Childhood trauma and adult declarative memory performance in the general population: The mediating effect of alexithymia

Child Abuse & Neglect 101 (2020) 104311

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Childhood trauma and adult declarative memory performance in the general population: The mediating effect of alexithymia

T

Jan Terocka,b,*, Sandra Van der Auweraa,c, Deborah Janowitza, Katharina Wittfeldc, Stefan Frenzela, Johanna Klinger-Königa, Hans J. Grabea,c a

Department of Psychiatry and Psychotherapy, University Medicine Greifswald, Ellernholzstraße 1-2, 17475 Greifswald, Germany Department of Psychiatry and Psychotherapy, HELIOS Hanseklinikum Stralsund, Rostocker Chaussee 70, 18437 Stralsund, Germany c German Center for Neurodegenerative Diseases DZNE, Site Rostock/ Greifswald, Ellernholzstraße 1-2, 17475 Greifswald, Germany b

A R T IC LE I N F O

ABS TRA CT

Keywords: Childhood abuse Childhood neglect Verbal declarative memory Alexithymia Emotion processing General population

Background: Previous studies suggested that childhood maltreatment is associated with altered memory performance in adulthood. Deficits in identifying and describing feelings as captured by the alexithymia construct are strongly linked with childhood trauma and may mediate the associations with memory function. Objective: To investigate the associations of childhood trauma with verbal declarative memory performance and the putative mediating role of alexithymia. Method: Associations of the different dimensions of childhood trauma with adult declarative memory performance were tested in two large, independent general population samples comprising a total of N = 5574 participants. Moreover, we tested whether associations were mediated by alexithymia. Results: In both samples, childhood emotional neglect, but not abuse emerged as a negative statistical predictor of early (sample 1: β=-1.79; p < 0.001, sample 2: β=-0.26; p < 0.001) as well as delayed recall (β=-0.78; p < 0.001; β=-0.24; p < 0.05). Likewise, childhood emotional neglect was the strongest predictor for alexithymia (β = 3.2; p < 0.001; β = 3.54; p < 0.001). Finally, the association between childhood emotional neglect and early (Total Mediated Effect (TME): 13.2, CI: 0.087-0.302; TME: 20.1; CI: 0.123-0.619) as well as late recall (TME: 13.2, CI: 0.086-0.301; TME: 9; CI: -0.442-0.699) was significantly mediated by alexithymia. Conclusions: Our findings suggest that childhood emotional neglect is particularly detrimental to memory functioning in adulthood. In comparison, childhood abuse was not associated with reduced declarative memory capacity. Our results contribute to explain the mechanism underlying the relation of childhood trauma and memory deficits: Finding specific associations with emotional neglect and a mediating role of alexithymia highlights the relevance of emotion processing capacities for memory functioning.

1. Introduction Severe childhood adversities such as abuse and neglect have been found to be associated with lasting effects on

⁎ Corresponding author at: Department of Psychiatry and Psychotherapy, HELIOS Hanseklinikum Stralsund, Rostocker Chaussee 70, 18437 Stralsund, Germany. E-mail address: [email protected] (J. Terock).

https://doi.org/10.1016/j.chiabu.2019.104311 Received 6 July 2019; Received in revised form 21 October 2019; Accepted 2 December 2019 0145-2134/ © 2019 Elsevier Ltd. All rights reserved.

