Journal of Psychosomatic Obstetrics & Gynecology, March 2009; 30(1): 5864

Cognitive function after pre-eclampsia: an explorative study

MARTINA BAECKE1, MARK E. A. SPAANDERMAN2, & SIEBEREN P. VAN DER WERF3

Department of Clinical Psychology, Medical Centre Spectrum, Enschede, The Netherlands, 2Department of Obstetrics and Gynaecology, Radboud University Nijmegen Medical Centre, The Netherlands, and 3Department of Medical Psychology, Radboud University Nijmegen Medical Centre, The Netherlands
1

(Received 24 July 2008; accepted 25 August 2008)

Abstract Background. Pre-eclampsia and eclampsia relate to cerebral damage. Memory and concentration problems are frequently reported after these pregnancy-related vascular complications. We tested the hypothesis that in formerly pre-eclamptic women cognitive functioning is impaired as compared with healthy parous controls. Methods. Women with a recent history of pre-term pre-eclampsia (PPE; n 47), term pre-eclampsia (TPE; N 18), preterm birth (PBI; n 32) or an uneventful pregnancy (UPR; n 72) completed a set of questionnaires, measuring cognitive problems, PTSD, depression, anxiety and fatigue. In addition, in PPE and UPR participants we tested neuropsychological performance. Results. PBI is related to higher levels of post-traumatic distress symptoms, which in turn diminished the neuropsychological test performance of PPE women. Nonetheless, women in the PPE and TPE groups did not report more cognitive problems than women in the PBI and UPR groups, but PPE raised the need for psychosocial cared. Conclusions. Cognitive complaints are common amongst young mothers. When tested, only those with psychological comorbidity have neuropsychological impairment.

Keywords: Pre-eclampsia, cognition, fatigue, anxiety, depression

Introduction Pre-eclampsia is a relatively common vascular complication of pregnancy, affecting about 5% of all gestations. These problems can be characterised by capillary leak and subsequent alterations in perfusion of maternal kidneys, liver, placenta as well as the brain [14]. Although delivery of the fetus and removal of the placenta eliminate the syndrome, pre-eclampsia may be viewed upon as a lifelong vascular disorder [3]. In this reasoning pre-eclampsia is the rst clinical expression of chronic endothelial cell dysfunction [5]. This may have remote consequences, as indicated by the more than fourfold risk on stroke [6]. Many studies focused on the acute neurological consequences of eclampsia, pre-eclampsia with epileptic seizures, and showed that neurological decits, such as cortical blindness, aphasia, limb weakness, paralysis, hemi paresis, facial nerve palsies, comatose and headache may result from cerebral oedema or cerebral hemorrhages. Yet, some imaging studies also

observed acute cerebral damage in small groups of pre-eclamptic patients with neurological symptoms [2,717]. Studies focusing on the acute cognitive consequences of severe pre-eclampsia gave conicting results. Rana et al. (2006) did not nd any neuropsychological performance differences, measured within 2 days postpartum, between pre-eclamptic patients and women with an uncomplicated pregnancy. In contrast, Brusse et al. (2008) showed, that 3 to 8 months post-partum, the word learning capacity was less for pre-eclamptic patients compared to women who had a normal pregnancy [18,19]. In clinical practice, many former pre-eclamptic patients report cognitive complaints until years after delivery, which may be an indication that long-term endothelial dysfunction causes cerebral damage. Concentration problems and a diminished ability to think are, however, also included in the DSM IV criteria of depression and PTSD [20], which are conditions that occur in more than 25% of formerly pre-eclamptic women [21]. In addition research showed that post-partum women in any case tend to

Correspondence: M. Baecke, Medisch Spectrum Twente, Department of clinical psychology, Haaksbergerstraat 55, 7513 ER Enschede, The Netherlands. E-mail: m.baecke@ziekenhuis-mst.nl ISSN 0167-482X print/ISSN 1743-8942 online 2009 Informa Healthcare USA, Inc. DOI: 10.1080/01674820802546212

