Accepted Manuscript Trunk forward flexion mobility in reference to postural sway in women after delivery: A prospective longitudinal comparison between early pregnancy and 2- and 6-month postpartum followups
Agnieszka Opala-Berdzik, Janusz W. Błaszczyk, Dariusz Świder, Joanna Cieślińska-Świder PII: DOI: Reference:
S0268-0033(18)30044-5 doi:10.1016/j.clinbiomech.2018.05.009 JCLB 4536
To appear in:
Clinical Biomechanics
Received date: Accepted date:
18 January 2018 18 May 2018
Please cite this article as: Agnieszka Opala-Berdzik, Janusz W. Błaszczyk, Dariusz Świder, Joanna Cieślińska-Świder , Trunk forward flexion mobility in reference to postural sway in women after delivery: A prospective longitudinal comparison between early pregnancy and 2- and 6-month postpartum follow-ups. The address for the corresponding author was captured as affiliation for all authors. Please check if appropriate. Jclb(2017), doi:10.1016/ j.clinbiomech.2018.05.009
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ACCEPTED MANUSCRIPT Trunk forward flexion mobility in reference to postural sway in women after delivery: A prospective longitudinal comparison between early pregnancy and 2- and 6-month postpartum follow-ups Agnieszka Opala-Berdzik a,*, Janusz W. Błaszczyk
b,c
, Dariusz Świder d, Joanna Cieślińska-
Świder e
Department of Physiotherapy in Internal Diseases, Academy of Physical Education,
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a
Katowice, Poland
Department of Human Motor Behavior, Academy of Physical Education, Katowice, Poland
c
Nencki Institute of Experimental Biology, Polish Academy of Sciences, Warsaw, Poland
d
Institute of Computer Science, Silesian University of Technology, Gliwice, Poland
e
Department of Physiotherapy of the Nervous and Locomotor Systems, Academy of Physical
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b
Education, Katowice, Poland
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Corresponding author at: Academy of Physical Education in Katowice, Mikołowska 72, 40-
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065 Katowice, Poland. E-mail address:
[email protected] (A. Opala-Berdzik)
Highlights
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Total trunk forward flexion mobility was increased up to 6 months postpartum. Increased connective tissue laxity may persist for 6 months after pregnancy.
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Postpartum women may benefit from pelvis-spine complex stability exercises.
Author Contribution
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AOB, JWB, JCŚ: Conceived and designed the experiments. AOB: Performed the experiments. AOB, JWB, DŚ: Analyzed the data. AOB: Interpreted the data and wrote the paper. JWB, JCŚ: Critically revised the article. AOB, JWB, DŚ, JCŚ: Approved the final version to be submitted.
Declarations of interest: none
Word count: Abstract: 225, Main Text: 3180
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ACCEPTED MANUSCRIPT ABSTRACT Background: It has been documented that pregnancy-related increased connective tissue laxity may persist postpartum; however, it is still unclear for how long. This longitudinal study aimed to compare total trunk forward flexion mobility in women between their first trimester of pregnancy and at 2- and 6-month postpartum follow-ups. We also searched for a correlation between women’s trunk flexibility and their postural stability in the sagittal plane. Methods: Seventeen healthy women participated in the study. Data were collected at their 7-
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12 weeks gestation appointments and at 6-10 and 25-28 weeks postpartum. At each session, the women performed a finger floor distance test, and data were collected on their waist
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circumference and BMI. The women’s center of foot pressure mean velocity in the anterior-
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posterior direction was computed from 30-s long quiet-standing trials on a stationary force plate.
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Findings: Total trunk forward flexion mobility was significantly higher at 2 and 6 months postpartum compared to that in early pregnancy (P < 0.05). At 6 months postpartum, a moderate negative correlation between finger floor distance test values and their anterior-
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posterior center of foot pressure mean velocity was observed (r = -0.6, P < 0.05). Interpretation: Increased total trunk flexibility may be present in women 6 months
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postpartum. During that period, women with higher trunk flexibility may be more likely to
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present higher anterior-posterior postural sway velocity in quiet standing.
