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Association of maternal prenatal psychological stressors and distress with maternal and early infant faecal bacterial profile

Published online by Cambridge University Press:  20 December 2019

Petrus J.W. Naudé Open the ORCID record for Petrus J.W. Naudé [Opens in a new window] ,
Shantelle Claassen-Weitz ,
Sugnet Gardner-Lubbe ,
Gerrit Botha ,
Mamadou Kaba ,
Heather J. Zar ,
Mark P. Nicol  and
Dan J. Stein
Petrus J.W. Naudé*
Affiliation:
Department of Psychiatry and Mental Health and Neuroscience Institute, Brain Behaviour Unit, University of Cape Town, Cape Town, South Africa
Shantelle Claassen-Weitz
Affiliation:
Division of Medical Microbiology, Department of Pathology, Faculty of Health Sciences, University of Cape Town, Cape Town, South Africa
Sugnet Gardner-Lubbe
Affiliation:
Department of Statistics and Actuarial Science, Stellenbosch University, Stellenbosch, South Africa
Gerrit Botha
Affiliation:
Computational Biology Group and H3ABioNet, Department of Integrative Biomedical Sciences, University of Cape Town, Cape Town, South Africa
Mamadou Kaba
Affiliation:
Division of Medical Microbiology, Department of Pathology, Faculty of Health Sciences, University of Cape Town, Cape Town, South Africa Institute of Infectious Disease and Molecular Medicine, Faculty of Health Sciences, University of Cape Town, Cape Town, South Africa SA-MRC Unit on Child and Adolescent Health, University of Cape Town, Cape Town, South Africa
Heather J. Zar
Affiliation:
SA-MRC Unit on Child and Adolescent Health, University of Cape Town, Cape Town, South Africa Department of Paediatrics and Child Health, Red Cross War Memorial Children’s Hospital, Cape Town, South Africa
Mark P. Nicol
Affiliation:
Division of Medical Microbiology, Department of Pathology, Faculty of Health Sciences, University of Cape Town, Cape Town, South Africa Institute of Infectious Disease and Molecular Medicine, Faculty of Health Sciences, University of Cape Town, Cape Town, South Africa SA-MRC Unit on Child and Adolescent Health, University of Cape Town, Cape Town, South Africa National Health Laboratory Service of South Africa, Groote Schuur Hospital, Cape Town, South Africa Division of Infection and Immunity, School of Biomedical Sciences, The University of Western Australia, Perth, Australia
Dan J. Stein
Affiliation:
Department of Psychiatry and Mental Health and Neuroscience Institute, Brain Behaviour Unit, University of Cape Town, Cape Town, South Africa SU/UCT MRC Unit on Risk and Resilience in Mental Disorders, Department of Psychiatry and Mental Health and Neuroscience Institute, University of Cape Town, Cape Town, South Africa
*
Author for correspondence: Petrus J.W. Naudé, Email: [email protected]
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Abstract

Objective:

Findings from animal studies indicate that the early gut bacteriome is a potential mechanism linking maternal prenatal stress with health trajectories in offspring. However, clinical studies are scarce and the associations of maternal psychological profiles with the early infant faecal bacteriome are unknown. This study aimed to investigate the associations of prenatal stressors and distress with early infant faecal bacterial profiles in a South African birth cohort study.

Methods:

Associations between prenatal symptoms of depression, distress, intimate partner violence (IPV) and posttraumatic stress disorder (PTSD) and faecal bacterial profiles were evaluated in meconium and subsequent stool specimens from 84 mothers and 101 infants at birth, and longitudinally from a subset of 69 and 36 infants at 4–12 and 20–28 weeks of age, respectively, in a South African birth cohort study.

Results:

Infants born to mothers that were exposed to high levels of IPV had significantly higher proportions of Citrobacter and three unclassified genera, all of which belonging to the family Enterobacteriaceae detected at birth. Proportions of these Enterobacteriaceae remained significantly increased over time (birth to 20–28 weeks of life) in infants born to mothers with high levels of IPV exposure compared to infants from mothers with no/low IPV exposure. Infants born to mothers exposed to IPV also had higher proportions of the genus Weissella at 4–12 weeks compared to infants from mothers with no/low IPV exposure. Faecal specimens from mothers exposed to IPV had higher proportions of the family Lactobacillaceae and lower proportions of Peptostreptococcaceae at birth. Maternal psychological distress was associated with decreased proportions of the family Veillonellaceae in infants at 20–28 weeks and a slower decline in Gammaproteobacteria over time. No changes in beta diversity were apparent for maternal or infant faecal bacterial profiles in relation to any of the prenatal measures for psychological adversities.

