of maternal, placen- memory was not attributable to these factors. It is tal and fetal tissue occurs and, consequently, the not likely that our findings were influenced by LC-PUFA requirements of pregnant women and mood changes or depression, because our study their developing fetuses are high (Clandinin et al., was performed in early pregnancy, when mood 1980). To obtain these LC-PUFA, the fetus mainly changes are minor, if present, in contrast to late depends on placental transfer and thus on the EFA pregnancy, close to delivery, when a substantial status and/or supply of the mother (Innis, 1991). proportion of pregnant women experience some- The overall biochemical LC-PUFA status of times profound psychological changes. However, women declines during pregnancy (Al, van preexisting mood differences between our two Houwelingen, & Hornstra, 2000) which may have groups cannot be completely ruled out, as this is functional consequences on maternal cognition. one of the limitations of a cross-sectional study In summary this cross-sectional study demon- design as has been stated before. strated less adequate memory performance in an Several biological factors may underlie the early pregnancy group as compared to a matched cognitive decline during pregnancy. One factor group of nonpregnant women. A longitudinal may be hormonal, because the levels of estrogen, study will be needed to establish clear association progesterone, testosterone, and dehydroepiandos- with pregnancy, especially any causal relation, Downloaded At: 14:45 23 June 2010 terone change considerably during pregnancy. and to find out whether the observed differences Buckwalter et al. (1999) tried to find a relation in early pregnancy disappear at some point after between impaired memory and the above-men- delivery. Currently, such a study is in progress in tioned hormones. They confirmed that cognitive our laboratory and results will become available functioning decreased during pregnancy, especially later this year. aspects of verbal memory, and that negative mood states were reported more often during pregnancy than after delivery. However, no consistent correla- REFERENCES tion was found between impaired memory and negative mood state or steroid hormone concentra- Al, M.D., van Houwelingen, A.C., & Hornstra, G. tions. Oxytocin has been mentioned as a possible (2000). Long-chain polyunsaturated fatty acids, pregnancy, and pregnancy outcome. The American factor, influencing cognitive function, but a corre- Journal of Clinical Nutrition, 71, 285S–291S. lation between oxytocin concentration and cogni- Baildam, E. (1991). Doctor as mum. BMJ, 303, 424. tive function during pregnancy has not been found Bie, S.E.D. (1987). Standaardvragen 1987: Voorstellen (Silber et al., 1990). Moreover, because the voor uniformering van vraagstellingen naar achter- oxytocin concentration does not change in early grondkenmerken en interviews [Standard questions pregnancy, this factor cannot explain the compro- 1987: Proposal for uniformisation of questions mised intentional learning and retrieval from regarding background variables and interviews] (2nd ed.). Leiden, The Netherlands: Leiden semantic memory found in our study. University Press. Another biological factor, which may be caus- Brand, N., & Jolles, J. (1985). Learning and retrieval ally implicated in the cognitive changes during rate of words presented auditorily and visually. The pregnancy, is nutrition. This particular applies to Journal of General Psychology, 112, 201–210. longer-chain, highly-unsaturated derivatives of Brett, M., & Baxendale, S. (2001). Motherhood and essential fatty acids, the so-called LC-PUFA. memory: A review. Psychoneuroendocrinology, 26, The latter compounds are very important struc- 339–362. Brindle, P.M., Brown, M.W., Brown, J., Griffith, H.B., tural components in brain tissue, where they & Turner, G.M. (1991). Objective and subjective perform an array of membrane-associated func- memory impairment in pregnancy. Psychological tions (Sastry, 1985). For instance, they can Medicine, 21, 647–653. influence membrane fluidity and thus affect the Buckwalter, J.G., Stanczyk, F.Z., McCleary, C.A., activities of neurotransmitters, peptides, releasing Bluestein, B.W., Buckwalter, D.K., Rankin, K.P.,
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