Keywords:
Trunk mobility
Pregnancy Postpartum
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Postural sway
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Trunk flexion
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ACCEPTED MANUSCRIPT 1. Introduction A pregnant woman’s body undergoes biomechanical changes that become apparent in her posture, gait and activities of daily living (Błaszczyk et al., 2016; Gilleard et al., 2008; Gilleard, 2013; Yousef et al., 2011). One of the visible changes caused by the enlarging uterus is a restriction in trunk forward flexion mobility (Cheng et al., 2006; Dumas et al., 1998). A decreasing trend in a range of trunk forward flexion with the progression of pregnancy has been documented (Gilleard et al., 2002). Concomitantly, there is little and contrary evidence
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regarding trunk flexibility in women after delivery, and this evidence is based on studies with sample size of only five and nine participants (Dumas et al., 1998; Gilleard et al., 2002). One
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of the studies demonstrated that the thoracolumbar spine range of forward flexion in women
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at 8 weeks postpartum was similar to that of a control group (Gilleard et al., 2002). Another study, however, suggested increased values for the lumbar spine range of flexion in women at
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16 weeks postpartum in comparison to their pre-pregnancy values. This post-pregnancy increase in lumbar spine flexibility was explained as a possible effect from the persisting pregnancy-related increase in connective tissue laxity after delivery (Dumas et al., 1998).
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An increase in joint mobility during pregnancy was reported in regards to the knee, hand and pelvic joints (Calguneri et al., 1982; Dumas and Reid, 1997; Lindgren and
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Kristiansson, 2014; Marnach et al., 2003; Mens et al., 2009; Schauberger et al., 1996). This phenomenon may be related to an elevated level of maternal serum relaxin and/or estradiol
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(Bjӧrklund et al., 2000; Charlton et al., 2001; Schauberger et al., 1996; Vøllestad et al., 2012). Because relaxin changes collagen architecture, it may influence connective tissue structures which contain the collagenous fibers (Samuel et al., 1998). In pregnancy, the increase in joint
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laxity was observed by as early as the second trimester (Lindgren and Kristiansson, 2014; Marnach et al., 2003). However, the available literature does not provide a clear answer
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regarding the length of time in which the increased joint laxity should resolve after pregnancy. Although some studies indicated recovery in the first few weeks postpartum (Calguneri et al., 1982; Charlton et al., 2001; Dumas and Reid, 1997), according to other studies, the increased joint laxity may still be present several weeks after delivery (Lindgren and Kristiansson, 2014; Marnach et al., 2003; Schauberger et al., 1996). Because excessive joint laxity may pose an increased risk of joint injury or dysfunction (Myer et al., 2008; Philippon and Schenker, 2005; Shultz et al., 2004; Wolf et al., 2011), it is very important to learn how long the increased joint mobility may persist after pregnancy. A method commonly used to assess total trunk forward flexion mobility is a finger floor distance (FFD) test. This test is a composite motion of the hips, lumbar and thoracic 3
ACCEPTED MANUSCRIPT spine, and shoulders (Carregaro et al., 2007; Kippers and Parker, 1987; Tully and Stillman, 1997). A hip flexion component depends to a great extent on the extensibility of a hamstring muscle group composed of the semitendinosus, semimembranosus and biceps femoris muscles (Kippers and Parker, 1987). This large muscular mass also plays an important role in anterior-posterior pelvic tilt and indirectly controls lumbar lordosis (López‐Miñarro et al., 2012; Muyor et al., 2011). The FFD method has been widely used in the clinical assessment of patients with low back pain (Demoulin et al., 2013; Filho, at al., 2014; Rao et al., 2012;
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Vroomen et al., 2002) and as a reflection of self-reported disability in activities of daily living (Ekedahl et al., 2012; Michel et al., 1997). The test has also been used in the assessment of
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healthy subjects (Carregaro et al., 2007; Kippers and Parker, 1987; Magnusson et al., 1997),
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and it has shown excellent intra- and intertester reliability, validity and responsiveness (Frost et al., 1982; Gauvin et al., 1990; Omata et al., 2010; Perret et al., 2001). To our knowledge,
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the assessment of total trunk flexibility by the FFD method in pregnant/postpartum women has not been previously documented.
