Pelvic floor and abdominal muscle cocontraction in women with and without pelvic floor dysfunction: a systematic review and meta-analysis

There is an ongoing discussion regarding abdominal muscle (AbM) and pelvic floor muscle (PFM) synergism. Therefore, this study aimed to investigate the cocontraction between AbMs and PFMs in women with or without pelvic floor dysfunction (PFD). The following databases were searched up to December 21, 2018: MEDLINE, EMBASE, LILACS, PEDro and CENTRAL. We included any study that assessed the cocontraction between PFMs and AbMs in women with and without PFD. Two reviewers independently screened eligible articles and extracted data. The outcomes were extracted and analyzed as continuous variables with random effect models. Twenty studies were included. A meta-analysis did not show differences in women with and without PFD. However, a sensitivity analysis suggested cocontraction of the transversus abdominis (TrA) during PFM contraction in healthy women (standardized mean difference (SMD) –1.02 [95% confidence interval (CI) −1.90 to −0.14], P=0.02; I2= not applicable; very low quality of evidence). Women with PFD during contraction of PFMs showed cocontraction of the obliquus internus (OI) (SMD 1.10 [95% CI 0.27 to 1.94], P=0.01; I2= not applicable; very low quality of evidence), and obliquus externus (OE) (SMD 2.08 [95% CI 1.10 to 3.06], P<0.0001; I2 = not applicable; very low quality of evidence). Increased cocontraction of the TrA may be associated with maximal contraction of PFMs in women without PFD. On the other hand, there is likely an increased cocontraction with the OI and OE in women with PFD.


' INTRODUCTION
Pelvic floor dysfunction (PFD) refers to a group of disturbances in the pelvic floor muscles (PFM) or connective tissues usually associated with pelvic organ prolapse, urinary and/or anal incontinence, sexual dysfunction, and pelvic pain (1). Treatment-related costs are estimated to correspond to an annual expenditure of 12 billion dollars and are projected to increase every year (2), with a considerable prevalence according to the population and definition used (3). The estimated prevalence is reported to be 25% to 46% in high-income (4), low-income and middle-income countries (5). PFD is a common disease that affects women at all ages, exerting a severe impact on their lives and consuming considerable healthcare resources (4).
Researchers have reported strategies, such as the use of a model of abdominal muscle (AbM) training to stimulate tonic PFM activity (6). This scientific evidence is based on the idea of synergistic cocontraction of the PFMs and AbMs, which occurs during normal activities (7,8). Although there is an established literature highlighting that PFM and AbM interaction is usually present in asymptomatic women (9), clinical practice guidelines for conservative management of PFD (10,11) have demonstrated that the AbMs remain a neglected aspect of care. The addition of AbM training might improve clinical outcomes for patients with PFD (12) and restore normal PFM function. The lack of establishment of coactivation between PFMs and AbMs in women with PFD might reflect the lack of robust evidence that exercise regimens other than PFM training would potentially add benefits to conservative management of PFD (13).
The understanding of cocontraction among AbMs and PFMs could be valuable for alternative strategies of PFM exercises to promote continence. In this systematic review, we investigate the coactivity of AbMstransversus abdominis (TrA), rectus abdominis (RA), obliquus internus (OI), and obliquus externus (OE)and PFMs in women with or without PFD. We hypothesized that women with PFD would show decreased coactivity of the AbMs or PFMs during maximal voluntary contraction (MVC) of the PFMs or AbMs, respectively, compared to women with no history of PFD.

' MATERIALS AND METHODS
This review adhered to the Preferred Reporting Items for Systematic Reviews and Meta-analyses -PRISMA (14) and Meta-analysis of Observational Studies in Epidemiology -MOOSE (15) guidelines and was registered on PROSPERO (CRD42017055462).

Eligibility criteria
Study design: any observational study (cohort, crosssectional, comparative cross-sectional) or any baseline subset of data provided by randomized controlled trials, to avoid interaction effects due to any applied interventions. Studies that aimed to assess the reliability of scoring systems for the investigation of cocontraction of the muscles under investigation in this review, as well as studies that provided information on our predefined outcomes, were also included; Participants: women with or without PFD, with urinary incontinence (UI), pelvic organ prolapse (POP), and pelvic pain; Interventions: any voluntary contraction of PFMs that recorded the cocontraction of AbMs (TrA, RA, OI, and OE) and vice versa; Outcomes: J The cocontraction of AbMs (TrA, RA, OI, and OE) and PFMs was measured by surface electromyography (EMG), ultrasonography (US), a digital palpation scale, or a perineometer; We also considered any indirect assessment of the muscle contraction.
We excluded full-text peer-review studies that evaluated AbMs and PFMs in resting activity.

