REVIEW ARTICLE Pelvic ﬂoor and abdominal muscle cocontraction in women with and without pelvic ﬂoor dysfunction: a systematic review and meta-analysis I, II,III IV I 0000-0000-0000-0000 0000-0000-0000-0000 Giovana Vesentini , * Regina El Dib, Leonardo Augusto Rachele Righesso , Fernanda Piculo, I,V I I Gabriela Marini, Guilherme Augusto Rago Ferraz, Iracema de Mattos Paranhos Calderon, Ange´lica VI I Mercia Pascon Barbosa, Marilza Vieira Cunha Rudge Departamento de Ginecologia e Obstetricia, Faculdade de Medicina de Botucatu, Universidade Estadual Paulista (UNESP), Botucatu, SP, BR. II Departamento de Biociencias e Diagnostico Bucal, Instituto de Ciencia e Tecnologia, Universidade Estadual Paulista (UNESP), Sao Jose dos Campos, SP, BR. III IV McMaster Institute of Urology, McMaster University, Hamilton, Ontario, Canada. Department of Oral and Maxillofacial Surgery, Mainz University V VI Medical Center, Mainz, Germany. Departamento de Ciencias da Saude, Universidade Sagrado Coracao, Bauru, SP, BR. Departamento de Fisioterapia e Terapia Ocupacional, Universidade Estadual Paulista (UNESP), Marilia, SP, BR. Vesentini G, El Dib R, Righesso LAR, Piculo F, Marini G, Ferraz GAR, et al. Pelvic ﬂoor and abdominal muscle cocontraction in women with and without pelvic ﬂoor dysfunction: a systematic review and meta-analysis. Clinics. 2019;74:e1319 *Corresponding author. E-mail: email@example.com 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; 1.02 [95% conﬁdence interval (CI) 1.90 to #1; 0.14], P=0.02; I = 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; I = not applicable; very low quality of evidence), and obliquus externus (OE) (SMD 2.08 [95% CI 1.10 to 3.06], Po0.0001; I = 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. KEYWORDS: Pelvic Floor Disorders; Abdominopelvic Muscles; Pelvic Floor Function; Synergism. prevalence is reported to be 25% to 46% in high-income (4), ’ INTRODUCTION low-income and middle-income countries (5). PFD is a Pelvic floor dysfunction (PFD) refers to a group of dis- common disease that affects women at all ages, exerting a turbances in the pelvic floor muscles (PFM) or connective severe impact on their lives and consuming considerable tissues usually associated with pelvic organ prolapse, urinary healthcare resources (4). and/or anal incontinence, sexual dysfunction, and pelvic pain Researchers have reported strategies, such as the use of a (1). Treatment-related costs are estimated to correspond to an model of abdominal muscle (AbM) training to stimulate annual expenditure of 12 billion dollars and are projected to tonic PFM activity (6). This scientific evidence is based on the increase every year (2), with a considerable prevalence accor- idea of synergistic cocontraction of the PFMs and AbMs, ding to the population and definition used (3). The estimated 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 Copyright & 2019 CLINICS – This is an Open Access article distributed under the terms of the Creative Commons License (http://creativecommons.org/licenses/by/ neglected aspect of care. The addition of AbM training might 4.0/) which permits unrestricted use, distribution, and reproduction in any improve clinical outcomes for patients with PFD (12) and medium or format, provided the original work is properly cited. restore normal PFM function. The lack of establishment of No potential conﬂict of interest was reported. coactivation between PFMs and AbMs in women with PFD Received for publication on April 30, 2019. Accepted for publication might reflect the lack of robust evidence that exercise regi- on October 4, 2019 mens other than PFM training would potentially add benefits to conservative management of PFD (13). DOI: 10.6061/clinics/2019/e1319 1 Cocontraction of the PFMs and abdominal muscles CLINICS 2019;74:e1319 Vesentini G et al. The understanding of cocontraction among AbMs and and evaluated them. Disagreements were resolved through PFMs could be valuable for alternative strategies of PFM exer- discussion or by consulting a third person (RED). cises to promote continence. In this systematic review, we investigate the coactivity of AbMs – transversus abdominis Data extraction (TrA), rectus abdominis (RA), obliquus internus (OI), and Data from included studies were summarized in a obliquus externus (OE) – and PFMs in women with or with- standardized data extraction with participant demographics, out PFD. We hypothesized that women with PFD would inclusion and exclusion criteria, cocontraction measurement show decreased coactivity of the AbMs or PFMs during maxi- methods, muscles studied and outcomes. Two reviewers (GV mal voluntary contraction (MVC) of the PFMs or AbMs, and LARR) extracted the sample size, means and stan- respectively, compared