Conclusion:

Maternal lifetime IPV and antenatal psychological distress are associated with altered bacterial profiles in infant and maternal faecal bacteria. These findings may provide insights in the involvement of the gut bacteria linking maternal psychological adversity and the maturing infant brain.

Keywords

microbiotameconiumdomestic violenceintimate partner violencematernal antenatal stress
Type
Original Article
Information
Acta Neuropsychiatrica , Volume 32 , Issue 1 , February 2020 , pp. 32 - 42
Copyright
© Scandinavian College of Neuropsychopharmacology 2019 

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Footnotes

*

Authors contributed equally to this manuscript.

References

Anders, S and Huber, W (2010) Differential expression analysis for sequence count data. Genome Biology 11, R106–R106.CrossRefGoogle ScholarPubMed
Anderson, MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecology 26, 32–46.Google Scholar
Arboleya, S, Binetti, A, Salazar, N, Fernández, N, Solís, G, Hernández-Barranco, A, Margolles, A, de los Reyes-Gavilán, CG and Gueimonde, M (2012) Establishment and development of intestinal microbiota in preterm neonates. FEMS Microbiology Ecology 79, 763–772.CrossRefGoogle ScholarPubMed
Arrieta, MC, Stiemsma, LT, Amenyogbe, N, Brown, EM and Finlay, B (2014) The intestinal microbiome in early life: health and disease. Frontiers in Immunology 5, 427.CrossRefGoogle ScholarPubMed
Bailey, MT, Lubach, GR and Coe, CL (2004) Prenatal stress alters bacterial colonization of the gut in infant monkeys. Journal of Pediatric Gastroenterology and Nutrition 38, 414–421.CrossRefGoogle ScholarPubMed
Barnett, W, Halligan, S, Heron, J, Fraser, A, Koen, N, Zar, HJ, Donald, KA and Stein, DJ (2018) Maltreatment in childhood and intimate partner violence: a latent class growth analysis in a South African pregnancy cohort. Child Abuse and Neglect 86, 336–348.CrossRefGoogle Scholar
Beck, AT, Steer, RA and Brown, GK (1996) Manual for the Beck Depression Inventory-II . San Antonio: Psychological Corporation.Google Scholar
Beck, AT, Steer, RA and Carbin, MG (1988) Psychometric properties of the Beck Depression Inventory: twenty-five years of evaluation. Clinical Psychology Review 8, 77–100.CrossRefGoogle Scholar
Benjamini, Y and Hochberg, Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society, Series B (Methodology) 57, 289–300.Google Scholar
Bernstein, M, Phillips, T, Zerbe, A, McIntyre, JA, Brittain, K, Petro, G, Abrams, EJ and Myer, L (2016) Intimate partner violence experienced by HIV-infected pregnant women in South Africa: a cross-sectional study. BMJ Open 6, e011999.CrossRefGoogle ScholarPubMed
Bokulich, NA, Chung, J, Battaglia, T, Henderson, N, Jay, M, Li, H, D Lieber, A, Wu, F, Perez-Perez, GI, Chen, Y, Schweizer, W, Zheng, X, Contreras, M, Dominguez-Bello, MG and Blaser, MJ (2016) Antibiotics, birth mode, and diet shape microbiome maturation during early life. Science Translational Medicine 8, 343ra82.CrossRefGoogle ScholarPubMed
Borg, I and Groenen, PJF (2005) Modern Multidimensional Scaling: Theory and Applications. New York: Springer Science & Business Media.Google Scholar
Bray, JR and Curtis, JT (1957) An ordination of the upland forest communities of southern Wisconsin. Ecological Monographs 27, 325–349.CrossRefGoogle Scholar
Carlson, AL, Xia, K, Azcarate-Peril, MA, Goldman, BD, Ahn, M, Styner, MA, Thompson, AL, Geng, X, Gilmore, JH and Knickmeyer, RC (2018) Infant gut microbiome associated with cognitive development. Biol Psychiatry 83, 148–159.CrossRefGoogle ScholarPubMed