Joint mobility is one of the factors that influence postural control (Martínez-López et
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al., 2014; Siqueira et al., 2011). There is evidence suggesting a decline of postural stability in pregnancy and at 6-8 weeks postpartum (Butler et al., 2006, Jang et al., 2008) and a high
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incidence of falls during the perinatal period (Dunning, 2010; Lockwood and Anderson, 2013). We are unaware of any study investigating the relationship between trunk flexibility
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and postural control in women during and after pregnancy. Because total trunk forward flexion occurs in the sagittal plane it would be particularly interesting to search for its relation with the anterior-posterior postural sway. Static postural stability can be assessed by
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analyzing a subject’s quiet standing postural sway. Postural sway is a constant horizontal movement of the body’s center of gravity caused by its internal and external perturbations. An
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evaluation of quiet standing postural sway can be performed with the use of force plate posturography. This method records spontaneous center of foot pressure (CoP) movements reflecting the center of gravity excursions and the ground reaction forces due to muscular activity (Winter, 1995). The primary aim of this study was to compare FFD in women between their first trimester of pregnancy and at 2- and 6-month postpartum follow-ups. We hypothesized that the FFD would indicate increased trunk flexibility at 2 months after delivery compared to that at early pregnancy. At 6 months postpartum, we expected the values of the FFD to be similar to those of early pregnancy values. Our secondary aim was to verify the influence of the evaluation period on women’s waist circumference, BMI and anterior-posterior postural sway 4
ACCEPTED MANUSCRIPT mean velocity. We also aimed to determine whether the FFD was associated with anteriorposterior postural sway in each of the three evaluation periods.
2. Methods
This study was conducted following the approval of the Senate Ethics Committee of the Katowice Academy of Physical Education, Poland.
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The present study is part of our longitudinal study of postural stability in women during and after pregnancy, in which forty-five healthy pregnant women were initially
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enrolled (Opala-Berdzik et al., 2015). The women were recruited for the study by
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obstetricians from antenatal clinics in the region of Upper Silesia, Poland. For the purpose of this study, seventeen women in their first trimester of unifetal pregnancies (13 primigravida
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and 4 multigravida) were included. Exclusion criteria were any conditions considered by an obstetrician to indicate a high-risk pregnancy, as well as any disabilities that affect trunk mobility or postural stability, including musculoskeletal (e.g., spinal, hip, or knee
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pain/pathology) and neurologic abnormalities, uncorrectable vision disorders, obesity, or diabetes mellitus. Subjects were also excluded if they had previous delivery within one year
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before enrollment and were under treatment with any medication that would affect balance. Eligibility criteria were confirmed by physical examination and a medical interview.
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Women enrolled in the study reported for testing at the Biomechanics Laboratory at the Department of Human Motor Behavior at the Academy of Physical Education in Katowice. The aim of the study and the experimental procedures were explained to all
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subjects, and written informed consent was obtained. The women were tested on the following three occasions: in the first trimester of
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pregnancy (up to 12 weeks gestation) and at 2 and 6 months postpartum. Because no significant differences were observed in the hip and lumbar range of flexion between prepregnancy and 12-week gestation periods (Dumas et al., 1998), the data acquired in the first trimester were treated as a reference for the two postpartum periods. A nulliparous control group was not included in the experiment because of high variability of total trunk flexibility which is mainly caused by inter-individual differences in anthropometric characteristics and hamstring muscle extensibility (Gleim & McHugh, 1997; Magnusson et al., 1997). In a small sample of healthy subjects, the reliability of a between-group comparison of FFD values might be low.
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ACCEPTED MANUSCRIPT At the beginning of the study, the mean (SD) age of the women was 28.6 (4.4) years (range 20 - 38 years). The characteristics of the subjects at the three data collection sessions are presented in Table 1.
Table 1. Characteristics of 17 women during the first trimester of pregnancy (P) and at 2 (PP1) and 6 (PP2) months postpartum.*
weeks
kg
10.8 (1.6)
59.6 (8.2)
Body height
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Body mass
cm
166.8 (4.2)
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P
Gestation
Postpartum
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weeks 8.3 (1.5)
62.4 (8.9)
PP2
26.8 (1.0)
60.7 (8.9)
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PP1
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* Data are shown as the means and standard deviations (denoted in parentheses).