to women with no history of PFD. dard deviations (SD). When SD data were unavailable, we estimated the SD using the standard error according to the ’ MATERIALS AND METHODS recommendations of the Cochrane Handbook (16). If data regarding methods or results were incomplete, we This review adhered to the Preferred Reporting Items for attempted to contact the authors for further information. Systematic Reviews and Meta-analyses - PRISMA (14) and Moreover, when we found figures without data, we used the Meta-analysis of Observational Studies in Epidemiology - WebPlotDigitizer (v. 3.8) for Windows to extract an MOOSE (15) guidelines and was registered on PROSPERO estimation of the data from the figures. (CRD42017055462). Eligibility criteria Risk of bias assessment The risk of bias with a modified version of the Ottawa- Study design: any observational study (cohort, cross- Newcastle instrument was independently assessed by the sectional, comparative cross-sectional) or any baseline reviewers (17). This tool includes confidence in the assess- subset of data provided by randomized controlled trials, ment of exposure and outcome and an adjusted analysis for to avoid interaction effects due to any applied interven- differences between groups in prognostic characteristics tions. Studies that aimed to assess the reliability of scoring and missing data (17). When information regarding risk of systems for the investigation of cocontraction of the mus- bias or other aspects of methods or results was unavailable, cles under investigation in this review, as well as studies we attempted to contact the study authors for additional that provided information on our predefined outcomes, information. were also included; Participants: women with or without PFD, with urinary Certainty of evidence incontinence (UI), pelvic organ prolapse (POP), and pelvic The Grading of Recommendations Assessment, Develop- pain; ment and Evaluation (GRADE) system was used to rate the Interventions: any voluntary contraction of PFMs that certainty of the evidence for each outcome measure as high, recorded the cocontraction of AbMs (TrA, RA, OI, and OE) moderate, low, or very low (18). Detailed GRADE guidance and vice versa; was performed according to the following criteria: impreci- Outcomes: sion (19), inconsistency (20), and indirectness (21). The results are summarized in a table of evidence profile. J The cocontraction of AbMs (TrA, RA, OI, and OE) and PFMs was measured by surface electromyography (EMG), ultrasonography (US), a digital palpation scale, Data synthesis and statistical analysis or a perineometer; We analyzed the outcomes as continuous variables with random effect models on the results from the muscles investi- We also considered any indirect assessment of the muscle gated (TrA, RA, OI, and OE). Since the assessment of cocon- contraction. traction in the included studies was measured in different We excluded full-text peer-review studies that evaluated ways (e.g., US and EMG), the individual scales were aligned AbMs and PFMs in resting activity. to point in the same direction, and we calculated the standardized mean difference (SMD) along with the respec- Data source and searches tive confidence interval (CI) of 95%, using the extracted Using the Medical Subject Headings (MeSH), based on means and SDs (16). Positive SMD values indicated higher the combination of terms ‘‘female urinary incontinence,’’ cocontraction of the evaluated muscle in the PFD group ‘‘continent,’’ ‘‘pelvic floor,’’ ‘‘abdominopelvic musculature,’’ compared to the asymptomatic group, and a negative SMD and ‘‘abdominal muscle,’’ we ran the search strategy in indicated higher cocontraction of the evaluated muscle in the MEDLINE (1980 to December 21, 2018), EMBASE (1980 to asymptomatic group compared to the PFD group. December 21, 2018), PEDro (1999 to December 21, 2018), We also conducted sensitivity analyses to test the robust- LILACS (1982 to December 21, 2018), and CENTRAL (1999 ness of these results. When data were obtained from RCTs to December 21, 2018). No language restriction was applied. and the results were provided separately by intervention and This strategy was similar for the other databases and was control groups, we calculated the baseline mean and SD executed until December 21, 2018 (Appendix). based on the mean and SD from the studies. Furthermore, when studies provided both the left and right sides of the Selection of studies AbMs, we also calculated the mean and SD based on the Two reviewers (GV and LARR) independently screened mean and SD provided for both sides. all titles and abstracts identified by the literature search, We calculated the heterogeneity across studies using the I obtained full-text articles of all potentially relevant records, statistic and the p-value for the Chi-square test using Review 2 CLINICS 2019;74:e1319 Cocontraction of the PFMs and abdominal muscles Vesentini G et al. Figure 1 - Flowchart of the studies included in this review. Manager software (RevMan version 5.3; Nordic Cochrane supine position (8,9,22,25,29-31,35-38). Four studies (28,32,- Center, Cochrane). 