Charles, P and Perreira, KM (2007) Intimate partner violence during pregnancy and 1-year post-partum. Journal of Family Violence 22, 609–619.CrossRefGoogle Scholar
Claassen, S, du Toit, E, Kaba, M, Moodley, C, Zar, HJ and Nicol, MP (2013) A comparison of the efficiency of five different commercial DNA extraction kits for extraction of DNA from faecal samples. Journal of Microbiological Methods 94, 103–110.CrossRefGoogle ScholarPubMed
Claassen-Weitz, S, Gardner-Lubbe, S, Nicol, P, Botha, G, Mounaud, S, Shankar, J, Nierman, WC, Mulder, N, Budree, S, Zar, HJ, Nicol, MP and Kaba, M (2018) HIV-exposure, early life feeding practices and delivery mode impacts on faecal bacterial profiles in a South African birth cohort. Scientific Reports 8, 5078.CrossRefGoogle Scholar
Clarke, RK and Warwick, RM ((2001) Change in Marine Communities: An Approach to Statistical Analysis and Interpretation . Plymouth, UK: Primer-E Ltd.Google Scholar
D’Argenio, V (2018) The prenatal microbiome: a new player for human health. High Throughput 7, 38.CrossRefGoogle ScholarPubMed
Drell, T, Štšepetova, J, Simm, J, Rull, K, Aleksejeva, A, Antson, A, Tillmann, V, Metsis, M, Sepp, E, Salumets, A and Mändar, R (2017) The influence of different maternal microbial communities on the development of infant gut and oral microbiota. Scientific reports 7, 9940–9940.CrossRefGoogle ScholarPubMed
Dunkle, KL, Jewkes, RK, Brown, HC, Gray, GE, McIntryre, JA and Harlow, SD (2004) Gender-based violence, relationship power, and risk of HIV infection in women attending antenatal clinics in South Africa. Lancet 363, 1415–1421.CrossRefGoogle ScholarPubMed
Faith, DP, Minchin, PR and Belbin, L (1987) Compositional dissimilarity as a robust measure of ecological distance. Vegetatio 69, 57–68.CrossRefGoogle Scholar
Falsetti, SA, Resnick, HS, Resick, PA and Kilpatrick, D (1993) The modified PTSD symptom scale: a brief self-report measure of posttraumatic stress disorder. The Behavioral Therapist 16, 161–162.Google Scholar
Fernandes, AD, Reid, JNS, Macklaim, JM, McMurrough, TA, Edgell, DR and Gloor, GB (2014) Unifying the analysis of high-throughput sequencing datasets: characterizing RNA-seq, 16S rRNA gene sequencing and selective growth experiments by compositional data analysis. Microbiome 2, 15.CrossRefGoogle ScholarPubMed
Foa, EB and Tolin, DF (2000) Comparison of the PTSD symptom scale–interview version and the clinician-administered PTSD scale. Journal of Traumatic Stress 13, 181–191.CrossRefGoogle ScholarPubMed
Garcia-Rodenas, CL, Bergonzelli, GE, Nutten, S, Schumann, A, Cherbut, C, Turini, M, Ornstein, K, Rochat, F and Corthesy-Theulaz, I (2006) Nutritional approach to restore impaired intestinal barrier function and growth after neonatal stress in rats. Journal of Pediatric Gastroenterology and Nutrition 43, 16–24.CrossRefGoogle ScholarPubMed
Groves, AK, Moodley, D, McNaughton-Reyes, L, Martin, SL, Foshee, V and Maman, S (2015) Prevalence, rates and correlates of intimate partner violence among South African women during pregnancy and the postpartum period. Maternal and Child Health Journal 19, 487–495.CrossRefGoogle ScholarPubMed
Gur, TL, Palkar, AV, Rajasekera, T, Allen, J, Niraula, A, Godbout, J and Bailey, MT (2019) Prenatal stress disrupts social behavior, cortical neurobiology and commensal microbes in adult male offspring. Behavioural Brain Research 359, 886–894.CrossRefGoogle ScholarPubMed