At the beginning of each session, the women were interviewed about any medication
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intake and musculoskeletal complaints. The subject height was recorded at the initial visit and
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body mass was measured at each visit to calculate BMI. Waist circumference measurement (midway between the highest point of the iliac crest and the bottom of the ribcage), FFD and posturographic tests were performed at each session. The measurements were repeated at the
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same time of day by the same licensed physical therapist. For the FFD test, each woman was asked to stand barefoot by the edge of a 35-cm-
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high platform with her feet hip-width apart. She was then instructed to bend forward as far as possible in an attempt to reach for the ground with her fingers while keeping her knees extended. The distance between the third fingertip of the right hand and the top of the platform was measured with a standard tape measure (Gauvin et al., 1990). A zero distance was assumed if the woman reached the top of the platform. The distance above the platform was considered as positive and that below the platform as negative. For the posturographic test, the woman was instructed to be barefoot and stand quietly with her arms at her sides and at a comfortable, stance on a stable force platform (model 9281C, Kistler Instruments Corp, Winterthur, Switzerland), looking straight ahead at a wall 3 m away. Recording started 10 s after the woman assumed the quiet standing position on the 6
ACCEPTED MANUSCRIPT force plate. The test was performed according to the manufacturer’s operating instructions. Two 30-s trials were recorded and were separated by short (up to 1 min) rest breaks to avoid any discomfort. The CoP trajectories were sampled at 100 samples/s and were digitally filtered with a 12th order low-pass Chebychev type II filter at a 7-Hz cut-off frequency (Jang et al., 2008). A CoP mean velocity was used to characterize the postural sway. This measure is considered very reliable and particularly valuable in clinical practice (Lafond et al., 2004; Pinsault and
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Vuillerme, 2009; Ruhe et al., 2010; Słomka et al., 2013). For the purpose of this study the CoP anterior-posterior mean velocity was calculated using Matlab (Mathworks©, Natick, MA
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USA) on the basis of the means of two trials (Lafond et al., 2004).
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Friedman repeated measures analysis of variance by ranks was performed to determine the effects of the three sessions (first trimester of pregnancy, 2 and 6 months postpartum) on
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FFD, waist circumference, BMI and CoP anterior-posterior mean velocity. When the results of the Friedman ANOVA were significant, a Wilcoxon signed-rank test was applied to compare the measures from the particular sessions. A Spearman’s Rank Correlation
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Coefficient test was used to determine whether the pregnant/postpartum subjects’ FFD correlated with their CoP anterior-posterior mean velocity, BMI and waist circumference. The
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(StatSoft Inc., Tulsa, OK USA).
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level of significance was set at P < 0.05. Analyses were performed using Statistica 9.0
3. Results
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A Friedman ANOVA showed a significant effect of the test session on FFD (P = 0.006). The FFD significantly decreased from a positive value at the first trimester of
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pregnancy to an approximately zero value at 2 months postpartum (P = 0.04). From 2 to 6 months postpartum, the FFD further decreased to a negative value (P = 0.01). A highly significant decrease of the FFD was noted from the first trimester of pregnancy to 6 months postpartum (P = 0.002; Table 2). The Friedman ANOVA showed a significant effect of the test session on waist circumference (P = 0.02). The circumference of the waist significantly increased from early pregnancy to 2 months postpartum (P = 0.001), and decreased from 2 to 6 months after delivery (P = 0.02). It was not significantly different between early pregnancy and 6 months postpartum (P = 0.13; Table 2).
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ACCEPTED MANUSCRIPT The Friedman ANOVA showed a non-significant effect of the evaluation period on women’s BMI (P = 0.06) and on the CoP anterior-posterior mean velocity recorded during 30-s of quiet standing (P = 0.94; Table 2).
