Pediatric Urology 180 PEDIATRIC UROLOGY The Differences Between Preterm and Term Birth Affecting Initiation and Completion of Toilet Training Among Children: A Retrospective Case-Control Study Dilek Yildiz1, Derya Suluhan1*,Berna Eren Fidanci1,Merve Mert1, Turan Tunç2, Bülent Altunkaynak3 Purpose: This study seeks to investigate the possibility the existence of a difference in terms of start and end dates of toilet training between term and preterm children as well as the possible determining factors. Materials and Methods: This study was conducted as a 5-year retrospective case (children born preterm-(32 to <37 weeks) – and control (children born at term (>37 weeks + 1 day)) study. The data were collected with a form consisted of questions about demographic data (12 questions) and toilet traning features (10 questions) through face-to-face interviews with the mothers. A chi-square test and logistic regression analysis were conducted to ex- amine the data. Odds ratio was used as a measure of the relation between levels of the dependent variable. Results: The study examined a total of 133 children including 59 preterm children and 74 children born at term including 60 (45.1%) boys and 73 (54.9%) girls. The possibility of starting toilet training at or before 24 months was found to be 6.4 times greater in full-term children than preterm children (OR = 6.493). The logistic regression analysis, which aimed at identifying any variables that might affect end date of toilet training, found that despite the tendency to consider preterm birth as a factor prolonging the duration of toilet training, the difference was not found to be statistically significant (P = .07). Conclusion: This study compared full-term and preterm children in terms of start and end dates of toilet training and found that preterm children start toilet training later than full-term children. Based on the results of the study, it is possible to say that preterm birth, gender and birth order affect start date of toilet training. However there is no difference between term and preterm babies on the end date of toilet training. Keywords: toilet training; preterm birth; parents INTRODUCTION While toilet training is a challenging experience for parents, it constitutes one of the most sig- nificant developmental tasks of childhood.(1-3) Smooth accomplishment of this task is critically important for both the child and the parents. A multitude of factors influences—either by enabling or obstructing—the start and achievement of the child’s toilet training. Parent-re- lated factors include educational attainment, family so- ciocultural structure, income level, living environment, type of toilet, methods used, and parents’ knowledge/ experience of the subject, while factors such as age, gender, physical and mental readiness, gestational age at birth, and birth weight are cited among the child-re- lated factors.(3-7) A review of the existing literature shows that very few studies have looked into the effect of gestation- al age on start and completion of toilet training.(8-9) In Drillien’s study on the growth and development of prematurely-born infants, the researcher reported on child-rearing practices and bladder control develop- 1 Department of Pediatric Nursing, Gülhane Faculty of Nursing, Saglik Bilimleri University, Ankara, 06010, Turkey. 2 Department of Pediatrics, Memorial Ataşehir Hospital, Istanbul, 34758, Turkey. 3 Department of Department of Statistics, Gazi University, Faculty of Science, Ankara, 06500, Turkey. *Correspondence: Department of Pediatric Nursing, Gülhane Faculty of Nursing, Saglik Bilimleri University, Ankara, 06010, Turkey. Tel: +90 506 3311738, Fax: +90 312 3043907, E-mail: derya.suluhan@sbu.edu.tr. Received October 2018 & Accepted March 2019 ment.(9) Toilet-training, and the age at which children became reliably dry both day and night, was related to prematurity, impairment, socioeconomic conditions, and sex. Small, prematurely-born children acquired sphincter control later than full-term-born children. The researcher also pointed out that girls were more ad- vanced in gaining bladder control than boys. Largo et al. reported that developing bladder and bowel control is not affected by prematurity, adverse perinatal events, or mild-to-moderate neurological impairment, nor is it related to psychomotor development or socioeconomic conditions.