Cognitive function after pre-eclampsia report worsening in memory performance [2225]. At the same time these studies did not nd any signicant underperformance of post-partum women on neuropsychological tests. Since there are no research data available about the frequency and specicity of cognitive complaints in former pre-eclamptic patients, it remains unclear whether these self-reported cognitive problems are a specic consequence of pre-eclampsia, reect actual neuropsychological dysfunction due to possible subtle cerebral vascular dysfunction, or can be ascribed to an affective disturbance following a major health threat involving both the mother and child. Furthermore, one can hypothesise that increased fatigue, which might be related to the care of a young child, contributes to cognitive complaints. To this end, we studied both the frequency and severity of cognitive complaints among pre-term- and term formerly pre-eclamptic women and compared these data to (1) women with a pre-term birth (PBI), but no other maternal complications, and (2) women with an uneventful pregnancy (UPR) and term delivery in their history. In all of these groups, we assessed the occurrence of mood disturbances and severe fatigue and their relation to cognitive complaints. Finally, cognitive functioning, mapped out by a standardised neuropsychological assessment, of former pre-eclamptic women was compared with that of women with an uneventful pregnancy. Measures

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Demographics. Information about demographics, age and education level, was gathered from all women with a standardised questionnaire. Cognitive complaints. The Cognitive Failures Questionnaire (CFQ) (score range: 0100) and a subscale of the Checklist Individual Strength (CIS_ concentration) (score range: 535) were used to measure the amount of self-reported cognitive complaints [2628]. Furthermore, we asked all women whether they experienced any of six different cognitive complaints since their pregnancy (Table I). Neuropsychological performance. To measure the cognitive and psychomotor capacity of two subgroups, pre-term pre-eclamptic women and women with an UPR in history, we administered a set of neuropsychological tests: The California Verbal Learning Task, The Symbol Digit Test, two reaction time tasks, The Grooved Pegboard and the Paced Auditory Serial Addition Test. The total words recalled after ve subsequent learning sessions on the California Verbal Learning Task (CVLT) is an indication of the womens verbal learning capacity [29,30]. The total number of correct responses on the Symbol Digit Test (SDT) of the Dutch version of the Wechsler Adult Intelligence Scale III (1970) is an indication of psychomotor speed capacity as well as the information processing ability [3133]. The mean reaction time on the simple and incompatible choice reaction time task is also an indication of movement speed capacity and information processing ability [34]. The time required to nish The Grooved Pegboard Test (GP) with the dominant hand is an indication of the ne motor control in the dominant hand [35]. The total number of correct responses on the 2-s stimulus interval condition of The Paced Auditory Serial Addition Test (PASAT) served as measure for divided attention under time pressure [36,37]. Affective functioning. The Beck Depression Inventory for Primary Care (BDI-PC) [38,39] (score range: 021) and the Dutch Trait Anxiety Scale (STAI) of the STAI-DY [40,41] (score range: 080) served as general measures of self-reported depressive symptoms and anxiety complaints. Higher scores on these questionnaires are indicative of higher levels of psychological distress. To establish possible symptoms of a post-traumatic stress (e.g., intrusions and avoidance) we used the Dutch version of the Impact of Event Scale (IES) [42]. The subscale scores, avoidance (score range: 040) and intrusions (score range: 035), are indicative of the size of the post-traumatic stress reaction.

Methods Participants and procedure This study was carried out at the Radboud University Nijmegen Medical Centre in the Netherlands and has been approved by the local medical ethical committee. Women who were hospitalised between January 2003 and January 2005 for preterm pre-eclampsia (PPE), term pre-eclampsia (TPE), PBI or UPR received a set of questionnaires 6 to 18 months post-partum. The former preeclamptic participants fullled the following criteria for pre-eclampsia: blood pressure exceeding 140/ 90 mmHg and proteinuria as urinary protein excretion over 300 mg per 24 h [1]. Participants in both pre-term groups delivered before 32 gestational weeks and participants in the TPE group and the UPR group delivered after 37 gestational weeks. Women with a multiple pregnancy were excluded in this study. Response rates were 76% (n 47) in the PPE group, 62% (n 18) in the TPE group, 75% (n 32) in the PBI group or 48% (n 72) in the UPR group. We administered a standardised neuropsychological assessment in subgroups of 26 pre-term pre-eclamptic women and 19 women with an UPR in history.