Table 2. Finger floor distance (FFD), waist circumference (girth), body mass index (BMI) and center of pressure (CoP) anterior-posterior (AP) mean velocity (recorded in 30-s quiet
months postpartum. PP1
FFD (cm)*
3.5 (12.0)
0.2 (12.9)
Waist girth (cm)**
74.5 (6.3)
BMI
21.4 (2.4)
CoP AP velocity (mm/s)
4.7 (1.0)
PP2 -2.4 (11.2)
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P
78.3 (6.8)
76.3 (6.8)
22.4 (2.8)
21.8 (2.7)
4.8 (0.8)
4.8 (1.0)
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Measure
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standing) in 17 women in the first trimester of pregnancy (P) and at 2 (PP1) and 6 (PP2)
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Data are shown as the means and standard deviations (denoted in parentheses). * Significantly decreased from P to PP1 (P = 0.04), from PP1 to PP2 (P = 0.01), and from P
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to PP2 (P = 0.002; Wilcoxon signed-rank tests; Friedman ANOVA: P = 0.006); lower values
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of FFD = higher total trunk flexion mobility. ** Significantly increased from P to PP1 (P = 0.001), and decreased from PP1 to PP2 (P = 0.02; Wilcoxon signed-rank tests; Friedman ANOVA: P = 0.02).
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The FFD did not correlate with the CoP anterior-posterior mean velocity in the first trimester of pregnancy or at 2 months postpartum (P > 0.05); however, at 6 months after
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delivery the FFD was moderately negatively correlated with the CoP anterior-posterior mean velocity (r = -0.6, P < 0.05; Figure 1). The FFD did not correlate with BMI or waist circumference either in early pregnancy or postpartum (P > 0.05).
Insert Figure 1 here
Figure 1. Spearman correlation of a finger floor distance (FFD) test with the center of pressure (CoP) anterior-posterior (AP) mean velocity during 30-s quiet standing in 17 women in their early pregnancy and at 2 and 6 months postpartum.
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ACCEPTED MANUSCRIPT 4. Discussion
The primary objective of this study was to compare total trunk forward flexion mobility (based on the outcome of the FFD test) in women between their first trimester of pregnancy and at 2- and 6-month postpartum follow-ups. We assumed that the women would demonstrate increased trunk flexibility at 2 months postpartum compared to that in early pregnancy. We also expected that at 6 months postpartum, the flexibility of the trunk would
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be similar to that in early pregnancy. Our study confirmed that at 2 months after delivery, women’s total trunk forward flexion mobility was increased in comparison to that at 11 weeks
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of pregnancy. Surprisingly, at 6 months postpartum, the total trunk flexibility was further
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increased.
In our study, we assumed that in the first trimester, total trunk forward flexion
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mobility was similar to its flexion mobility before pregnancy, because a pregnancy-related increase in joint laxity was observed by as early as the second trimester (Lindgren and Kristiansson, 2014; Marnach et al., 2003). We treated the first trimester FFD values as a
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reference to the postpartum values based on the study by Dumas et al. (1998). The authors had a unique possibility to evaluate trunk and hip flexibility longitudinally in five women
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before, during and after pregnancy. Their study indicated no significant differences in the hip and lumbar range of flexion between pre-pregnancy and the 12-week gestation period.
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Our findings of increased total trunk forward flexion mobility in women at 2 and 6 months postpartum compared to that at the 11th week of pregnancy suggest that pregnancyrelated increase in connective tissue laxity may persist throughout half a year after delivery.