Gur, TL, Shay, L, Palkar, AV, Fisher, S, Varaljay, VA, Dowd, S and Bailey, MT (2017) Prenatal stress affects placental cytokines and neurotrophins, commensal microbes, and anxiety-like behavior in adult female offspring. Brain, Behavior, and Immunity 64, 50–58.CrossRefGoogle ScholarPubMed
Harding, TW, de Arango, MV, Baltazar, J, Climent, CE, Ibrahim, HH, Ladrido-Ignacio, L, Murthy, RS and Wig, NN (1980) Mental disorders in primary health care: a study of their frequency and diagnosis in four developing countries. Psychological Medicine 10, 231–241.CrossRefGoogle ScholarPubMed
Hartley, M, Tomlinson, M, Greco, E, Comulada, WS, Stewart, J, le Roux, I, Mbewu, N and Rotheram-Borus, MJ (2011) Depressed mood in pregnancy: prevalence and correlates in two Cape Town peri-urban settlements. Reproductive Health 8, 9.CrossRefGoogle ScholarPubMed
Hu, J, Ly, J, Zhang, W, Huang, Y, Glover, V, Peter, I, Hurd, YL and Nomura, Y (2019) Microbiota of newborn meconium is associated with maternal anxiety experienced during pregnancy. Developmental Psychobiology 61, 640–649.CrossRefGoogle ScholarPubMed
Jansen, HAFM, Watts, C, Ellsberg, M, Heise, L and García-Moreno, C (2004) Interviewer training in the WHO multi-country study on women’s health and domestic violence. Violence Against Women 10, 831–849.CrossRefGoogle Scholar
Jašarević, E, Rodgers, AB and Bale, TL (2015) A novel role for maternal stress and microbial transmission in early life programming and neurodevelopment. Neurobiology of Stress 1, 81–88.CrossRefGoogle ScholarPubMed
Jewkes, R (2002) Intimate partner violence: causes and prevention. Lancet 359, 1423–1429.CrossRefGoogle Scholar
Jiang, H, Ling, Z, Zhang, Y, Mao, H, Ma, Z, Yin, Y, Wang, W, Tang, W, Tan, Z, Shi, J, Li, L and Ruan, B (2015) Altered fecal microbiota composition in patients with major depressive disorder. Brain, Behavior, and Immunity 48, 186–194.CrossRefGoogle ScholarPubMed
Kane, AV, Dinh, DM and Ward, HD (2015) Childhood malnutrition and the intestinal microbiome. Pediatric Research 77, 256–262.CrossRefGoogle ScholarPubMed
Kang, D-W, Park, JG, Ilhan, ZE, Wallstrom, G, LaBaer, J, Adams, JB and Krajmalnik-Brown, R (2013) Reduced incidence of prevotella and other fermenters in intestinal microflora of autistic children. PLoS One 8, e68322.CrossRefGoogle ScholarPubMed
Koen, N, Brittain, K, Donald, KA, Barnett, W, Koopowitz, S, Maré, K, Zar, HJ and Stein, DJ (2016) Psychological trauma and posttraumatic stress disorder: risk factors and associations with birth outcomes in the Drakenstein Child Health Study. European Journal of Psychotraumatology 7, doi:10.3402/ejpt.v7.28720.CrossRefGoogle Scholar
Koleff, P, Gaston, KJ and Lennon, JJ (2003) Measuring beta diversity for presence–absence data. Journal of Animal Ecology 72, 367–382.CrossRefGoogle Scholar
Laursen, MF, Andersen, LBB, Michaelsen, KF, Mølgaard, C, Trolle, E, Bahl, MI and Licht, TR (2016) Infant Gut microbiota development is driven by transition to family foods independent of maternal obesity. mSphere 1, e00069–15.CrossRefGoogle ScholarPubMed
Mari, JJ and Williams, P (1986) A validity study of a psychiatric screening questionnaire (SRQ-20) in primary care in the city of Sao Paulo. The British Journal of Psychiatry 148, 23–26.CrossRefGoogle ScholarPubMed
McGowan, TC and Kagee, A (2013) Exposure to traumatic events and symptoms of post-traumatic stress among South African university students. South African Journal of Psychology 43, 327–339.CrossRefGoogle Scholar