Selection of studies
Two reviewers (GV and LARR) independently screened all titles and abstracts identified by the literature search, obtained full-text articles of all potentially relevant records, and evaluated them. Disagreements were resolved through discussion or by consulting a third person (RED).

Data extraction
Data from included studies were summarized in a standardized data extraction with participant demographics, inclusion and exclusion criteria, cocontraction measurement methods, muscles studied and outcomes. Two reviewers (GV and LARR) extracted the sample size, means and standard deviations (SD). When SD data were unavailable, we estimated the SD using the standard error according to the recommendations of the Cochrane Handbook (16).
If data regarding methods or results were incomplete, we attempted to contact the authors for further information. Moreover, when we found figures without data, we used the WebPlotDigitizer s (v. 3.8) for Windows to extract an estimation of the data from the figures.

Risk of bias assessment
The risk of bias with a modified version of the Ottawa-Newcastle instrument was independently assessed by the reviewers (17). This tool includes confidence in the assessment of exposure and outcome and an adjusted analysis for differences between groups in prognostic characteristics and missing data (17). When information regarding risk of bias or other aspects of methods or results was unavailable, we attempted to contact the study authors for additional information.

Certainty of evidence
The Grading of Recommendations Assessment, Development and Evaluation (GRADE) system was used to rate the certainty of the evidence for each outcome measure as high, moderate, low, or very low (18). Detailed GRADE guidance was performed according to the following criteria: imprecision (19), inconsistency (20), and indirectness (21). The results are summarized in a table of evidence profile.

Data synthesis and statistical analysis
We analyzed the outcomes as continuous variables with random effect models on the results from the muscles investigated (TrA, RA, OI, and OE). Since the assessment of cocontraction in the included studies was measured in different ways (e.g., US and EMG), the individual scales were aligned to point in the same direction, and we calculated the standardized mean difference (SMD) along with the respective confidence interval (CI) of 95%, using the extracted means and SDs (16). Positive SMD values indicated higher cocontraction of the evaluated muscle in the PFD group compared to the asymptomatic group, and a negative SMD indicated higher cocontraction of the evaluated muscle in the asymptomatic group compared to the PFD group.
We also conducted sensitivity analyses to test the robustness of these results. When data were obtained from RCTs and the results were provided separately by intervention and control groups, we calculated the baseline mean and SD based on the mean and SD from the studies. Furthermore, when studies provided both the left and right sides of the AbMs, we also calculated the mean and SD based on the mean and SD provided for both sides.

Outcomes
Meta-analysis of TrA muscle cocontraction when the PFMs contract. The results from two studies (24,36) with a total of 52 participants assessing cocontraction by US failed to show a difference in the cocontraction of the TrA in women with and without PFD (SMD À 0.61 [95% CI À 1.41 to 0.20],      p=0.14; I 2 = 41%) ( Figure 3). However, a plausible sensitivity analysis, excluding the study of Arab et al. (24), yielded results that were inconsistent with the primary analysis, showing higher coactivity of the TrA during MVC of the PFMs in women without PFD (SMD À 1.02 [95% CI À 1.90 to À 0.14], p=0.02; I 2 = not applicable) ( Figure 4). Certainty evidence was rated down to low because of serious limitations on the high risk of bias, indirectness due to the evaluation of only one PFD (UI) ( Figure 3) and different ages, as well as imprecision (Table 4).
Meta-analysis of RA muscle cocontraction when the PFMs contract. The results from three studies (31,34,38) with a total of 128 participants were unable to demonstrate a difference in the cocontraction of the RA between women with a normal pelvic floor and women with PFD (UI) (SMD À 2.05 [95% CI À 6.51 to 2.42], P=0.37; I 2 = 98%) ( Figure 3). Furthermore, the sensitivity analysis, excluding the Madill et al. study (31), showed results that were inconsistent with the primary analysis, with higher cocontraction of the RA during MVC of the PFMs in women with PFD, however, with no statistical significance (SMD 0.89 [95% CI -0.03 to 1.82], P=0.06; I 2 = 63%) (Figure 4).
Certainty of evidence was rated down to very low because of serious limitations on the high risk of bias, inconsistency due to high heterogeneity (Figure 3), indirectness due to evaluation of only one PFD (UI), different assessments of UI and different ages, and imprecision (Table 4).
Meta-analysis of OI abdominis muscle cocontraction when the PFMs contract. The results from three studies (24,31,38) with a total of 118 participants showed no difference between women with a normal pelvic floor and women with PFD (UI) (SMD À 0.47 [95% CI À 2.38 to 1.44], I 2 = 95%; P=0.63) ( Figure 3). However, a plausible sensitivity analysis, excluding the studies of Madill et al. (31) and Arab et al. (24), presented results that were inconsistent with the primary analysis, showing a higher mean of cocontraction in women with PFD (UI) than in women with a normal pelvic floor (SMD 1.10 [95% CI 0.27 to 1.94], P=0.01; I 2 = not applicable) (Figure 4).
Certainty of evidence was rated down to very low because of serious limitations on inconsistency due to high risk of bias, high heterogeneity (Figure 3), indirectness due to the evaluation of only one PFD (UI), different assessments of UI and different ages, and imprecision (Table 4).
Meta-analysis of OE abdominis muscle cocontraction when the PFMs contract. The results from two studies (31,38) with a total of 98 participants failed to show a difference between women with a normal pelvic floor and women with PFD (SMD 0.01 [95% CI À 4.00 to 4.03], P=1.00; I 2 = 98%) (Figure 3). However, a plausible sensitivity analysis, excluding the study of Madill et al. (31), demonstrated results that were inconsistent with the primary analysis, showing a higher mean of cocontraction in women with PFD (UI) than in women with a normal pelvic floor (SMD 2.08 [95% CI 1.10 to 3.06], Po0.0001; I 2 = not applicable) ( Figure 4).
Certainty of evidence was rated down to very low because of serious limitations on inconsistency due to high heterogeneity (Figure 3), indirectness due to high risk of bias, evaluation of only one PFD (UI), different assessments of UI and different ages, and imprecision (Table 4).