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neuropsychological functioning across the lifespan. For example, studies investigating adult survivors of childhood traumatization showed lower IQ levels, reading abilities, school performance and academic achievements (Aas et al., 2012; Bücker et al., 2013). Regarding effects of child maltreatment on memory functioning, results from existing studies are inconsistent to some degree: Gould et al. investigated different dimensions of neuropsychological functioning in a mixed sample of traumatized subjects with and without major depressive disorder or PTSD (Gould et al., 2012). The authors found differential effects of abuse and neglect on various aspects of cognitive performance including visual memory and spatial working memory. In their review and meta-analysis, Malarbi et al. found an overall deficit in neuropsychological functioning in trauma-exposed children with specific deficits in learning and memory functioning (Malarbi, Abu-Rayya, Muscara, & Stargatt, 2017). Only few studies investigated memory functioning in relation to childhood trauma in non-clinical samples: Majer et al. examined 47 healthy participants and found associations of emotional abuse and physical neglect with impaired spatial working memory performance (Majer, Nater, Lin, Capuron, & Reeves, 2010). In contrast, Barzilay et al. found episodic memory performance being the only cognitive domain that was not negatively associated with traumatic stress in a community sample of children and adolescents (Barzilay et al., 2018). Finally, in their large-scale general-population study, Dunn et al. (2016) found that exposure to childhood physical or sexual abuse was not generally associated with altered memory performance, However, their findings revealed differential associations depending on the developmental timing of exposure to abuse. Cromheeke et al. reported about impaired working memory capacities specifically for positive emotions in women with history of childhood abuse, indicating that childhood abuse has lasting influence on emotion processing, which in turn affects memory performance (Cromheeke, Herpoel, & Mueller, 2014). In sum, previous studies provided evidence for differential effects depending on the type of trauma, the time of exposure and specific memory domains. Inconsistencies in existing studies may also partly be due to sample sizes and sample compositions with studies comprising relatively healthy participants (Barzilay et al., 2018; Majer et al., 2010) on one hand and clinical subjects with severe mental disorders like PTSD or depression (Gould et al., 2012) on the other hand. Alexithymia, a personality trait characterized by difficulties in identifying and describing emotions may also contribute to explain the association between childhood adversities and impaired memory performance: previous studies showed that childhood adversities and particularly emotional neglect are strongly associated with alexithymic personality features (Terock, Van der Auwera, Janowitz, Homuth et al., 2018, 2016; Zlotnick, Mattia, & Zimmerman, 2001). Emotions facilitate indexing memories of value and therefore represent important moderators of learning and memory performance (Dolan, 2002). It has been suggested that individuals high in alexithymia show problems in linking emotions with memories (Taylor, Bagby, & Parker, 1999) and therefore may have reduced abilities to learn and recall information. Support for this hypothesis came from Luminet et al., who found highly alexithymic students showing deficits in the recall of emotional words compared to students low in alexithymia, while the authors found no difference in the recall of neutral expressions (Olivier Luminet, Vermeulen, Demaret, Taylor, & Bagby, 2006). Vermeulen et al. investigated the subfactors of alexithymia in relation to memory for emotion and neutral words in a sample of 65 healthy students. The authors found negative associations of the “difficulties identifying feelings” factor (DIF) with memory performance for emotion words, while the “externally oriented thinking” factor (EOT) was positively associated with the recall of emotion as well as neutral words (Vermeulen & Luminet, 2009). In a previous study of our working group, we found associations of alexithymia and particularly the EOT factor with poorer immediate and delayed retrieval of semantically unrelated words in the general population (Terock, Van der Auwera, Janowitz, Klinger-König et al., 2018). Contrasting with these findings, Nielson and Meltzer found no differences in delayed word recall after emotional arousal between participants scoring high versus low in alexithymia in a sample of 60 healthy subjects (Nielson & Meltzer, 2009). Likewise, Suslow et al. as well as Lundh et al. found no significant correlations of alexithymia with recalling emotional words in non-clinical subjects (Lundh, Johnsson, Sundqvist, & Olsson, 2002; Suslow, Kersting, & Arolt, 2003). Taken together, studies on the relation of childhood adversities and memory performance produced mixed results. In contrast, childhood adversities were consistently found to be strongly associated with alexithymia. Given that emotions are important factors in learning and recalling information, the occurrence of alexithymic personality traits may mediate the relationship between childhood adversities and impaired memory functioning and contribute to explain the currently inconclusive findings. In detail, we expected that (I) childhood trauma and its different dimensions are negatively associated with immediate and delayed recall of words and that (II) this association is mediated by alexithymic personality traits. 2. Methods 2.1. Samples We analyzed data from the Study of Health in Pomerania (SHIP) (Völzke et al., 2011) comprising adult German residents in northeastern Germany. From the total population of West Pomerania comprising 213 057 inhabitants in 1996, a two-stage stratified cluster sample of adults aged 20–79 years was drawn. The net sample (without migrated or deceased persons) comprised 6265 eligible subjects. 4308 Caucasian subjects participated at baseline SHIP-0 (1997–2001). To date, three regular follow‐ups have been carried out (SHIP‐1 with n = 3300 from 2002 to 2006; SHIP‐2 with n = 2333 from 2008 to 2012 and SHIP-3 with n = 1718 from 2014 to 2016). In parallel, detailed assessments of life events and mental disorders were conducted within the SHIP‐LEGENDE study (Life Events and Gene–Environment Interaction in Depression) from 2007 to 2010. A separate stratified random sample of 8016 adults aged 20–79 years was drawn for SHIP-TREND (Völzke et al., 2011) in 2008 from the same area and n = 4420 subjects participated. The target sample size was chosen to obtain a final sample size similar to that of SHIP-0. Similar examinations like in SHIP and SHIP-LEGENDE were conducted. 2