(8) This study seeks to answer the following questions: 1) Do preterm children and full-term children differ with respect to the start date of toilet training? ; 2) Do pre- term children and full-term children differ with respect to the end date of toilet training? METHODS Setting This study was conducted as a 5-year retrospective case study with a control group, examining preterm children Vol 16 No 02 March-April 2019 181 and full-term children in a Training and Research Hos- pital in Turkey from March 1, 2015, through January 1, 2016. Subjects The data used in the study pertained to children admit- ted as inpatients to the Neonatal Intensive Care Unit due to preterm birth during the one-year period be- tween January 2010 and January 2011; these data were reviewed retrospectively, and the contact information of the patients was accessed. The cases were selected according to gestastional age. Preterm birth is defined as “babies born alive before 37 weeks of pregnancy are completed”. Sub-categories of preterm birth are based on weeks of gestational age: Extremely preterm (<28 weeks), Very preterm (28 to <32 weeks), and Moderate to late preterm (32 to <37 weeks).(10) The case group consisted of moderate to late preterm babies, and the control group consisted of full-term babies (>37 weeks + 1 day). The case group consisted of 59 preterm chil- dren in the then-current age group of 4-6 years with no neurological, genetic, or metabolic diseases that impacted their cognitive and motor development. Ex- tremely preterm and very preterm babies were excluded due to common prematurity complications. The control group comprised 74 children born full-term between January 2010 and January 2011 who were hospitalized for a different reason. The control group was selected after matching for age and gender with the case group. In both groups, the children were evaluated by a doc- tor with a voiding dysfunction symptom score. Chil- dren with voiding dysfunction were not included in the study. The files of children in the control group were reviewed, and their contact information was accessed. Data collection The contact information obtained in the file review was used to invite parents in the case and control groups to the hospital to fill out data collection forms. These forms were filled out in 10-15 minutes through face- to-face interviews with the mothers. The data collec- tion forms were developed by the researcher through a review of the literature.(1,3,5,11-14) The form consisted of a total of 22 questions, including 12 questions about so- ciodemographic data (the parent’s age, the child’s age and gender, the parent’s educational attainment and em- ployment status, the number of children, and the family structure) and 10 questions on toilet training (child’s age when toilet training started, duration of training, training methods used by parents, and any problems encountered). Data analysis SPSS v22 (Statistical Package for Social Sciences) was employed to analyze the data obtained in the study. A chi-square test and a logistic regression analysis were conducted to examine the data. Numbers and percent- ages were used for interpretation in chi-square tables. Odds ratio was used to measure the relation between levels of the dependent variable. Throughout the analy- ses, P < 0.01 and P < 0.05 values were considered sta- tistically significant. The dependent variables were ‘‘start date of toilet train- ing’’ and ‘‘duration of toilet training’’. The independ- ent variables were the child’s gender, birth order, the mother’s educational attainment, her perception of in- come level, and family type. Though there is no specific age at which toilet training should begin, it is advised Table 1. Comparison of start date of toilet training in preterm (n=59) and full-term (n=74) children by sociodemographic characteristics Start date of toilet training Characteristics Before 24 months After 24 months Child’ characteristics Gender Number (n) Percent (%) Number (n) Percent(%) χ2 p Girl Preterm (n=35) 12 34.3 23 65.7 9.90 Full-term (n=38) 27 71.1 11 28.9 < .001b Boy Preterm (n=24) 2 8.3 22 91.7 8.94 Full-term (n=36) 16 44.4 20 55.6 < .001b Birth order χ2 p First-born Preterm (n=28) 11 39.3 17 60.7 5.47 Full-term (n=43) 29 67.4 14 32.6 0.02a Later born Preterm (n=31) 3 9.7 28 90.3 9.81 Full-term (n=31) 14 45.2 17 54.8 < .001b Mother’s characteristics χ2 Educational attainment p 11 years or less Preterm (n=34) 6 17.6 28 82.4 15.37 Full-term (n=53) 32 60.4 21 39.6 < .001b More than 11 years Preterm (n=25) 8 32.0 17 68.0 1.96 