33,39) considered different positions – standing, sitting and supine, and one did not report the position for the assess- ment of coactivity (26). Fifteen studies (8,9,23,25,26,28,30-35, ’ RESULTS 37-39) measured the contraction by EMG, four studies (22,24, Search results 27,36) measured the contraction by US, and one study (29) Figure 1 presents the PRISMA flow diagram for identify- measured the contraction by visual inspection and digital ing eligible studies based on title and abstract screening. palpation scale (Table 2). After the assessment of 93 full texts, we included 20 studies included in the systematic review with a subset of data Risk of bias assessment provided by one RCT (22), one prospective (23) and 18 cross- Figure 2 describes the risk of bias summary of the studies sectional studies (8,9,24-39) with a total of 468 participants. that compared two groups. Six observational studies com- The interobserver agreement for screening was substantial pared women with and without PFD. The main problems (kappa 0.82). with the studies were follow-up (24,29,31,34,36,38), informa- tion regarding cointerventions (24,29,31,34,36,38), assess- Study characteristics ment of outcome (24,29,34,36,38) and exposure (31,36,38). The sample size of the studies ranged from three (26) to 44 Table 3 details the description for each study. (31) participants. Typical participants were aged from 19 (25) to 66 (34) years old (Table 1). From a total of 20 included Outcomes studies, four (8,9,32,39) recorded the activity of all AbMs (TrA, RA, OI, and OE) during PFM contraction, and 19 studies provided instructions to contract the PFMs and recorded the Meta-analysis of TrA muscle cocontraction when the AbM coactivity (8,9,22-35,37-39). Fifteen studies (8,9,22-24,26, PFMs contract. The results from two studies (24,36) with a 28,31-37,39) reported the MVC of the PFMs. Three studies total of 52 participants assessing cocontraction by US failed to (23,27,34) considered the standing position for the assessment show a difference in the cocontraction of the TrA in women of the coactivity, and another eleven studies considered the with and without PFD (SMD #1; 0.61 [95% CI #1; 1.41 to 0.20], 3 Cocontraction of the PFMs and abdominal muscles CLINICS 2019;74:e1319 Vesentini G et al. Table 1 - Study characteristics related to the study design, location, number of participants, mean age, and inclusion and exclusion criteria. Author Study design Location No. participants Mean age Inclusion criteria Exclusion criteria With Pelvic Floor Dysfunction Bø et al. (27) Cross-sectional Europe 13 46.5 Consecutive women, at their ﬁrst Inability to understand the Norwegian language and consultation in an ongoing contract the PFMs; nulliparous or less than 12 m pp; randomized clinical trial on PFMT to previous pelvic surgery; chronic lung disease, or reduce POP stage 0 and 4 POP measured by the POP quantiﬁed Tajiri et al. (22) Randomized Asia 15 52 Women who had experienced one or NR control trial more SUI events in the last 1 m Without Pelvic Floor Dysfunction Bø et al. (26) Cross-sectional Europe 3 31.6 Physical therapists; aged 30-33 y; NR extensive experience in correct PFM contractions Bø et al. (25) Cross-sectional Europe 6 19.5 Women aged 19-21 y; nulliparous; no NR history of UI, neurological disease, or urinary tract infection; exercising regularly more than 3 #4; /week Sapsford et al. (6) Cross-sectional Australia 7 49.3 Parous women with a history of vaginal History of PFD or LBP; abdominal or pelvic surgery; deliveries neurological or respiratory condition; regularly performing sit-ups or AbM training Neumann et al. (33) Cross-sectional Australia 4 34 Nulliparous women aged 25-42 y, who Skinfold thickness of42.5 cm; history of LBP; known or were tested on two occasions 1 week suspected pregnancy; UI; urinary tract or vaginal apart infection; surgery involving incision of the left abdominal wall Madill et al. (9) Cross-sectional Canada 15 36.3 Continent women aged 21- 60 y; not History of DM, neurological conditions, or pregnant; had not given birth in the autoimmune CT disorders; used any medications to previous 12 months; in good general treat or known to exacerbate UI; previous history of health SUI Thompson et al. (37) Cross-sectional Australia 13 37 Women aged 20–55 y and premenopausal History of urinary tract or vaginal infection; known or