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2.2. Instruments Amongst others, subjects of SHIP-LEGENDE were administered the Auditory Verbal Learning and Memory Test (VLMT), a German adaption of the widely used Rey Auditory Verbal Learning Test (C. Helmstaedter & Durwen, 1990). In addition, participants filled in the Toronto Alexithymia Scale 20 (TAS-20) (Bach, Bach, de Zwaan, Serim, & Böhmer, 1996; Bagby, Parker, & Taylor, 1994) and the Childhood trauma questionnaire (CTQ) (Bernstein & Fink, 1998; Wingenfeld et al., 2010). In SHIP-TREND similar instruments like the TAS-20 and the CTQ were used. For the assessment of verbal memory, the Nuremberg Age Inventory (NAI) was used (Oswald & Fleischmann, 1999). In SHIP-LEGENDE, an abridged version of the VLMT was used to assess short-term learning as well as delayed retrieval. Subjects were asked to remember semantically unrelated nouns from an orally presented list in three consecutive encoding runs. Participants had 120 s after each encoding run for immediate retrieval. A sum score of the correctly remembered terms of the three encoding runs was formed to measure short-term learning. Late retrieval was tested 20 min after the first encoding trial. The number of correctly remembered words reflected long-term retrieval. The English Auditory Verbal Learning Test showed satisfactory recall reliability (0.70) and a moderate test-retest reliability (0.55). A close correlation with the California Test of Verbal Learning (0.5 – 0.65) support its validity (Schmidt, Lezak, & Test, 2019). For the German VLMT, no metrics on reliability are available. However, results showed a high convergent validity with the AVLT (Helmstaedter, Lendt, & Lux, 2001). Instead of the VLMT, the word list of the Nuremberg Age Inventory (NAI) was used as a measure for short- and delayed memory performance with recall after 20 min in SHIP-TREND. The NAI is a German test developed to measure the cognitive abilities during brain aging (Oswald & Fleischmann, 1999). It consists among others subtests of a list of eight semantically unrelated words. Eight words are read to the participant, who is asked to recall as many words as possible immediately. After 20 min the participant is asked to retrieve the eight words previously learned from a list containing eight additional distractor words. The number of correctly identified words is summarized to a sum score minus the number of identified distractor words. It validated in a large general population sample and showed satisfactory psychometric properties with a good objectivity, an internal consistency of 0.69 and retest reliability of 0.66. Alexithymia was assessed using the German version of the TAS-20 (Bach et al., 1996; Bagby et al., 1994), composed of 20 items representing three different factors: (1) Difficulty in identifying feeling (DIF), (2) difficulty in describing feeling (DDF) and (3) externally oriented thinking (EOT). The German version has similarly good psychometric properties as the original version. The English version showed a good internal consistency (Cronbach’s α: 0.81) and a satisfactory test-retest reliability (5-year interval: 0.69, (Salminen, Saarijärvi, Toikka, Kauhanen, & Äärelä, 2006). For the German version, Bach et al. found a comparable internal consistency as well as a satisfactory test-retest reliability and could replicate the three factor structure (Bach et al., 1996). Childhood trauma was assessed using the 34-item version of the CTQ, a widely used self-report scale (Bernstein & Fink, 1998; Wingenfeld et al., 2010). It comprises 5 different subscales: emotional abuse, physical abuse, sexual abuse, emotional neglect, and physical neglect. Responses are made on a 5-point Likert-type scale to express the frequency of occurrence and ranges from ‘never true’ to ‘very often true’. In addition to dimensional scoring procedures the manual provides threshold scores to determine the severity of abuse and neglect dimensions (none = 0, mild = 1, moderate = 2 and severe to extreme = 3). A subject was rated as positive for a subscale when a severity score of ≥2 (at least moderate) was reported. A subject was rated as positive for overall abuse/ neglect when at least in one of the subscale a severity score of ≥2 (at least moderate) was reported. Factor structure and construct validity of the German version showed sufficient psychometric properties with some limitations due to the high inter-correlations of the different subscales and a weak internal consistency of the physical neglect subscale (Klinitzke, Romppel, Häuser, Brähler, & Glaesmer, 2012). In both samples, the lifetime diagnosis of major depressive disorder (MDD) according to DSM-IV criteria was determined using the standardized and computerized Munich-Composite International Diagnostic Interview (M-CIDI) (Wittchen, Lachner, Wunderlich, & Pfister, 1998). The M-CIDI is a fully structured interview-based instrument for the assessment of eight major classes of DSM-IV diagnoses including MDD over the lifespan. It was developed based on the WHO-CIDI in order to enhance the feasibility while maintaining the reliability (Wittchen et al., 1998). Excellent psychometric properties for the M-CIDI have been shown (Wittchen, 1994). The computer-assisted interview was conducted by clinically experienced interviewers (psychologists). We used the lifetime diagnosis of MDD as a dichotomous outcome measure. Wittchen et al. found a combined sensitivity for the two questions of 62.6 % for depressive disorders. However, more detailed analysis in the original investigation showed that primarily fairly short depressive episodes were not detected by the CID-S (H.-U. Wittchen et al., 1999). The PTSD module of the Structured Clinical Interview for Diagnostic and Statistical Manual of Mental Disorders, 4th Edition (DSM-IV) was applied for the assessment of PTSD (Elhai, Gray, Kashdan, & Franklin, 2005) in SHIP-LEGENDE only. First, subjects were asked if they had been exposed to one of the following events which are enlisted as traumatic events in the DSM-IV: combat or war-zone experience, physical assault, rape, childhood sexual abuse, natural disaster, life-threatening illness, serious or nearly fatal accident, imprisonment and/or torture, sudden and unexpected death of a loved one, as well as witnessing or learning about traumas to others. If the participant answered with “no” to each of these questions, the module was terminated. If a participant affirmed exposure to more than one traumatic event, the person was asked to identify the most distressing experience and to relate to this event when answering the subsequent questions. The PTSD symptoms according the DSM-IV were then continuously asked in the interview. If the respondent did not pass the required diagnostic threshold (e. g. at least one re-experiencing symptom), the interview was also terminated. It has been found as a useful screening device with satisfactory sensitivity (66 %–76 %) and specificity (67 %–87 %) for detecting traumas in samples of medical patients as well as healthy subjects (Elhai, Franklin, & Gray, 2008). After exclusion of subjects due to missing data, at least 1916 subjects from SHIP-LEGENDE and 3658 subjects from SHIP-TREND were included in our analyses. 3