Full-term (n=21) 11 52.4 10 47.6 0.16 Family’s income level χ2 p Less income than Preterm (n=19) 8 42.1 11 57.9 3.08 expenses Full-term (n=20) 14 70.0 6 30.0 .08 Balanced income Preterm (n=40) 6 15.0 34 85.0 14.73 and expenses or more < .001b Full-term (n=54) 29 53.7 25 46.3 χ2 p Family type Nuclear family Preterm (n=50) 10 20.0 40 80.0 17.16 < .001b Full-term (n=69) 40 58.0 29 42.0 Other Preterm (n=9) 4 44.4 5 55.6 - Full-term (n=5) 3 60.0 2 40.0 *ap < .05; b p< .001 The differences between preterm and term birth about toilet training -Yildiz et al. Pediatric Urology 182 for parents to start at 18-24 months in healthy children. (15,16) ‘‘Start date of toilet training’’ was defined as ş 24 months and > 24 months, allowing the variable to be discrete and thus enabling logistic regression. Ethical Considerations Permission from Hospital’s Board of Ethics and written consent from the participating mothers were obtained (1491-678-10/1539). RESULTS The study examined a total of 133 children, 59 preterm children and 74 full-term children, including 60 (45.1%) boys and 73 (54.9%) girls. The median age was 4.3±0.8 years. All parents consist of mothers whose median age was 35.08±5.63 years. In terms of mother’s educational attainment, duration of education was ≤11 years for 75 (56.4%) mothers and >11 years for 58 (43.6%) moth- ers. 119 children (89.5%) lived in a nuclear family, 9 (6.8%) lived in an extended family, and 5 (3.8%) lived in a single-parent family. 39 mothers (29.3%) had lower income than their expenses, 88 (66.2%) mothers had as much income as their expenses, and 6 (4.5%) had more income than their expenses. Table 1 compares toilet training start date in preterm and full-term children by sociodemographic character- istics. In both genders, start of training at ≤ 24 months was found to be significantly higher for children born full-term (P < 0.001 and P < 0.001) than children born preterm. In terms of birth order, the number of first- born full-term children who started toilet training at ≤ 24 months was significantly higher than that of non- first-born children. The share of children who started training >24 months was found to be significantly high- er in the preterm group regardless of birth order (P = 0.02 and P < 0.001). The number of full-term children of mothers with an educational attainment of ş11 years who started toilet training at ≤ 24 months was found to be significantly higher (P < 0.001) than those of preterm children of similarly-educated mothers; this difference was not found for full-term children with mothers with an edu- cational attainment of >11 years (P = 0.16). In terms of family income level, in families with income-expense balance or a higher income, the number of children who start toilet training ≥ 24 months was found to be signif- icantly higher (P < 0.001) in the preterm group than the full-term group; this difference did not exist in families with lower income (P = 0.08). Rates of late start dates were found to be higher in preterm children living in nuclear families (P < 0.001) (Table 1). A comparison of toilet training completion by demo- Completion of toilet training Characteristics 2-30 days Longer than 30 days Child’ characteristics Gender Number (n) Percent (%) Number (n) Percent (%) χ2 p Girl Preterm 21 60.0 14 40.0 .40 .53 Full-term 20 52.6 18 47.4 Boy Preterm 17 70.8 7 29.2 4.05 .04a Full-term 16 44.4 20 55.6 Birth order χ2 p First-bornPreterm 18 64.3 10 35.7 3.41 .07 Full-term 18 41.9 25 58.1 Later born Preterm 20 64.5 11 35.5 .27 .60 Full-term 18 58.1 13 41.9 Mother’s characteristics χ2 Educational attainment p 11 years or less Preterm 23 67.6 11 32.4 3.51 .06 Full-term 25 47.2 28 52.8 More than 11 years Preterm 15 60.0 10 40.0 .27 .60 Full-term 11 52.4 10 47.6 Family’s income level χ2 p Less income than Preterm 9 47.4 10 52.6 .23 expenses .63 Full-term 11 55.0 9 45.0 Balanced income and Preterm 29 72.5 11 27.5 6.45 expenses or more .01a Full-term 25 46.3 29 53.7 Family type χ2 p Nuclear family Preterm 33 66.0 17 34.0 3.30 .07 Full-term 34 49.3 35 50.7 Other Preterm 5 55.6 4 44.4 - Full-term 2 40.0 3 60.0 a p < 0.05 Table 2. Comparison of completion times of toilet training in preterm (n=59) and full-term (n=74) children by sociodemographic char- acteristics The differences between preterm and term birth about toilet training -Yildiz et al. Vol 16 No 02 March-April 2019 183 graphic characteristics of children and mothers shows that the rates of toilet training