McMurdie, PJ and Holmes, S (2014) Waste not, want not: why rarefying microbiome data is inadmissible. PLOS Computational Biology 10, e1003531.CrossRefGoogle Scholar
Misch, ES and Yount, KM (2014) Intimate partner violence and breastfeeding in Africa. Maternal and Child Health Journal 18, 688–697.CrossRefGoogle ScholarPubMed
Morgan, XC and Huttenhower, C (2012) Chapter 12: Human microbiome analysis. PLoS Computer Biology 8, e1002808.CrossRefGoogle ScholarPubMed
O’Mahony, SM, Clarke, G, Dinan, TG and Cryan, JF (2017) Early-life adversity and brain development: is the microbiome a missing piece of the puzzle? Neuroscience 342, 37–54.CrossRefGoogle ScholarPubMed
Oksanen, J, Blanchet, FG, Kindt, R, Legendre, P, Minchin, PR, O’hara, R, Simpson, GL, Solymos, P, Stevens, MHH and Wagner, H (2013) Package ‘vegan’. Community Ecology Package, version 2.Google Scholar
Pannaraj, PS, Li, F, Cerini, C, Bender, JM, Yang, S, Rollie, A, Adisetiyo, H, Zabih, S, Lincez, PJ, Bittinger, K, Bailey, A, Bushman, FD, Sleasman, JW and Aldrovandi, GM (2017) Association between breast milk bacterial communities and establishment and development of the infant gut microbiome. JAMA Pediatrics 171, 647–654.CrossRefGoogle ScholarPubMed
Pusceddu, MM, El Aidy, S, Crispie, F, O’Sullivan, O, Cotter, P, Stanton, C, Kelly, P, Cryan, JF and Dinan, TG (2015) N-3 Polyunsaturated Fatty Acids (PUFAs) reverse the impact of early-life stress on the gut microbiota. PLoS One 10, e0139721.CrossRefGoogle ScholarPubMed
R_Development_Core_Team (2014) R Foundation for Statistical Computing. R: A language and environment for statistical computing.Google Scholar
Rico, E, Fenn, B, Abramsky, T and Watts, C (2011) Associations between maternal experiences of intimate partner violence and child nutrition and mortality: findings from Demographic and Health Surveys in Egypt, Honduras, Kenya, Malawi and Rwanda. Journal of Epidemiology and Community Health 65, 360–367.CrossRefGoogle ScholarPubMed
Rochat, TJ, Richter, LM, Doll, HA, Buthelezi, NP, Tomkins, A and Stein, A (2006) Depression among pregnant rural South African women undergoing HIV testing. JAMA 295, 1376–1378.CrossRefGoogle ScholarPubMed
Rumble, S, Swartz, L, Parry, C and Zwarenstein, M (1996) Prevalence of psychiatric morbidity in the adult population of a rural South African village. Psychological Medicine 26, 997–1007.CrossRefGoogle ScholarPubMed
Seferovic, MD, Belfort, B, Major, A, Chu, D, Racusin, D, Castro, E, Carroll, M, Stewart, C, Versalovic, J and Aagaard, K (2018) 695: visualization of intact placental microbes in both term and preterm births. American Journal of Obstetrics and Gynecology 218, S417–S418.CrossRefGoogle Scholar
Shamu, S, Abrahams, N, Temmerman, M, Musekiwa, A and Zarowsky, C (2011) A systematic review of African studies on intimate partner violence against pregnant women: prevalence and risk factors. PLoS One 6, e17591.CrossRefGoogle ScholarPubMed
Shannon, CE (1948) A mathematical theory of communication. Bell System Technical Journal 27, 379–423.CrossRefGoogle Scholar
Sordillo, JE, Korrick, S, Laranjo, N, Carey, V, Weinstock, GM, Gold, DR, O’Connor, G, Sandel, M, Bacharier, LB, Beigelman, A, Zeiger, R, Litonjua, AA and Weiss, ST (2019) Association of the infant gut microbiome with early childhood neurodevelopmental outcomes: an ancillary study to the VDAART randomized clinical trial. JAMA Network Open 2, e190905.CrossRefGoogle ScholarPubMed