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In SHIP-LEGENDE the missings were mainly due to the psychometric variables TAS-20, childhood trauma and verbal memory. Subjects that had to be excluded were significantly older and had a lower level of education. There were no differences in sex and MDD. In SHIP-TREND the missings were mainly due to TAS-20 and childhood trauma. Subjects that had to be excluded were significantly older, had a lower level of education and a lower verbal memory score for immediate recall. There were no differences in sex, MDD and delayed recall. 2.3. Statistical analyses Subject characteristics were assessed by mean and standard deviations for metric variables and with numbers and percentages for categorical data. Sample comparisons were performed using t-test for metric variables and Chi2-test for categorical variables. 2.3.1. Association analyses To assess the strength of the association between childhood trauma, including the five subscales, with immediate as well as delayed recall of neutral words, linear regression analyses were applied. Additional linear regression analyses were performed to assess the associations of childhood trauma, including the five subscales, with TAS-20. Analyses were performed in each sample separately as different measures for verbal memory (VLMT in SHIP-LEGENDE and NAI in SHIP-TREND) were applied. To account for the non-normal distribution of the outcome variables, confidence intervals and p-values were assessed through bootstrapped regression with 1000 replicates. All analyses were adjusted for age, sex, school education and lifetime diagnosis of MDD. Based on previous studies showing effects on memory performance, sensitivity analyses adjusting for the behavioral factors current smoking status, weekly alcohol consumption and self-reported physical activity were performed. As we performed one analysis for each CTQ subscale on immediate and delayed retrieval of words each, we set the Bonferroni corrected p-value threshold in the discovery sample SHIP-LEGENDE to pcorrected < 0.005 correcting for N = 5 tests. In the replication sample SHIP-TREND nominal significance (p < 0.05) was considered statistically significant. 2.3.2. Mediation analyses In mediation analyses we tested if the effect of childhood trauma on verbal memory was at least partly mediated through TAS-20 scores. Mediation analyses were performed with the medeff function from the mediation package for STATA (Hicks & Tingley, 2011). Medeff reports the summary estimates of the mediation, direct, and total effects after 1000 simulations. Finally, medeff also reports the average causal mediation effect and percentage of the effect that was mediated. In our models the CTQ subscales were taken as predictor variables, TAS-20 as mediating factor and verbal memory (immediate and delayed recall of words) as outcome variable. The models were again adjusted for age, sex, school education and lifetime diagnosis of MDD. Analyses were performed using STATA/MP software, version 14 (StataCorp LP, College Station, TX). 3. Results Table 1 presents basic sociodemographic data and mean scores of CTQ, TAS-20 and VLMT/NAI in SHIP-LEGENDE and SHIPTREND. Multiple linear regression results of the association between abuse (and its 3 subscales) and neglect (and its 2 subscales) and cognitive performance are presented by Table 2. 3.1. Childhood trauma and memory Childhood neglect and particularly emotional neglect showed significant negative associations with immediate recall of words in both samples (SHIP-LEGENDE p = 8.0E-7, SHIP-TREND p = 1.9E-4; Fig. 1) as well as negative associations with delayed recall in SHIP-LEGENDE (p = 4.7E-4). In SHIP-LEGENDE the occurrence of childhood emotional neglect led to a decreased VLMT score of 1.79 and 0.78 for immediate and delayed recall, respectively. This corresponds to 29 % and 25 % of the standard deviation in immediate and delayed recall of words in the VLMT. Similar in SHIP-TREND a decrease of 1.3 score points for immediate recall of the NAI corresponds to 26 % of the standard deviation of this variable. Childhood abuse showed no significant association in any of the analyses. The association with childhood neglect were mainly carried by the subscale emotional neglect which showed significant negative associations with immediate and delayed recall in both samples (see Table 2). We also tested physical neglect which only showed a significant impact in SHIP-TREND regarding immediate recall. 3.2. Alexithymia and memory Alexithymia had a negative impact on early recall of words in both samples and delayed recall of words in SHIP-LEGENDE. In this subsample the p-values for early recall were p = 8.1E-6 and 1.0E-6 for SHIP-LEGENDE and SHIP-TREND, respectively, and p = 4.3E6 for delayed recall in SHIP-LEGENDE. These associations were mainly carried by the externally oriented thinking (EOT) factor. Alexithymia showed no significant associations with delayed recall of the NAI in SHIP-TREND (p = 0.13). However, the test procedure for the delayed recall of the NAI is considerably different to all other memory assessments applied in this study which will be addressed in the discussion. Additional adjustment for physical activity, alcohol consumption and smoking status did not change the significance of the results (Table 3). 4

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Table 1 Descriptive statistic of outcome, predictor and covariables used in the statistical models for SHIP-LEGEND and SHIP-TREND.