lasting >30 days were significantly higher with preterm children in families with income-expense balance or with a higher income (P = .01) and in boys (P = 0.04) (Table 2). A logistic regression analysis was conducted to identify any variables that might affect toilet training start date. Preterm birth, gender, and birth order were found to be statistically significant. The possibility of starting toilet training at ≤ 24 months was found to be 6.493 times greater with full-term children than with preterm chil- dren (OR=1/0.154=6.493). The ratio was found to be 4 times higher in girls than boys (OR=4.009). Similarly, the share of start dates ≤ 24 months was found to be 3.8 times higher in first-born children than in children with a birth order of 2 or later (OR=3.886) (Table 3). The logistic regression analysis also aimed to identify any variables that might affect toilet training end date; it found that, despite the tendency to consider preterm birth as a factor prolonging toilet training duration, the difference was not found to be statistically significant (P = 0.07). Other variables were not found to have a statistically significant effect on duration (Table 4). DISCUSSION This study seeks to investigate a possible difference in toilet training start and end dates between full-term and preterm children, as well as potential determining fac- tors. Preterm birth, gender, birth order, socio-economic status, family structure, and the mother’s educational attainment were found to be correlated with the start date of toilet training. A logistic regression analysis was carried out to identify the factors that had an actual effect. The analysis showed that preterm birth, gender, and birth order are the only determining factors and that all three variables delay the start date of toilet training. Drillien et al. showed that preterm birth and gender are factors that influence toilet training.(9) It is worth noting that rates of start dates >24 months is high in both gen- ders in the preterm group. Regardless of birth order, late start was observed in the preterm group. Also, despite family socio-economic status and the child being a boy correlating with duration of toilet training, such a link was not validated by the logistic regression analysis. However, literature has shown that low socioeconomic status has an effect on toilet training.(17) Toilet training start date varies from one society to an- other. While it was common in the 1940s to start toilet training before 18 months in the US and Europe, recent studies show start dates as late as 21-36 months.(14) The American Academy of Pediatrics and the Canadian Pae- diatric Society recommend a child-centered toilet train- ing approach, which starts at 18-24 months.(10,17) Moth- ers with a lower socio-economic status are known to have a higher risk of preterm birth.(8) This could be one factor that might influence delayed toilet training. Lar- go et al. showed that preterm children start toilet train- ing earlier (<18 months) than full-term children and that they are subject to more frequent training. The same study reports that start date and intensity of the training are not related to socioeconomic status. The study also maintains that gestation week at birth does not affect bladder and bowel control.(8) Similarly, this study did not find a correlation between socioeconomic status and toilet training start date. However, as opposed to other studies, our study found that preterm children start toilet training later than full-term children. The reason could be mothers’ belief that a preterm birth will result in de- layed acquisition of the skill. While one of the factors influencing toilet training start date is gender, earlier bladder and bowel control among girls is known to be linked with maturation. Addition- ally, a number of studies have found that both full-term and preterm girls start toilet training at a younger age than boys.(2,7,8,12,15-17) One study reports that preterm girls (both SGA (small for gestational age) and AGA (appropriate for gestational age)) start toilet training at a younger age than boys, predominantly between 12- 18 months. The same study reports that gender has no impact on start date of toilet training at ≥24 months.