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M. Baecke et al.
Table I. Survey results concerning demographics, daily cognitive failures, post-traumatic stress and affective symptoms, fatigue. Term pre-eclampsia Group (n 18) Uneventful pregnancy Group (n 72)

Pre-term pre-eclampsia Group (n 48) Demographic variables Mean (sd) age Percentage (No.) education level Lower Intermediate Upper Daily Cognitive Failures Mean (sd) daily cognitive failures score (BCFQ) Mean (sd) daily concentration problems score (CIS-concentration) Mean (sd) of the total number of the following cognitive complaints Percentage (No.) Memory problems Percentage (No.) Cant think as quickly as before Percentage (No.) More easily distracted Percentage (No.) More difcult to concentrate Percentage (No.) Remembering the right word when talking Percentage (No.) Problems following conversation Psychological distress Mean (sd) impact of event score (IES_total) Percentage (No.) of women with an elevated (425) IES_total score Mean (sd) IES intrusions score (IES_intrusions) Mean (sd) IES avoidance score (IES_avoidance) Mean (sd) depression score (BDI_pc) Mean (sd) trait anxiety core (STAI_trait) Percentage (No.) of women with a denite childwish Percentage (No.) of women with a child wish that are seriously worried concerning a next pregnancy

Pre-term birth Group (n 32)

p-value

31.2 (3.7) 0.0 (0) 66.7 (32) 33.3 (16) 41.1 (17.3) 19.7 (8.8) 3.1 (2.3) 54 51 61 61 46 37 (22) (21) (25) (25) (19) (15)

30.9 (3.3) 0.0 (0) 61.1 (11) 38.9 (7) 40.9 (12.3) 18.7 (8.3) 3.7 (2.2) 56 61 78 72 61 50 (10) (11) (14) (13) (11) (10)

32.4 (4.8) 0.0 (0) 56.3 (18) 43.8 (14) 35.9 (13.7) 16.7 (9.7) 2.1 (2.2) 47 41 34 38 25 25 (15) (13) (11) (12) (8) (8)

34.0 (4.1) 1.4.(1) 47.2 (34) 51.4 (37) 39.1 (13.9) 18.0 (7.7) 2.7 (2.3) 38 46 56 58 35 39 (27) (33) (40) (42) (25) (28)

0.00*** 0.46

0.46 0.44 0.07

25.3 (15.4) 44 (21) 16.6 8.7 2.7 39.9 65 39 (9.3) (8.2) (3.5) (11.8) (31) (15)

10.5 (9.7) 11 (2) 8.3 2.2 1.3 39.6 59 14 (6.9) (3.9) (1.5) (10.0) (10) (2)

20.0 (15.2) 41 (13) 12.9 7.2 1.2 35.4 47 43 (8.4) (8.1) (1.8) (11.1) (15) (9)

12.7 (11.4) 11 (8) 7.0 5.7 1.8 37.2 57 9 (6.6) (7.0) (3.4) (10.6) (41) (5)

0.00*** 0.00*** 0.00*** 0.01** 0.11 0.27 0.77 0.00***

Percentage (No.) of women who received psychosocial care after pregnancy Social worker 23 (11) Psychologist 4 (2) Psychiatrist 4 (2) Fatigue Fatigue (CIS-fatigue) Percentage (No.) severe fatigue (Cis-fatigue 439) *p 5 0.05, **p 5 0.01, ***p 5 0.00. 35.1 (15.3) 47 (23)

6 (1) 0 (0) 0 (0) 36.0 (11.7) 44 (8)

15 (5) 0 (0) 0 (0) 31.4 (14.1) 28 (9)

4 (3) 3 (2) 2 (1) 33.7 (12.3) 38 (27)

0.01** 0.58 0.47 0.60 0.38

Fatigue The degree of experienced fatigue was measured the fatigue severity subscale of Checklist Individual Strength (CIS-fatigue: range 856), scores exceeding 39 are indicative of severe fatigue [43]. Statistics One-way analyses of variance were used to identify group differences among the survey data and neuropsychological test results. In case of signicant demographic differences the analyses of variance of the survey data were repeated with the specic demographic variable as covariate. A similar approach was used to study the relations between psychological distress and neuropsychological

performance. In case of signicant differences on distress variables, we used these variables as covariates in the comparisons of the neuropsychological test results between a subgroup of pre-term pre-eclamptic women and a subgroup of women with an UPR in history. a was set at 0.05 and posthoc tests were carried out by using the Scheffe correction. Results With respect to the survey participants there was a signicant difference in mean age. The group of women with an UPR in history was older compared with the group of pre-term pre-eclamptic women. The four groups did, however, not differ on education level (Table I).