or on HRT and consistent PFM exercise suspected pregnancy; surgery involving incision of technique the abdominal wall; obesity; history of LBP or sporting activities; neurological disorders; inability to understand English Madill et al. (32) Cross-sectional Canada 15 36.3 Women aged 21–60 y; no history of SUI; History of DM; neurological conditions; autoimmune not pregnant or had not given birth in CT disorders; used any medications to treat or known the previous 12 m and in good general to exacerbate UI; history of SUI health Junginger et al. (30) Cross-sectional NR 9 42 Volunteers without PFM disorders; aged History of LBP; hip or abdominal surgery or history of 32-59 y; with height of 157–174 cm and PFD and of laparotomy weight of 57-72 kg Strupp et al. (35) Cross-sectional Central and 34 28.1 Willingness to participate in the study Unable to contract AbM and PFM correctly; pregnancy; South America and ability to contract the PFM and neurological disease; autoimmune CT disorder or perform the AHT correctly PFD Chmielewska et al. (28) Cross-sectional Europe 19 23.6 Continent women aged 19-28 y SUI; pregnancy; childbirth(s); pelvic surgery; DM; hypertension; neurological abnormalities; urinary tract infection; elevated temperature; practicing a professional sport; spinal pain; obesity CLINICS 2019;74:e1319 Cocontraction of the PFMs and abdominal muscles Vesentini G et al. Table 1 - Continued. Author Study design Location No. participants Mean age Inclusion criteria Exclusion criteria Silva et al. (23) Prospective Central and 25 24.76 Women aged 18–35 y; no history of UI Virgin women; abdominal-pelvic surgeries; metabolic South America disorders; presence of myopathies and collagen diseases, neurological disorders, cognitive disturbance and physical limitations; previous PFM training; inability to contract PFM Ithamar et al. (39) Cross-sectional Central and 30 25.77 women aged 18-35 y; BMI between 18.50- Abdominal or pelvic surgery; pregnancy; metabolic South America 24.99 kg/m ; abdominal skinfold disorders; smoking; neurological; respiratory or p3 cm; with active or irregularly active cardiac disease; PFD or menstrual dysfunctions physical activity Both Devreese et al. (29) Cross-sectional Europe C: 40 C: 50.9 Patients were referred by the hospital for Subjects with a vaginal, urethral, or bladder infection, I: 40 I: 48.4 an individual pelvic ﬂoor exercise neurological disorders, LBP or pregnancy program Thompson et al. (38) Cross-sectional Australia C: 13 C: 37 Inclusion criteria for both groups were History of urinary tract or vaginal infection; known or I: 13 I: 38 women aged 20-55 y, premenopausal suspected pregnancy; surgery involving incision of or on HRT, and using a consistent PFM the abdominal wall; obesity; history of LBP or exercise technique sporting activities; neurological disorders; inability to understand English Madill et al. (31) Cross-sectional Canada C: 28 C: 46.8 C and SUI women aged 21-60 y; not Previous gynecological or continence surgery, POP I: 44 I: 49.65 pregnant and not given birth in the last greater than stage 2; intrinsic sphincter deﬁciency; 12 m; in good general health. history of DM; neurological conditions; autoimmune CT disorders; use of any medications to treat or known to exacerbate UI Arab et al. (24) Cross-sectional Asia C: 10 C: 41.66 Women who had UI, were Pregnancy and parturition in the previous 12 m; I: 10 I: 38.47 premenopausal, or were on HRT. neurological or respiratory disorders; severe LBP; POP Asymptomatic females, matched in age greater than stage 2; surgery of the abdominal or and body mass index and with no pelvic regions symptoms of UI. Tajiri (36) Cross-sectional Asia C: 25I: 7 C: 45.8 Primiparous women Not reported I: 50.1 Ptaszkowski et al. (34) Cross-sectional Europe C: 14 C: 66.1 Control group: no history of SUI; UI Inability to contract the PFMs; previous gynecological I: 16 I: 63.9 group: history of SUI. and abdominal surgery; neurologic condition; contraindications to measurements such as infection, menstruation, and allergy to nickel; other symptoms of PFD Thompson et al. study (37). Thompson et al. study (38). Abbreviations: NR: not reported; C: continent; I: incontinent; No. number; PFM: pelvic ﬂoor muscle; PFD: pelvic ﬂoor dysfunction; PFMT: pelvic ﬂoor muscle training; AbM: abdominal muscle; LBP: low back pain; HRT: hormone replacement therapy; DM: Diabetes mellitus; UI: urinary incontinence; POP: pelvic organ prolapse; CT: connective tissue; y: years; m: months; pp: postpartum; SUI: stress urinary incontinence; cm: centimeters; kg: kilograms; AHT: abdominal hypopressive technique; BMI: body mass index; cm: centimeters Cocontraction of the PFMs and abdominal muscles CLINICS 2019;74:e1319 Vesentini G et al. Table 2 - Study characteristics related to population, co-activity, and assessed outcomes. Author Instruction of co-activity Maximal Measurement of correct PFM Position Measurement PFMC Measurement and Muscles voluntary contraction tested of contraction variable assessed tested contraction (PFM) With Pelvic Floor Dysfunction Bø et al. (27) Activity of PFMs during TrA contraction. NR Inward lifting and squeezing of the Standing US Axial plane of minimal PFMs pelvic openings and vaginal hiatal dimensions. palpation. Area measured as cm . Tajiri et al. (22) Recorded TrA during PFM contraction. Yes Verbal orientation Supine US Not applicable AbMs Without Pelvic Floor Dysfunction Bø et al. (26) Activity of the RA during PFM contraction. Yes Perineal and vaginal palpation; NR EMG Balloon catheters. Result AbMs observation of movement and speciﬁcations not vaginal pressure measurements. described. Bø et al. (25) Activity of PFMs during abdominal NR Vaginal palpation; observation and Supine EMG Needle EMG. Result PFMs contraction. vaginal pressure measurements. speciﬁcations not described Sapsford et al. (6) Activity of the TrA, RA, OI, OE and PFM was Yes Vaginal palpation. Supine EMG Intravaginal probe using AbMs recorded during PFM contraction in three NEEN HealthCare. different lumbar spine positions. %MVC-normalized EMG amplitudes. Neuman et al. (33) Activity of the TrA, OI, and PFM was Yes Perineal and vaginal palpation; Supine and EMG Vaginal surface EMG. PFMs recorded. The subjects performed PFM observation of movement and standing %MVC-normalized and and abdominal contraction. vaginal pressure measurements. EMG amplitudes. AbMs Madill et al. (9) Activity of the TrA, RA, OI, OE and PFM was Yes Squeezing around the vagina and Supine EMG Modiﬁed Femiscant AbMs recorded during PFM contraction. visible cephalad movement of the EMG probe. %MVC- perineum, without breath normalized EMG holding. amplitudes. Thompson et al. (37) Activity of the RA, OI, OE, and PFM was Yes Vaginal palpation. Supine EMG Intravaginal probe PFMs recorded during PFM contraction and Using NEEN and valsalva. HealthCare. AbMs %MVC-normalized EMG amplitudes. Madill et al. (32) Activity of the TrA, RA, OI, and OE was Yes EMG and pressure and observation Supine, EMG Modiﬁed Femiscant AbMs recorded during PFM contraction. of the perineum. sitting, and EMG probe. %MVC- standing normalized EMG amplitudes. Junginger et al. (30) Activity of the TrA and PFM was recorded No Conﬁrmed by EMG. Supine EMG Intravaginal probe PFMs during abdominal and PFM contraction. Periform . %MVC- and normalized EMG AbMs amplitudes. Strupp et al. (35) Activity of the TrA and PFM was recorded. Yes Inspection and vaginal palpation. Supine EMG Intravaginal probe PFMs The subjects performed AHT and PFM Chattanooga Group . and contraction. MVEA-normalized AbMs EMG. CLINICS 2019;74:e1319 Cocontraction of the PFMs and abdominal muscles Vesentini G et al. Table 2 - Continued. Author Instruction of co-activity Maximal Measurement of correct PFM Position Measurement PFMC Measurement and Muscles voluntary contraction tested of contraction variable assessed tested contraction (PFM) Chmielewska et al. (28) Measurement of the TrA and RA during Yes Conﬁrmed by EMG. Supine, EMG Small diameter AbMs PFM contraction. sitting, and intravaginal probe. standing %MVC-normalized EMG amplitudes. Silva et al. (23) Activity of the TrA/OI during PFM Yes Vaginal palpation; orientation on Standing EMG Endovaginal sensor PFMs contraction. Activity of the PFM during how to effectively contract the PhysioMed Services and TrA/OI contraction. PFMs %. MVC-normalized AbMs EMG amplitudes. Ithamar et al. (39) Activity of the TrA/OI, RA, OE and PFM Yes Verbal orientation on how to Supine, EMG Intravaginal probe. PFMs during AHT effectively contract the PFMs standing %MVC-normalized and EMG amplitudes. quadrupedal Both Devreese et al. (29) PFMs during abdominal contraction. NR Inward observation of the perineum Supine Other Digital palpation. PFMs and vaginal palpation Scoring system Thompson et al. (38) Activity of the RA, OI, OE, and PFM was NR Vaginal palpation. Supine EMG Intravaginal probe PFMs recorded during PFM contraction and the Using NEEN and Valsalva maneuver. HealthCare. AbMs %MRC-normalized EMG amplitudes. Madill et al. (31) Activity of the RA, OI, and OE was recorded Yes Visible cephalad movement of the Supine EMG Modiﬁed Femiscant AbMs during PFM contraction. perineum. EMG probe. RMS-MVC EMG amplitudes. Arab et al. (24) Activity of the TrA and OI was recorded Yes Lifting of the bladder base on Not US Not applicable. AbMs during PFM contraction. transabdominal US. reported Tajiri et al. (36) TrA during PFM contraction. Yes NR Supine US Not applicable AbMs Ptaszkowski et al. (34) RA