Age Sex CTQ sum Abuse* Emotional Physical Sexual Neglect* Emotional Physical TAS sum TAS DIF TAS DDF TAS EOT Verbal recall score Immediate recall Delayed recall Education < 10 years 10 years > 10 years MDD PTSD

SHIP-LEGEND (N = 1916)

SHIP-TREND (N = 3658)

Comparison

55 ± 13.7 Male: 902 (47%) 33.7 ± 9.2 Range: 25-119 164 (8.6%) 61 (3.2%) 90 (4.7%) 66 (3.4%) 250 (13%) 215 (11%) 90 (5%) 44.8 ± 9.5 Range: 20-77 12.6 ± 4.5 11.8 ± 3.4 20.4 ± 4.2 VLMT 24.8 ± 6.2 Range: 2-45 8 ± 3.1 Range: 0-15

51 ± 15.2 Male: 1789 (49%) 33.2 ± 9.5 Range: 25-115 256 (7.0%) 134 (3.7%) 138 (3.8%) 89 (2.4%) 695 (19.00%) 394 (11%) 553 (15%) 41.5 ± 9.1 Range: 20-85 10.8 ± 4 10.5 ± 3.4 20.1 ± 4.4 NAI 5.3 ± 1.3 Range: 0-8 5.7 ± 1.7 Range: -3-8

T = 9.5, p < 0.001 Chi2 = 1.7, p = 0.19 T = 1.7, p = 0.1

501 (26%) 1023 (53%) 392 (21%) 317 (16.5%) 19 (1%)

752 (20%)693 1932 (53%) 974 (27%) 673 (18.4%) NA

Chi2 = 4.4, p = 0.036 Chi2 = 0.9, p = 0.36 Chi2 = 2.7, p = 0.1 Chi2 = 4.8, p = 0.029 Chi2 = 31.6, p < 0.001 Chi2 = 0.26, p = 0.61 Chi2 = 133.8, p < 0.001 T = 12.9, p < 0.001 T = 15.4, p < 0.001 T = 13.8, p < 0.001 T = 1.9, p = 0.06 N/A N/A Chi2 = 37.1, p < 0.001

Chi2 = 3.0, p = 0.09 N/A

CTQ: Childhood Trauma Questionnaire; TAS: Toronto Alexithymia Scale-20; DIF: Difficulties Identifying Feeling; DDF: Difficulties Describing Feelings; EOT: Externally Oriented Thinking; VLMT: Verbal Learning and Memory Test; NAI: Nuremberg Age Inventory; MDD: Major Depressive Disorder; PTSD: Posttraumatic Stress Disorder; N/A: Not applicant. * abuse and neglect are dichotomized variables, a subject was rated as positive for overall abuse/neglect when at least in one of the dimensions a severity score of ≥2 (at least moderate) was reported. Subscales for abuse/neglect are coded none/mild versus moderate/severe.

3.3. Childhood trauma and alexithymia We tested the association between childhood abuse/neglect (and subscales) and alexithymia (sum score and subscales) (see supplement Table S1). Neglect and particularly emotional neglect were highly positively associated with TAS-20 sum score in SHIPLEGENDE as well as in SHIP-TREND (see Table 4). Physical neglect was mainly significant in SHIP-TREND. The individual alexithymia factors DIF and DDF showed the strongest associations with neglect (see supplement Table S1). 3.4. Mediation analyses As the requirements for mediation analyses are fulfilled for childhood neglect, alexithymia and verbal memory, we performed mediation analyses for the path from childhood neglect to recall of words (immediate or delayed) mediated by alexithymia (TAS-20 sum score). Each model was applied on the SHIP-LEGENDE and SHIP-TREND sample (Table 4). Significant mediating effects were found for immediate and delayed word recall in SHIP-LEGENDE with total mediated effect (TME) around 13 % in both analyses and average causal mediated effect (ACME): -0.164 and -0.082, respectively. In SHIP-TREND, 20 % of the statistical effect of childhood neglect were mediated through TAS-20 for immediate recall. No significant mediating effect for TAS-20 on late recall emerged in SHIP-TREND. In exploratory analyses we investigated the mediating effects of the subscales of TAS-20 on the path from emotional and physical neglect to recall of words using the same set of covariables. The results showed that TAS-20 was a significant statistical mediator in all models except for delayed recall in SHIP-TREND. We found EOT emerging as a significant mediator on the path from emotional neglect to immediate as well as delayed recall of words. 4. Discussion The aims of the present study were to investigate the associations of different dimensions of childhood maltreatment with adult declarative memory performance and the mediating effects of alexithymia. We found that childhood neglect, but not abuse was significantly associated with immediate as well as delayed recall of words. When analyzing the CTQ subscales, we found that this association was predominantly carried by the emotional neglect dimension, while physical neglect was not significantly associated with altered memory performance except in one analysis. Replicating previous 5

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Table 2 Results for the multiple linear regression analyses investigating the association between childhood trauma dimensions and verbal memory in SHIPLEGEND and SHIP-TREND. Predictor SHIP-LEGEND Neglect Emotional neglect Physical neglect Abuse Emotional abuse Physical abuse Sexual abuse Neglect Emotional neglect Physical neglect Abuse Emotional abuse Physical abuse Sexual abuse SHIP-TREND Neglect Emotional neglect Physical neglect Abuse Emotional abuse Physical abuse Sexual abuse Neglect Emotional neglect Physical neglect Abuse Emotional abuse Physical abuse Sexual abuse