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Interestingly, in our study, the women were even more flexible at 6 months than at 2 months postpartum. We suppose that at 2 months postpartum, some restriction in the total trunk
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forward flexion could have been caused by post-pregnancy back muscle tightness. During advanced pregnancy the thoracolumbar spine range of forward flexion is severely restricted by the notably enlarged uterus (Gilleard et al., 2002), therefore, in the first few weeks postpartum, the extensibility of the back muscles may still be decreased. Our findings concerning postpartum trunk flexibility are in accordance to those obtained by Dumas et al. (1998). As in our study, the authors evaluated women twice after pregnancy, however, in slightly different evaluation periods. They reported no significant increase in the values for the lumbar spine range of flexion in women at 6 weeks postpartum and a significant increase of the values at 4 months postpartum compared to pre-pregnancy values. In turn, Gilleard et
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ACCEPTED MANUSCRIPT al. (2002) compared the thoracolumbar spine range of forward flexion between women at 8 weeks postpartum and a control group indicating non-significant between-group differences. In regard to the mobility of other joints in postpartum women, Marnach et al. (2003) reported that increased wrist range of motion in pregnancy did not resolve by 6 weeks postpartum. A similar observation was made by Schauberger et al. (1996) concerning knee laxity. Lindgren and Kristiansson (2014) tested the finger joint range of motion throughout pregnancy and until the 13th week postpartum. They indicated that the increased mobility of
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that peripheral joint was still present at 3 months after delivery. According to Robinson et al. (2014), the prevalence of pelvic girdle pain (related to increased sacroiliac joint laxity)
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remained unchanged from 12 weeks to 1 year after delivery in 30% of postpartum women.
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In our study, we also aimed to determine possible relationship between pregnant/postpartum women’s FFD values and their anterior-posterior postural sway. The
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results indicate that in women at 6 months postpartum there was a moderate association between their total trunk forward flexion mobility and their anterior-posterior postural sway velocity. These findings suggest that at 6 months postpartum the women with higher trunk
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flexibility were more likely to sway faster in the anterior-posterior direction during quiet standing. It is possible that proprioceptive signals sent from looser ligaments and/or tendons
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to the central nervous system “trigger” different response of the muscles responsible for controlling joint stability (Shultz et al., 2004). According to the reverse pendulum model,
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mainly ankle plantar/dorsiflexor co-activation is related to the control of the anterior-posterior quiet standing postural sway (Vieira et al., 2012; Winter, 1995). However, around the neutral standing posture an antagonistic trunk flexor-extensor muscle co-activation may also be
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present (Cholewicki et al., 1997). When assuming that the increased connective tissue laxity is a cause of the higher total trunk flexibility in the postpartum women, our results appear to
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be in agreement with the study by Siqueira et al. (2011). The authors indicated higher postural sway velocity in women with knee hyperextension compared to that in women with normal knee alignment.
Interestingly, our study indicates no correlation of the FFD with the velocity of the anterior-posterior postural sway in early pregnancy and at 2 months postpartum. This suggests that no association between these two factors was present when the women had unchanged total trunk forward flexion mobility at the beginning of pregnancy or when some increase in the women’s total trunk flexibility was observed at 2 months postpartum (in that evaluation period two possible pregnancy-related factors influenced FFD: increased connective tissue
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ACCEPTED MANUSCRIPT laxity might have led to the increased trunk flexibility; however, back muscle tightness might have restricted full range of total trunk flexion).
5. Conclusions
In conclusion, persistence of the increased total trunk flexion mobility in women at 2 and 6 months postpartum may be an effect of pregnancy-related hormonal changes on the
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connective tissue laxity. Postpartum women with higher total trunk flexibility may be more likely to demonstrate increased anterior-posterior postural sway velocity. This may suggest
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that in these women, different proprioception and kinesthetic feedback from the looser
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connective tissue structures may result in altered postural control. Because of relatively small sample size of our study the results and conclusions should be considered with caution.
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Further studies on larger populations of pregnant/postpartum women are needed to investigate possible maintenance of the increased joint mobility within one year after pregnancy. Based on our findings, we suggest that postpartum women, at least up to 6 months after delivery,
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should follow exercise recommendations similar to those for pregnant women in regard to avoiding excessive stretching predisposing to their joint hypermobility. The role of exercises
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Acknowledgements
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increasing pelvis-spine complex stability in postpartum women may be enhanced.
This study is a part of the study of postural stability assessment in women during and after
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pregnancy which was funded by a Polish Ministry of Science and Higher Education grant 2 P05D 05227. We gratefully acknowledge Professor Andrzej Markiewicz for contributing to
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the general conception of the study and Doctor Grzegorz Sobota for calculating the CoP anterior-posterior mean velocity in Matlab. We also thank the Academy of Physical Education in Katowice for funding the editorial assistance.
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Figure 1