Main findings
This systematic review that investigated the cocontraction of AbMs and PFMs in women with or without PFD identified 20 studies. Therefore, it might provide evidence of synergism between PFMs and the TrA, RA, OI and OE, i.e., the cocontraction of PFMs and AbMs occurs during both voluntary contraction of the pelvic floor and abdominal muscle contractions. The studies showed a cocontraction of AbMs during the contraction of PFMs in women with no history of symptoms of PFD, with PFD, or both. Metaanalysis of data from five cross-sectional studies assessed the synergism of the TrA, RA, OI, and OE during MVC of PFMs. As the primary meta-analysis failed to show any difference between women with and without PFD, we performed a sensitivity analysis to minimize the heterogeneity of data. Our sensitivity analysis showed a different cocontraction pattern according to the four AbMs considered. The cocontraction between the TrA and PFMs in asymptomatic women showed a higher activation than that in symptomatic women.
However, compared to women without PFD, women with PFD, such as UI, demonstrated an increased cocontraction of AbMs (RA, OI, and OE), suggesting an altered mechanism.
One study (24) was excluded for a sensitivity analysis on the cocontraction of the TrA and OI because it did not report the position of women during the measurement. Additionally, as prior to the testing, the participants were trained until the correct performance of PFM contraction, we believe that such training before the measurement may have affected the data provided. Furthermore, another study (31) was not included in a sensitivity analysis of RA, OI, and OE. Although this study had the highest sample size, women with PFD were classified as having mild or severe UI, according to the severity of urine leakage. Moreover, the EMG data provided were smoothed by computing the root mean square. In this sensitivity analysis of RA, the I 2 value, previously at 100%, was reduced to 0% when this study (31) was removed. Moreover, the results from the sensitivity analysis in OI and OE reached statistical significance favoring the PFD group.

Strengths and limitations
The strengths of our study include our unique analysis of the influence of each of the four muscles from the abdominal wall during maximal and submaximal contraction of PFMs. Additionally, we have provided evidence of a different synergism between AbMs and PFMs in women with and without PFD.  14) The mean rate of coactivity of the transversus abdominis muscles was 2.5. The mean rate of coactivity of the transversus abdominis muscles in the exposed group was on average 1.02 lower (1.9 lower to 0.14 lower). of the obliquus externus in the exposed group was on average 0.01 higher (4.00 lower to 4.03 higher).

VERY LOW
The primary limitation of our review is the low evidence because of study limitations. We identified a small number of studies with a small number of participants, resulting in high CIs; therefore, these findings should be carefully interpreted. EMG results should be cautiously interpreted because most studies used surface electrodes, which may contaminate data and distort their interpretation because of the surrounding muscles (40). Additionally, the data processing of EMG studies widely differs, mostly in the position of the electrodes, the position of evaluation, and the type of data normalization.
Another limitation of this review was the insufficient number of included studies; we were not able to perform the complete statistical analysis. Furthermore, publication bias was not assessed because there were o10 eligible studies for each outcome in the meta-analysis (16).