(8) It should be noted that as in Largo’s study, our study found that preterm children start toilet training >24 months regardless of gender. These findings are in line with the results of other studies found in the literature, and one reason could be faster maturational develop- ment in girls. (7,19-20) The current study also investigated the possibility of birth order being a determining factor affecting toilet training start date. No relevant data was found in the lit- erature. The study found that being the second child or Table 3. Result of last step of backward logistic regression analysis for determining the variables that affect on the time to start toilet training B S.E. df Sig. Unadjusted OR (95% CI) Adjusted OR (95% CI) Birth -1.871 .458 1 .000 .224 (.105 to .478) .154 (.063 to .378) Gender 1.389 .449 1 .002 2.676 (.1305 to 5.491) 4.009 (1.663 to 9.665) Birth Order 1.357 .431 1 .002 3.416 (1.648 to 7.080) 3.886 (1.670 to 9.046) Family Type .806 .458 1 .078 2.182 (1.022 to 4.658) 2.239 (.913 to 5.492) Constant -2.039 1.204 1 .090 .130 Note: Binary Dependent variable is “the time to start toilet training” (Before 24 months; After 24 months). Note: Binary Dependent variable is “the completion of toilet training” (2-30 days; Longer than 30 days). B S.E. df Sig. Unadjusted OR (95% CI) Adjusted OR (95% CI) Birth .647 .358 1 .071 1.910 (.947 to 3.851) 1.910 (.947 to 3.851) Constant 1 .240 .591 1 .036 Table4. Result of last step of backward logistic regression analysis for determining the variables that affect on the completion of toilet training The differences between preterm and term birth about toilet training -Yildiz et al. Pediatric Urology 184 later delayed the toilet training start date (>24 months) in the preterm group. The reason could be mothers’ belief that preterm birth may delay acquisition of toi- let skills, despite their experience in child care. In the full-term group, first-born children started toilet train- ing earlier, whereas later children did not show such a difference. The reason could be the family’s desire to start toilet training at a later age for later-born siblings, either due to difficulties encountered with their first- born child or due to parents’ level of experience. Horn et al. compared toilet training start date by car- egivers’ educational attainment and showed that full- term children of parents with lower levels of educational attainment start toilet training earlier.(17,21) In our study, mothers with lower levels of educational attainment were also found to delay toilet training for their preterm children. However, no correlation was found between educational attainment and the timing of toilet training. The reason could be that timing of toilet training varies in different societies, or that mothers believe a preterm birth might delay acquisition of toilet skills and it would not be good to force their child to achieve this develop- mental task too early. However, a comparison of toilet training end dates shows that, despite a relatively short- er toilet training duration in preterm children in families with lower levels of educational attainment, the differ- ence was not found to be statistically significant. The reason could be that later start dates result in shorter durations, due to maturation. Family socio-economic status may be another deter- mining factor affecting toilet training start date. Koc et al. reported in their study that parents with a higher socioeconomic status start toilet training at a later age. (22) In another study that compared full-term and pre- term children, socioeconomic status was not found to impact toilet training start date in preterm children.(21) Our study did not find any correlation between soci- oeconomic status and the timing of toilet training, in accordance with the existing literature. One of the limitations of this study was the use of retro- spective data. This might have affected the participants’ recollections of some of the details of their experience in toilet training their child. Another limitation is that toilet training methods were not taken into account. Toilet training methods are one of the important fac- tors that affects duration of toilet training, but it was not evaluated in our study. This study is the first study to examine the relationship between family type and toilet training. It can be argued that family structure does not have an impact on start and end dates of toilet training in preterm children. CONCLUSIONS This study compared full-term and preterm children in terms of start and end dates of toilet training, and it found that preterm children start toilet training lat- er than full-term children. Based on