Outcome

Effect estimate

p-value

CI

VLMT immediate recall

−1.22 −1.79 −0.07 0.07 −1.83 −0.07 0.16 −0.61 −0.78 −0.15 −0.02 −0.93 −0.15 0.11

5.9E-4 8.0E-7 0.91 0.86 6.4E-3 0.91 0.81 4.7E-4 1.6E-5 0.61 0.94 6.2E-3 0.62 0.75

[-1.92, [-2.50, [-1.16, [-0.78, [-3.14, [-1.17, [-1.12, [-0.95, [-1.14, [-0.73, [-0.45, [-1.59, [-0.74, [-0.56,

-0.52] -1.08] 1.03] 0.93] -0.51] 1.04] 1.44] -0.27] -0.43] 0.43] 0.42] -0.26] 0.44] 0.77]

−0.15 −0.26 −0.19 0.02 0.04 −0.06 0.04 −0.13 −0.24 −0.17 0.10 0.07 −0.003 0.19

4.6E-3 1.9E-4 1.6E-3 0.76 0.70 0.59 0.76 0.084 0.014 0.041 0.31 0.61 0.98 0.25

[-0.26, [-0.39, [-0.31, [-0.13, [-0.18, [-0.26, [-0.20, [-0.28, [-0.44, [-0.33, [-0.10, [-0.21, [-0.29, [-0.13,

0.05] 0.12] -0.07] 0.18] 0.27] 0.15] 0.28] 0.02] -0.05] -0.01] 0.30] 0.35] 0.28] 0.50]

VLMT immediate recall

VLMT delayed recall

VLMT delayed recall

NAI immediate recall

NAI immediate recall

NAI delayed recall

NAI delayed recall

Adjusted for age, sex, education, MDD; results in bold are statistically significant after correction for multiple testing (p < 0.005) in the discovery sample SHIP-LEGEND or nominal significant in the replication sample SHIP-TREND; abuse and neglect are dichotomized variables, a subject was rated as positive for overall abuse/neglect when at least in one of the dimensions a severity score of ≥2 (at least moderate) was reported. Subscales for abuse/neglect are coded none/mild versus moderate/severe.

findings, we found strong associations of all dimensions of childhood maltreatment and particularly emotional neglect with alexithymia (Terock, Van der Auwera, Janowitz, Homuth et al., 2018). Moreover, alexithymia and particularly the EOT factor showed significant negative associations with early and delayed word recall. Both factors, emotional neglect as well as the EOT factor, revealed significant negative associations towards early and delayed word recall in both independent samples. Finally, our data revealed that alexithymia statistically mediated the association between childhood neglect and specifically emotional neglect on declarative memory performance in all analyses but for delayed recall in SHIP-Trend. Our finding of emotional neglect showing strong associations with learning and memory contributes to clarify the currently inconclusive research body on the relation of childhood trauma and adult memory performance (Barzilay et al., 2018; Malarbi et al., 2017). While previous studies identified various factors influencing the association of childhood trauma with adult cognition including the time period of traumatization (Dunn et al., 2016) and whether the child was exposed to familial versus non-familial trauma (for review: (Malarbi et al., 2017)), we found differential associations depending on the type of childhood maltreatment. Identifying emotional neglect as the only subscale significantly associated with adult declarative memory performance is particularly relevant in the light of recent data from a large epidemiologic study showing that emotional neglect is the most prevalent form with rates of 6.2 % in a representative general-population sample from the US (Taillieu, Brownridge, Sareen, & Afifi, 2016). Moreover, it adds to consistent findings showing that emotional neglect is associated with various psychiatric disorders, including MDD (Hamilton et al., 2013), anxiety disorders (Kuo, Goldin, Werner, Heimberg, & Gross, 2011) and different personality disorders (Taillieu et al., 2016) and negatively associated with psychological resilience (Terock, Hannemann et al., 2019, 2019b). These results raise the question which mechanisms could link emotional neglect and poor memory performance. Childhood trauma is a severe and chronic stress factor with alterations of various neuroendocrine systems and particularly altered glucocorticoid, mineralocorticoid and catecholamine levels (Terock, Hannemann et al., 2018; Terock, Hannemann et al., 2019; Wilson, Hansen, & Li, 2011). Brain regions with a central role for the declarative memory functioning like the prefrontal cortex and the hippocampus have also been found to be particularly sensitive to the detrimental effects of stress hormones (Gunnar & Quevedo, 2007). However, in contrast to trauma types like child physical or sexual abuse which are often incident-specific, childhood neglect is typically considered a long-lasting adverse experience in the relationship to their primary caregivers. Moreover, childhood neglect typically begins at very young age and accumulates during infancy, childhood and adolescence. Given that neural connections 6

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Fig. 1. Box-plot of the association between emotional neglect and immediate recall in SHIP-LEGEND and SHIP-Trend.