Cognitive function after pre-eclampsia Self-reported cognitive problems (Table I) Among the four groups there were no signicant differences in any of the three cognitive symptom measures (BCFQ, CIS_concentration and total number of reported cognitive symptoms). Nonetheless, cognitive problems were experienced at high frequency in all groups of participants. Affective symptoms and fatigue (Table I) No signicant group differences were found with respect to general distress (BDI-pc and STAI), or fatigue (CIS-fatigue). However, irrespective of its cause, women with a pr-eterm delivery in their history reported more post-traumatic stress symptoms than women with a term delivery after an uncomplicated pregnancy (PPE vs. UPR; OR 6.2 (95% CI 2.4515.77), PBI vs. UPR; OR 5.5 (95% CI 1.9815.16) and even as compared with those with a-term maternal disease (PPE vs TPE; OR 6.2 (95% CI 1.2930.1). Furthermore the percentages of women who had serious worries about a possible next pregnancy were sixfold higher in both groups of women with a pre-term delivery than in both groups of women with a term delivery ( p 0.002). In addition, the women with a pre-term delivery overall received four to ve times more often help of a social worker after their problematic pregnancy than women with a term delivery ( p 0.012). Neuropsychological test results (Table II) The tested subgroups of pre-term pre-eclamptic women and women with an UPRin their history

61

did not differ on age and education level. These subgroups seemed also comparable with both the groups of pre-term pre-eclamptic survey participants and the survey participants with an uneventful pregnancy, since there were no signicant differences in age, marital status, years of education, reported cognitive complaints, distress and fatigue. The two tested subgroups did not differ in their verbal learning capacity, reaction and movement times and ne motor speed. The comparisons between both groups did, however, showed differences with respect to the number of correct responses on the PASAT, (95% CI: PASAT 71.10 to 711.52) and the SDT-total score (95% CI: 710.93 to 70.32). In both cases the group of women with an UPR outperformed the group of pre-term pre-eclamptic women. Relations between post-traumatic stress symptoms and cognitive test performance Since the group of women with an UPR and the group of pre-term pre-eclamptic women differed in their post-traumatic stress symptoms scores we carried out covariance analyses with PASAT and SDT scores as dependent measures and with the total IES score as covariate. In these analyses the original group differences disappeared while the IEStotal scores approached signicant associations with both PASAT and SDT. Post-hoc analyses showed that in the PPE group especially a higher degree of intrusions (IES-intrusions) was associated with worse PASAT and SDT performance (Spearmans rho correlations of 70.56, p 0.001 and 70.44, p 0.021 respectively).

Table II. Neuropsychological test results. Pre-term Pre-eclampsia (n 27) Demographic variables Mean (sd) age Percentage (No.) education level Lower Intermediate Upper Neuropsychological test results mean (sd) Total number of words recalled (Californian Verbal Learning Test) Information processing speed (simple RT) in milliseconds Movement time (simple RT) in milliseconds Information processing speed (complex RT) in milliseconds Movement speed (complex RT) in milliseconds Seconds to complete grooved pegboard with dominant hand Number of correct responses on the paced auditory serial attention test Number of correct responses on the symbol digit test *p 5 0.05. Uneventful pregnancy (n 19)

p-value

31.8 (3.8) 0.0 (0) 51.9 (14) 48.1 (13) 61.0 378 256 464 304 57 37.6 61.7 (8.9) (99) (75) (160) (106) (6) (9.1) (8.7)

33.4 (2.8) 0.0 (0) 42.1 (8) 57.9 (11) 64.5 369 262 433 291 55 44.0 67.4 (6.0) (42) (68) (54) (72) (4) (7.0) (8.9)