the results of the study, it can be said that preterm birth, gender, and birth order affect the toilet training start date. Although one may argue that being born preterm creates a tendency to shorten the duration of toilet training, no statistically significant relation was identified. More extensive re- search on larger groups of patients is needed to obtain reliable data on the subject. We recommend to parents or caregivers of children born preterm that gestational age at birth does not affect the occurrence of the child's initiative nor the development of bladder and bowel control. ACKNOWLEDGEMENT We would like to thank the registered nurses, Merve Demirhan for her help with collected data. CONFLICT ON INTEREST The authors declared no potential conflicts of interest with respect to the research, authorship, and/or publica- tion of this article. REFERENCES 1. Van Aggelpoel T, De Wachter S, Van Hal G, Van der Cruyssen K, Neels H, Vermandel A. Parents' views on toilet training: a cross- sectional study in Flanders. Nurs Child Young People. 2018 ;30:30-35. 2. Brazelton TB, Christophersen ER, Frauman AC, et al. Instruction, timeliness, and medical influences affecting toilet training. Pediatrics. 1999;103 (Supplement 3):1353-8. 3. Mota DM, Barros AJ. Toilet training: methods, parental expectations and associated dysfunctions. J Pediatr (Rio J). 2008;84:9-17. 4. Vermandel A, Van Kampen M, Van Gorp C, Wyndaele JJ. How to Toilet Train Healthy Children? A Review of the Literature. Neurourol Urodyn. 2008;27:162-6. 5. Bakker E, Van Gool J, Van Sprundel M, Van Der Auwera C, Wyndaele J. Results of a questionnaire evaluating the effects of different methods of toilet training on achieving bladder control. BJU Int. 2002;90:456-61. 6. Klassen TP, Kiddoo D, Lang ME, et al. The effectiveness of different methods of toilet training for bowel and bladder control. Evid Rep Technol Assess (Full Rep). 2006 ;(147):1- 57. 7. Schum TR, McAuliffe TL, Simms MD, Walter JA, Lewis M, Pupp R. Factors associated with toilet training in the 1990s. Ambul Pediatr. 1999;158:115-22. 8. Largo R, Molinari L, Von Siebenthal K, Wolfensberger U. Development of bladder and bowel control: significance of prematurity, perinatal risk factors, psychomotor development and gender. Eur J Pediatr. 1999;158:115-22. 9. Drillien CM. A longitudinal study of the growth and development of prematurely and maturely born children. Arch Dis Child. 1961;36:515-25. 10. Toilet Training Guidelines: parents—the role of the parents in toilet training. Pediatrics. 1999 ;103(6 Pt 2):1362-1363. 11. Clifford T, Gorodzinsky F. Toilet learning: anticipatory guidance with a child-oriented approach. Paediatr Child Health. 2000;5:333- 44. The differences between preterm and term birth about toilet training -Yildiz et al. Vol 16 No 02 March-April 2019 185 12. Stadtler AC, Gorski PA, Brazelton TB. Toilet training methods, clinical interventions, and recommendations. Pediatrics. 1999;103 (Supplement 3):1359-61. 13. Blum NJ, Taubman B, Nemeth N. Relationship between age at initiation of toilet training and duration of training: a prospective study. Pediatrics. 2003;111:810-4. 14. Gorodzinsky F. Toilet learning: Anticipatory guidance with a child-oriented approach. Paediatr Child Health. 2000 ;5:333-44. 15. Kaerts N, Vermandel A, Van Hal G, Wyndaele JJ. Toilet training in healthy children: results of a questionnaire study involving parents who make use of day-care at least once a week. Neurourol Urodyn. 2014;33:316-23. 16. Joinson C, Heron J, Von Gontard A, Butler U, Emond A, Golding J. A prospective study of age at initiation of toilet training and subsequent daytime bladder control in school-age children. J Dev Behav Pediatr. 2009;30:385-93. 17. Horn IB, Brenner R, Rao M, Cheng TL. Beliefs about the appropriate age for initiating toilet training: are there racial and socioeconomic differences? J Pediatr. 2006 ;149:165-8. 18. Koc I, Camurdan A, Beyazova U, Ilhan M, Sahin F. Toilet training in Turkey: the factors that affect timing and duration in different sociocultural groups. Child Care Health Dev. 2008 ;34:475-81. 19. Bloom DA, Seeley WW, Ritchey ML, McGuire E. Toilet habits and continence in children: an opportunity sampling in search of normal parameters. J Urol. 1993 ;149:1087- 90. 20. Taubman B. Toilet training and toileting refusal for stool only: a prospective study. Pediatrics. 1997;99:54-8. The differences between preterm and term birth about toilet training -Yildiz et al.