Table 3 Associations of childhood neglect (and dimensions) with TAS-20 sum score in SHIP-LEGEND and SHIP-TREND. Outcome SHIP-LEGEND TAS-20 score

SHIP-TREND TAS-20 score

Predictor

Coefficient

p-value

95%CI

Neglect Emotional neglect Physical neglect

2.88 3.20 1.93

1.5E-5 5.0E-6 0.066

[1.58, 4.18] [1.82, 4.57] [-0.13, 4.00]

Neglect Emotional neglect Physical neglect

3.21 3.54 3.20

6.0E-17 1.7E-11 2.2E-13

[2.46, 3.97] [2.51, 4.58] [2.35, 4.06]

Adjusted for age, sex, education, MDD; results in bold are statistically significant after correction for multiple testing (p < 0.005) in the discovery sample SHIP-LEGEND or nominal significant in the replication sample SHIP-TREND; abuse and neglect are dichotomized variables, a subject was rated as positive for overall abuse/neglect when at least in one of the dimensions a severity score of ≥2 (at least moderate) was reported. Subscales for abuse/neglect are coded none/mild versus moderate/severe.

continue to develop throughout childhood and adolescence, an enduring lack of appropriate stimulation and interaction may particularly impact on the neurobiological development of the memory capacity (Gunnar & Quevedo, 2007). In a longitudinal study following children being at specific risk for experiencing dysfunctional parenting, those children with psychologically unavailable mothers, which corresponds to emotional neglect, showed more severe decline in their cognitive development as compared to mothers who physically neglected their children (Egeland, 1991). In their review, Hildyard and Wolfe reported that childhood neglect is associated with severe short- and long-term effects on the cognitive, socio-emotional and behavioral development which are unique from the effects of physical abuse (Hildyard & Wolfe, 2002). The authors concluded that enduring adversities like emotional neglect are associated with specifically severe social and emotional deficits. Considering the concept of child neglect as a chronic exposure to multiple and accumulating adversities, our finding is in line with the cumulative risk model which posits that it is cumulative and simultaneous exposure to adversities rather than the impact of a specific risk factor that influences the child’s cognitive and emotional development (Rutter, Pickles, Murray, & Eaves, 2001). However, results from other studies showing a significant influence of multiple specific risk factors like socio-economic status or biological factors on the cognitive development of children indicates that results on the relation of childhood adversities and memory functioning may be confounded by various factors which are highly correlated with the different trauma types (Sylvestre & Mérette, 2010). There is evidence showing that particularly child emotional neglect is linked to dysfunctional or impaired emotion regulation as well as reduced cognitive capacities: For example, Gould et al. investigated patterns of neuropsychological functioning in relation to child maltreatment and found pronounced deficits in emotional processing and processing speed related to child neglect (Gould et al., 7

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Table 4 Results for mediation analyses on the path from childhood neglect to verbal memory over TAS-20 sum score. SHIP-LEGEND immediate recall of words Effect of TAS-20

Mean

95% CI

ACME Direct Effect Total Effect % of TME

−0.164 −1.069 −1.233 13.3

−0.294 −1.722 −1.883 0.087

Effect of TAS-20

Mean

95% CI

ACME Direct Effect Total Effect % of TME

−0.082 −0.538 −0.620 13.2

−0.149 −0.869 −0.948 0.086

Effect of TAS-20

Mean

95% CI

ACME Direct Effect Total Effect % of TME

−0.032 −0.126 −0.158 20.1

−0.050 0.228 −0.258 0.123

−0.069 −0.396 −0.544 0.302

SHIP-LEGEND delayed recall of words

−0.034 −0.197 −0.272 0.301

SHIP-TREND immediate recall of words

−0.017 −0.020 −0.051 0.619

SHIP-TREND delayed recall of words Effect of TAS-20

Mean

95% CI

ACME Direct Effect Total Effect % of TME

−0.012 −0.120 −0.133 9.0

−0.034 −0.261 −0.268 −0.442

0.006 0.025 0.011 0.699

TME: Total Mediated Effect; ACME: Average Causal Mediated Effect; CI: 95 % Confidence interval; TAS-20 = mediator, childhood neglect (dichotomized) = independent variable, recall of words (early or late) = dependent variable, sex, age, education, MDD lifetime = covariables.

2012). Frewen et al. found that emotional neglect was the only dimension of childhood trauma significantly correlated with adult alexithymia (Frewen, Dozois, Neufeld, & Lanius, 2008). These findings mesh well with our result that the association of emotional neglect with memory performance is partly statistically mediated by alexithymia. Finally, childhood trauma as well as alexithymia are associated with dissociation in children (Macfie, Cicchetti, & Toth, 2001) and adults (Terock et al., 2016). Given the concept that dissociation represents a regulatory strategy against negative and intolerable emotions and considering previous findings linking dissociation with different cognitive deficits including reduced memory performance (for review: (Giesbrecht, Lynn, Lilienfeld, & Merckelbach, 2008)), clinical and subclinical dissociation may contribute to impaired storage and recall of information. A mediating effect of alexithymia was observed for both, early and delayed recall in SHIP-LEGENDE and could be replicated for early recall in SHIP-TREND. In contrast, for delayed recall in TREND, associations with childhood neglect were – although significant – considerably weaker and no mediating effect of alexithymia was observed. However, the procedure for this test was substantially different to those in all other tests with passive recognition of words and discrimination from distractors. This result suggests that different cognitive capacities are required for the passive word recognition and more specifically that impaired emotion processing capacities may be of less significance for the passive recognition of words as compared to the free recall of words. Despite evidence for the absolute and relative stability of alexithymia (Honkalampi et al., 2001; Luminet, Bagby, & Taylor, 2001), there has been some debate whether alexithymia can be considered a distinct construct specifically in clinical samples. For example, Badura investigated alexithymia in combat-related PTSD and found strong correlations of alexithymia with the ‘emotional numbing’ aspect of PTSD (Badura, 2003). Marchesi et al. argued that the TAS-20 more likely measures negative affect rather than alexithymia in patients with depression, panic disorder or eating disorder (Marchesi, Ossola, Tonna, & De Panfilis, 2014). However, our results are based on a general population sample with only 1 % of the patients being diagnosed for having PTSD in SHIP-LEGENDE. Moreover, all analyses were adjusted for the lifetime diagnosis of MDD which may at least limit the influence of negative affectivity on alexithymia. Finally, the validity of the self-rating TAS-20 has been called into question as it may be particularly challenging for alexithymic subjects report adequately about their ability to perceive emotions. Our study includes some strengths including the large, independent and well-characterized general-population samples and adjustment for important psychiatric conditions. However, study design and methodology go along with some limitations which need