Relation to prior work
Although previous systematic reviews have shown evidence of cocontraction between PFMs and AbMs (41,42), investigators had not previously conducted a comparison between women with a normal pelvic floor and those with PFD involving all four muscles of the abdominal wall (TrA, RA, OI, and OE). Furthermore, to our knowledge, there is no published meta-analysis of the cocontraction between PFMs and the four AbMs.
The first systematic review related to this theme focused only on the combined training of the TrA and PFMs to treat UI and included five studies (41). Another previous systematic review focused only on healthy women and included ten studies (42). In contrast, our search found 20 studies, and only five could be included in the metaanalyses. Our much larger analyses, including 468 women, more precisely elucidated the biomechanics of the communication between the abdominopelvic muscles in both the normal pelvic floor and PFD. Furthermore, we have also been able to detect the influence of each of the four muscles of the abdominal wall in PFM contraction.

Implications
PFD is very common among women worldwide and has become an increasing socioeconomic problem with prejudicial public health consequences, including symptoms that could lead to a significant decrease in quality of life and disability (43). While the prevalence of PFD is high, many factors involved in PFD are often poorly recognized or understood. Knowing the pathways related to PFD in detail is a main goal facilitating the identification of tools to prevent or correct these disorders (44). Our findings suggest a mechanism of PFD that is related to changes in the biomechanics caused by the increased AbM activation strength or by recruitment timing activation associated with different coactivity mechanisms according to the AbMs and PFMs.
In our view, there is a plausible biomechanical explanation to support higher coactivation levels of AbMs during MVC of PFMs. The coactivation between the TrA and PFMs showed a higher activation in asymptomatic women than in symptomatic women. However, the pattern of activation of the other AbMs differs with respect to time and strength in symptomatic women. During muscle contraction in PFD, there is a rapid and stronger coactivity of the RA, OI, and OE. The stronger coactivity of these AbMs could cause an 3.06) The mean rate of coactivity of the obliquus externus muscle was 9. The mean rate of coactivity of the obliquus externus in the exposed group was on average 2.08 higher (1.10 higher to 3.06 higher).
* Cross-sectional studies started from high quality evidence because of the nature of the clinical question. ** The estimated risk control was taken from the mean estimated control risk from the Tajiri (2011) study (35). *** The estimated risk control was taken from the mean estimated control risk from the Thompson (2006b) study (37). ****The estimated risk control was taken from the mean estimated control risk from the Madill (2009)  increase in intra-abdominal pressure that, added to the insufficient PFM contraction, would increase the PFD. Pereira et al. (45) proposed a theory explaining the synergism between the TrA and PFM. The abdominopelvic cavity has a static function of containment of the viscera and interacts with the PFMs. The fibers from the TrA are prolonged by the transverse perineal muscle because these muscles belong to the same muscle chain. This is an important conclusion for rehabilitation therapy, since numerous studies focus only on TrA strengthening to induce greater contractile strength of PFMs (22,27,35,36). Knowledge of the synergism among PFMs and AbMs may be useful for assessing PFMs and teaching women how to perform PFM exercises.
Our results show a synergism between AbMs and PFMs in women with and without PFD in different positions of evaluation. However, the studies included in this review had no standardized methods for selecting the participants, sample size, EMG, and US measurement, which limits the reliability of the findings. Very low-quality evidence suggests an association between the cocontraction of the AbMs when PFMs contract either in women with a normal pelvic floor or in women with PFD and should be interpreted with caution. Further research is needed to provide a better understanding of the cocontraction between the PFMs and AbMs. ' AUTHOR CONTRIBUTIONS Vesentini G, El Dib R and Rudge MVC were involved in the conception and design of the review. Vesentini G and El Dib R developed the search strategy. Vesentini G and Righesso LAR performed the study selection and data collection. Vesentini G, El Dib R, Righesso LAR and Rudge MVC were involved in the data analysis. Vesentini G, El Dib R, Rudge MVC and Barbosa AMP were involved in the interpretation and discussion of results. Vesentini G drafted the manuscript, and El Dib R, Piculo F, Marini G, Ferraz GAR, Calderon IMP, Barbosa AMP and Rudge MVC contributed to the drafting of the review. All authors approved the final version of the manuscript for publication. muscle contractions OR synergistic co-contraction of abdominal muscles OR synergism cocontraction of abdominal muscles OR co-contraction OR muscle synergism OR muscle co-contraction OR co-activity OR co-activity muscle)) ' APPENDIX Search strategy.