0.12 0.52

0.14 0.75 0.81 0.46 0.66 0.09 0.02* 0.04*

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M. Baecke et al. as the women in our PPE group. A nding comparable to the results of both Engelhard and Kersting who also found that giving PBI is a traumatic event, which causes increased levels of post-traumatic stress symptoms [22,45]. Several limitations of this study should be taken into account. First, the neuropsychological tests were administered to samples that were relatively small and second, we choose to contrast a group of women who had a more severe pre-eclampsia in history with a group of women with an uncomplicated pregnancy in history. Perhaps we would have been able to come to a rmer and more decisive answer about the possible detrimental role of disease specic distress on the neuropsychological test performance when we would have tested all four patient groups. Third, in this study we controlled for pre-eclampsia severity by discriminating pre-term and term pregnancies. Correlating the test performance to both current somatic parameters and parameters measured during pregnancy would be an interesting addition to this study. Fourth, since we administered our survey and tests 6 to 18 months after delivery, we are unable to discriminate between the acute neuropsychological consequences and the consequences of chronic endothelial dysfunction. There is some evidence for an acute decline in word learning capacity in preeclamptic patients [19], which might have been recovered by the time we administered the test battery. A longitudinal study would give insight to the course of cognitive functioning after pre-eclampsia. Overall, the results suggest that cognitive complaints are common among former pre-eclamptic women, but comparable with other women who had a normal or otherwise complicated pregnancy. Although there was no conclusive evidence for widespread neuropsychological impairment among former pre-eclamptic women, some performance differences were found. The results of this study might be important for women with pre-eclampsia in their history. It is likely that these women attribute their cognitive complaints to the physical consequences of pre-eclampsia, which in turn might worry them. Explaining patients that cognitive complaints are quite common after having a baby and that reduced cognitive functioning may reect increased levels of stress and worry, could be helpful. Furthermore, we found similar levels of depression, anxiety and experienced fatigue among our groups, but pre-term pregnancy in general was associated with more post-traumatic symptoms and pre-disposed to more distress about planning a next pregnancy. The anxiety about a next pregnancy might stem from the increased risk for a next problematic pregnancy. Regarding the frequent consultation of a social worker due to this distress after giving PBI it might be recommended to offer

Discussion To our knowledge this is the rst study specically assessing cognitive complaints experienced after preeclampsia. Against our expectation, we found that former pre-eclamptic women did not report more concentration problems or daily cognitive failures compared with women who gave PBI, or who had an uncomplicated pregnancy. In all four groups considerable proportions of women indicated to experience memory problems, word nding difculties, or slowing of thinking, since their pregnancy. These ndings do suggest that these types of complaints and their severity are not specic to post-partum preeclampsia patients, but generally occur in mothers with young children. Other studies also found an increase in cognitive complaints in both pregnant or post-partum women, which were suggested to be a function of personal and social factors, and possibly sleep quality instead of cognitive deterioration [2225]. Albeit our study did not nd any group differences on reported cognitive problems we did nd group differences in actual test performance between preterm pre-eclamptic women and women with an uncomplicated pregnancy in history. The results of the pre-eclamptic women stayed behind on two tests of time pressured mental efciency, which are both considered sensitive for mental slowing and problems with working memory [33,37]. Because we did not nd an underperformance of the former preeclamptic patients on the verbal learning capacity, ne motor speed, reaction and movement times, one could argue that the cognitive impairment after preeclampsia might be subtle and only manifests on complex tasks, which require a combination of different cognitive processes simultaneous. Another possible explanation could be that since both the PASAT and the SDT were administered at the end of the assessment and therefore might reect deterioration in cognitive endurance in the former pre-eclamptic women. Because intrusions- and avoidance symptoms as well as worrying about planning a next pregnancy are more common after PBI, a third explanation might be the known sensitivity of these time-pressured tests for distress [44]. Post-hoc analyses indeed showed that the neuropsychological differences in test performance disappeared when we controlled for the severity of post-traumatic stress symptoms. In the pre-eclampsia group, the degree of experienced intrusive thoughts was related to the performance on the neuropsychological functioning. Perhaps the role of disease specic distress upon cognitive test performance can be elucidated if a group of women with a preterm delivery but no pre-eclampsia in history is also tested. The survey showed that these women suffer from similar levels of post-traumatic stress symptoms

Cognitive function after pre-eclampsia these women psychological consultations besides the medical check-up. Declaration of interest: The authors report no conicts of interest. The authors alone are responsible for the content and writing of the paper. References
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Current knowledge on this subject . . . Preeclampsia and eclampsia relate to cerebral damage. Preeclampsia is the rst expression of chronic endothelial dysfunction. In clinical practice many former preeclamptic patients report cognitive complaints until years after delivery.

What this study adds . . Cognitive complaints are not specically related to preeclampsia, but common amongst young mothers. Six to eighteen months postpartum pre-eclamptic women performed worse on two tests of time pressured mental efciency compared to women with an uncomplicated pregnancy. This subtle neuropsychological impairment is related to psychological co-morbidity.