during PFM contraction. Yes Conﬁrmed by the physiotherapist. Standing EMG Life-care Vaginal Probe PFMs PR-02. RMS-MVC EMG and amplitudes. AbMs Thompson et al. study (37). Thompson et al. study (38). Abbreviations: NR: not reported; AbM: abdominal muscle; PFM: pelvic ﬂoor muscle; TrA: transversus abdominis; RA: rectus abdominis; OI: obliquus internus abdominis; OE: obliquus externus abdominis; EMG: electromyography; US: ultrasonography; IAP: intra-abdominal pressure; MVC: maximal voluntary contraction; MRC: maximal reference contraction; MVEA: maximal voluntary electrical activity; RMS: root mean square. Cocontraction of the PFMs and abdominal muscles CLINICS 2019;74:e1319 Vesentini G et al. Figure 2 - Risk of bias assessment. We considered ‘‘probably high risk of bias’’ as ‘‘deﬁnitely high risk of bias’’ (red color) and ‘‘probably low risk of bias’’ as ‘‘deﬁnitely low risk of bias’’ (green color). Table 3 - Risk of bias assessment of the included studies. Author Was the selection of Can we be Can we be conﬁdent Did the study match exposure Can we be Can we be Was the follow-up Were co- exposed and conﬁdent in the that the outcome of and nonexposure for all conﬁdent in the conﬁdent in the of cohorts interventions nonexposed cohorts assessment of interest was not variables that are associated assessment of the assessment of the adequate? similar between drawn from the same exposure? present at the start of with the outcome of interest or presence or absence outcome? groups? population? the study? did the statistical analysis adjust of prognostic for these prognostic variables? factors? Devreese et al. (29) Deﬁnitely low risk Probably low risk Probably low risk Probably high risk Deﬁnitely low risk Probably high risk Deﬁnitely high risk Probably high risk Thompson et al. (38) Probably high risk Probably high risk Probably low risk Probably low risk Deﬁnitely low risk Probably high risk Deﬁnitely high risk Probably high risk Madill et al. (31) Probably low risk Probably high risk Probably low risk Probably low risk Deﬁnitely low risk Deﬁnitely low risk Deﬁnitely high risk Probably high risk Arab et al. (24) Probably low risk Probably low risk Probably low risk Probably low risk Probably low risk Probably high risk Deﬁnitely high risk Probably high risk Tajiri et al. (36) Probably high risk Probably high risk Probably low risk Probably high risk Deﬁnitely low risk Probably high risk Deﬁnitely high risk Probably high risk Ptaszkowski et al. (34) Deﬁnitely low risk Probably low risk Probably low risk Probably low risk Deﬁnitely low risk Probably high risk Deﬁnitely high risk Probably high risk Thompson et al. study (38). CLINICS 2019;74:e1319 Cocontraction of the PFMs and abdominal muscles Vesentini G et al. Figure 3 - Forest plot showing the co-activity of the transversus abdominis, rectus abdominis, obliquus internus and obliquus externus muscles during maximal pelvic ﬂoor muscle contraction. CI = Conﬁdence interval; PFD = Pelvic ﬂoor dysfunction. p=0.14; I = 41%) (Figure 3). However, a plausible sensitivity Meta-analysis of OI abdominis muscle cocontraction analysis, excluding the study of Arab et al. (24), yielded results when the PFMs contract. The results from three studies that were inconsistent with the primary analysis, showing (24,31,38) with a total of 118 participants showed no higher coactivity of the TrA during MVC of the PFMs in difference between women with a normal pelvic floor and women without PFD (SMD #1; 1.02 [95% CI #1; 1.90 to #1; 0.14], women with PFD (UI) (SMD #1; 0.47 [95% CI #1; 2.38 to 1.44], 2 2 p=0.02; I = not applicable) (Figure 4). I = 95%; P=0.63) (Figure 3). However, a plausible sensitivity Certainty evidence was rated down to low because of analysis, excluding the studies of Madill et al. (31) and Arab serious limitations on the high risk of bias, indirectness et al. (24), presented results that were inconsistent with the due to the evaluation of only one PFD (UI) (Figure 3) and primary analysis, showing a higher mean of cocontraction in different ages, as well as imprecision (Table 4). 