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to be acknowledged. First, the cross-sectional design of the study prevents from drawing any causal conclusions. For example, particularly older participants with declining memory may have problems to correctly recall traumatic memories from their childhood. Regarding alexithymia, it could also be speculated that impaired declarative memory performance results in difficulties in identifying and describing feelings. However, our findings are consistent with different previous studies on the relation of childhood trauma and declarative memory performance as well as alexithymia on one hand and declarative memory performance on the other hand, suggesting that a path as hypothesized in our model is at least plausible. Also, it is conceivable that the three factors childhood trauma, alexithymia and poor memory performance correlate because of a common cofounder which has not been controlled for in our study like socioeconomic status or social support. However, socioeconomic status is typically highly correlated with the level of education which was included as a covariate in this study. Second, in SHIP-LEGENDE and SHIP-TREND different methods were applied for the assessment of the declarative memory performance. Although the two studies include the same main principle of providing a list of semantically unrelated words which need to be recalled, there are some differences including the number of runs and the specific words themselves, which somewhat reduce the comparability of findings of the two samples. In particular, in SHIPTrend delayed recall was assessed using a considerably different test procedure comprising a passive recognition of words instead of free recall and distractor words which were subtracted from the recall score when recognized falsely. Thus, these specific test differences may have contributed to the inconsistency found in this study. Still, the replication of results in both samples although with different methodologies may also be seen as strength of our study. Third, another limitation is that the sample of the SHIP-study was comprised of Caucasian individuals only. Therefore, it has to remain unclear whether our results can be transferred on other ethnic groups or samples of different cultural background. Fourth, all results were adjusted for age, sex, education, and the lifetime diagnosis of MDD, may other mental and physical health conditions such as traumatic brain injury, mild cognitive impairment or abuse of alcohol or other psychotropic substances have not been included as covariables and may thus have influenced our findings. Although the absolute number of cases with any of these disorders may be small, the total number of conditions affecting the cognitive capacity as well as alexithymia is likely to be large in a general-population sample. This may be particularly important given that childhood trauma is an important predictor of physical and mental disease in adulthood. Also, alexithymia was found to be associated with many physical and mental disorders which may affect memory functioning. Finally, the concept of “secondary alexithymia” posits that organic brain disorders of traumatic brain injury may affect brain regions relevant to the processing and regulation of emotions and may thus lead to alexithymic personality features. In all, it needs to be acknowledged that our findings are based on a general-population study with a large variety of health related factors which have not been controlled for and which may have influenced our results. Finally, our analyses were not adjusted for the intake of medication. Drug intake may particularly influence effects in traumatized participants as these are at specific risk for having a psychiatric disorder as well as the corresponding medication. Although our data are based on a non-clinical sample, intake of medication was common which limits the specificity of our findings Altogether, our study highlights the role of childhood emotional neglect as a severe deleterious factor in the cognitive development. This and our finding of the mediating role of alexithymia further support the concept of emotions and emotional processing abilities as crucial factors for declarative memory functioning. Future studies aiming at investigating neurobiological correlates for the link of childhood trauma and cognition are needed

Financial support SHIP and SHIP-LEGENDE are part of the Community Medicine Research net of the University of Greifswald, Germany, which is funded by the Deutsche Forschungsgemeinschaft (GR 1912/5-1), Federal Ministry of Research and Education (grant no. 01ZZ9603, 01ZZ0103, and 01ZZ0403), BRIDGET Funding (FKZ: 01ED1615), the ministry of cultural affairs as well as the Social Ministry of the Federal State of Mecklenburg-West Pomerania. HJG received research funding from the Deutsche Forschungsgemeinschaft (DFG), the Germany Ministry of Education and Research (BMBF), DAMP Foundation, Fresenius Medical Care, the EU “Joint Program Neurodegenerative Disorders”. SV was funded by the German Federal Ministry of Education and Research (BMBF) within the framework of the e:Med research and funding concept (Integrament; grant no. 01ZX1614E). DJ was funded by the Deutsche Forschungsgemeinschaft (grant no. 257691738).

Ethical statement The investigations were carried out in accordance with the Declaration of Helsinki, including written informed consent of all participants included in the study. The survey and study methods of both the studies were approved by the institutional review boards of the University of Greifswald.

Declaration of Competing Interest HJG received travel grants and speakers honoraria from Fresenius Medical Care and Janssen CILAG. DJ received travel grants from Janssen CILAG. All other authors declare no conflicting interests. 9

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