Stein, A, Pearson, RM, Goodman, SH, Rapa, E, Rahman, A, McCallum, M, Howard, LM and Pariante, CM (2014) Effects of perinatal mental disorders on the fetus and child. The Lancet 384, 1800–1819.CrossRefGoogle Scholar
Stein, DJ, Koen, N, Donald, KA, Adnams, CM, Koopowitz, S, Lund, C, Marais, A, Myers, B, Roos, A, Sorsdahl, K, Stern, M, Tomlinson, M, van der Westhuizen, C, Vythilingum, B, Myer, L, Barnett, W, Brittain, K and Zar, HJ (2015) Investigating the psychosocial determinants of child health in Africa: the Drakenstein Child Health Study. Journal of Neuroscience Methods 252, 27–35.CrossRefGoogle ScholarPubMed
Stein, DJ, Williams, DR and Kessler, RC (2009) The South African Stress and Health (SASH) study: a scientific base for mental health policy. South African Medical Journal 99, 337.Google ScholarPubMed
Stinson, LF, Boyce, MC, Payne, MS and Keelan, JA (2019) The not-so-sterile womb: evidence that the human fetus is exposed to bacteria prior to birth. Frontiers in Microbiology 10, 1124.CrossRefGoogle Scholar
Sudo, N, Chida, Y, Aiba, Y, Sonoda, J, Oyama, N, Yu, X-N, Kubo, C and Koga, Y (2004) Postnatal microbial colonization programs the hypothalamic-pituitary-adrenal system for stress response in mice. The Journal of physiology 558, 263–275.CrossRefGoogle ScholarPubMed
Thompson, RS, Bonomi, AE, Anderson, M, Reid, RJ, Dimer, JA, Carrell, D and Rivara, FP (2006) Intimate partner violence: prevalence, types, and chronicity in adult women. American Journal of Preventive Medicine 30, 447–457.CrossRefGoogle ScholarPubMed
Valles-Colomer, M, Falony, G, Darzi, Y, Tigchelaar, EF, Wang, J, Tito, RY, Schiweck, C, Kurilshikov, A, Joossens, M, Wijmenga, C, Claes, S, Van Oudenhove, L, Zhernakova, A, Vieira-Silva, S and Raes, J (2019) The neuroactive potential of the human gut microbiota in quality of life and depression. Nature Microbiology 4, 623–632.CrossRefGoogle ScholarPubMed
van Heyningen, T, Honikman, S, Myer, L, Onah, MN, Field, S and Tomlinson, M (2017) Prevalence and predictors of anxiety disorders amongst low-income pregnant women in urban South Africa: a cross-sectional study. Archives of Women’s Mental Health 20, 765–775.CrossRefGoogle ScholarPubMed
Vythilingum, B, Roos, A, Faure, SC, Geerts, L and Stein, DJ (2012) Risk factors for substance use in pregnant women in South Africa. South African Medical Journal 102, 851–854.CrossRefGoogle ScholarPubMed
Willyard, C (2018) Could baby’s first bacteria take root before birth? Nature 553, 264–266.CrossRefGoogle ScholarPubMed
World Heatlh Organization (WHO) (2002) Handbook for Good Clinical Research Practice (GCP) - Guidance for Implementation. Available at http://apps.who.int/prequal/info_general/documents/GCP/gcp1.pdf (accessed December 2013).Google Scholar
Zar, HJ, Barnett, W, Myer, L, Stein, DJ and Nicol, MP (2015) Investigating the early-life determinants of illness in Africa: the Drakenstein Child Health Study. Thorax 70, 592–594.CrossRefGoogle ScholarPubMed
Zeitlin, D, Dhanjal, T and Colmsee, M (1999) Maternal-foetal bonding: the impact of domestic violence on the bonding process between a mother and child. Archives of Women’s Mental Health 2, 183–189.CrossRefGoogle Scholar
Zijlmans, MAC, Korpela, K, Riksen-Walraven, JM, de Vos, WM and de Weerth, C (2015) Maternal prenatal stress is associated with the infant intestinal microbiota. Psychoneuroendocrinology 53, 233–245.CrossRefGoogle ScholarPubMed
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