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 =not appli- cable) (Figure 4). Certainty of evidence was rated down to very low because Meta-analysis of RA muscle cocontraction when the of serious limitations on inconsistency due to high risk of bias, PFMs contract. The results from three studies (31,34,38) high heterogeneity (Figure 3), indirectness due to the evalua- with a total of 128 participants were unable to demonstrate a tion of only one PFD (UI), different assessments of UI and difference in the cocontraction of the RA between women different ages, and imprecision (Table 4). with a normal pelvic floor and women with PFD (UI) (SMD 2.05 [95% CI #1; 6.51 to 2.42], P=0.37; I = 98%) (Figure 3). Furthermore, the sensitivity analysis, excluding the Madill et al. study (31), showed results that were inconsistent with Meta-analysis of OE abdominis muscle cocontraction the primary analysis, with higher cocontraction of the RA when the PFMs contract. The results from two studies during MVC of the PFMs in women with PFD, however, (31,38) with a total of 98 participants failed to show a with no statistical significance (SMD 0.89 [95% CI -0.03 to difference between women with a normal pelvic floor and 1.82], P=0.06; I = 63%) (Figure 4). women with PFD (SMD 0.01 [95% CI #1; 4.00 to 4.03], P=1.00; Certainty of evidence was rated down to very low because I = 98%) (Figure 3). However, a plausible sensitivity analysis, of serious limitations on the high risk of bias, inconsistency excluding the study of Madill et al. (31), demonstrated due to high heterogeneity (Figure 3), indirectness due to results that were inconsistent with the primary analysis, evaluation of only one PFD (UI), different assessments of UI showing a higher mean of cocontraction in women with PFD and different ages, and imprecision (Table 4). (UI) than in women with a normal pelvic floor (SMD 2.08 9 Cocontraction of the PFMs and abdominal muscles CLINICS 2019;74:e1319 Vesentini G et al. Figure 4 - Sensitivity analysis of co-activity of transversus abdominis (without the Arab et al. 2011 study), rectus abdominis (without the Madill et al. (31)), obliquus internus (without the Madill et al. (31)) and obliquus externus (without the Madill et al. (31)) muscles when the pelvic ﬂoor muscles contract. CI = Conﬁdence interval; PFD = Pelvic ﬂoor dysfunction. [95% CI 1.10 to 3.06], Po0.0001; I = not applicable) However, compared to women without PFD, women with (Figure 4). PFD, such as UI, demonstrated an increased cocontraction of Certainty of evidence was rated down to very low AbMs (RA, OI, and OE), suggesting an altered mechanism. because of serious limitations on inconsistency due to high One study (24) was excluded for a sensitivity analysis on heterogeneity (Figure 3), indirectness due to high risk of bias, the cocontraction of the TrA and OI because it did not report evaluation of only one PFD (UI), different assessments of UI the position of women during the measurement. Addition- and different ages, and imprecision (Table 4). ally, 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 ’ DISCUSSION the data provided. Furthermore, another study (31) was not included in a sensitivity analysis of RA, OI, and OE. Main ﬁndings Although this study had the highest sample size, women This systematic review that investigated the cocontraction with PFD were classified as having mild or severe UI, of AbMs and PFMs in women with or without PFD according to the severity of urine leakage. Moreover, the identified 20 studies. Therefore, it might provide evidence EMG data provided were smoothed by computing the root of synergism between PFMs and the TrA, RA, OI and OE, mean square. In this sensitivity analysis of RA, the I value, i.e., the cocontraction of PFMs and AbMs occurs during both previously at 100%, was reduced to 0% when this study (31) voluntary contraction of the pelvic floor and abdominal was removed. Moreover, the results from the sensitivity muscle contractions. The studies showed a cocontraction of analysis in OI and OE reached statistical significance AbMs during the contraction of PFMs in women with no favoring the PFD group. history of symptoms of PFD, with PFD, or both. Meta- analysis 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 Strengths and limitations The strengths of our study include our unique analysis of between women with and without PFD, we performed a sensitivity analysis to minimize the heterogeneity of data. the influence of each of the four muscles from the abdominal Our sensitivity analysis showed a different cocontraction wall during maximal and submaximal contraction of PFMs. pattern according to the four AbMs considered. The cocon- Additionally, we have provided evidence of a different traction between the TrA and PFMs in asymptomatic women synergism between AbMs and PFMs in women with and showed a higher activation than that in symptomatic women. without PFD. 10 CLINICS 2019;74:e1319 Cocontraction of the PFMs and abdominal muscles Vesentini G et al. Table 4 - GRADE evidence proﬁle for cross-sectional studies: women without pelvic ﬂoor dysfunction versus women with pelvic ﬂoor dysfunction*. Quality assessment Summary of ﬁndings Certainty in estimates Studyeventrates MD(SD) Mean Anticipated absolute effects No. of difference OR participants Risk of bias Inconsistency Indirectness Imprecision Publication bias Women Women with Risk in women Risk in women with PFD* Quality of without PFD PFD (95% CI) without PFD* evidence (studies) Cocontraction activity of transversus abdominis muscles when the PFMs contract 52 Serious Nonserious Serious Serious Undetectable 2.5 (0.4)** 2.1 (0.3)** #1; 0.61 (#1; 1.42 The mean rate of The mean rate of coactivity ""OO a b d e (2) limitation limitation limitation limitation LOW to 0.20) coactivity of the of the transversus transversus abdominis abdominis muscles in the muscles was 2.5. exposed group was on average 0.61 lower (1.42 lower to 0.20 higher). Sensitivity analysis of cocontraction activity of transversus abdominis muscles when the PFMs contract 32 Serious Serious Serious Nonserious Undetectable 2.5 (0.4)** 2.1 #1; 1.02 The mean rate of The mean rate of coactivity "OOO a c d (1) limitation limitation limitation VERY LOW limitation (0.3)** (#1; 1.90 to coactivity of the of the transversus -0.14) transversus abdominis abdominis muscles in the muscles was 2.5. exposed group was on average 1.02 lower (1.9 lower to 0.14 lower). Cocontraction activity of the rectus abdominis muscle when the PFMs contract 128 Serious Serious Serious Serious "OOO Undetectable 6 (4)*** 8 (5)*** #1; 2.05 (#1; 6.51 The mean rate of The mean rate of coactivity a c d e limitation limitation limitation (3) limitation VERY LOW to 2.42) coactivity of the of the rectus abdominis rectus abdominis in the exposed group muscle was 6. was on average 2.05 lower (6.51 lower to 2.42 higher). Sensitivity analysis of the cocontraction activity of the rectus abdominis muscle when the PFMs contract 56 Serious Serious Serious Nonserious ""OO Undetectable 6 (4)*** 8 (5)*** 0.89 (-0.03 to The mean rate of The mean rate of coactivity a c d e (2) limitation limitation limitation limitation LOW 1.82) coactivity of the of the rectus abdominis rectus abdominis in the exposed group muscle was 6. was on average 0.89 higher (0.03 higher to 1.82 higher). Cocontraction activity of the obliquus internus abdominis muscle when the PFMs contract 118 Serious Serious Serious Serious "OOO Undetectable 23 (3)**** 18 (2)**** #1; 0.47 (#1; 2.38 The mean rate of The mean rate of coactivity a c d e (3) limitation limitation limitation limitation VERY LOW to 1.44) coactivity of the of the obliquus internus obliquus internus in the exposed group muscle was 0.23 was on average 0.47 lower (2.38 lower to 1.44 higher). Sensitivity analysis of the cocontraction activity of the obliquus internus abdominis muscle when the PFM contracts 26 Serious Serious Serious Nonserious Undetectable 26 (18)*** 57 (34)*** 1.10 (0.27 to The mean rate of The mean rate of coactivity ""OO a c d e (1) limitation limitation limitation limitation LOW 1.94) coactivity of the of the obliquus internus obliquus internus in the exposed group muscle was 26. was on average 1.10 higher (0.27 higher to 1.94 higher). Cocontraction activity of the obliquus externus abdominis muscles when the PFM contracts 98 Serious Serious Serious Serious Undetectable 30 (5)**** 21 (4)**** 0.01 (#1; 4.00 to The mean rate of The mean rate of coactivity "OOO a c d e (2) limitation limitation limitation limitation VERY LOW 4.03) coactivity of the of the obliquus externus obliquus externus in the exposed group muscle was 30. was on average 0.01 higher (4.00 lower to 4.03 higher). Cocontraction of the PFMs and abdominal muscles CLINICS 2019;74:e1319 Vesentini G et al. 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 contam- inate 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 evi- dence 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 meta- analyses. Our much larger analyses, including 468 women, more precisely elucidated the biomechanics of the commu- nication 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 prejudi- cial 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 mecha- nism of PFD that is related to changes in the biomechanics caused by the increased AbM activation strength or by recruit- ment 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 Table 4 - Continued. Quality assessment Summary of ﬁndings Certainty in estimates Study event ratesMD (SD) Mean Anticipated absolute effects No. of difference OR Risk of bias Inconsistency Indirectness Imprecision Publication bias Women Women with Risk in women Risk in women with PFD* Quality of participants without PFD PFD without PFD* (studies) (95% CI) evidence Sensitivity analysis of the cocontraction activity of the obliquus externus abdominis muscle when the PFMs contract 26 Serious Serious Serious Nonserious Undetectable 9 (4)*** 37 (18)*** 2.08 (1.10 to The mean rate of The mean rate of coactivity ""OO a c d e (1) limitation limitation limitation limitation LOW 3.06) coactivity of the of the obliquus externus obliquus externus in the exposed group muscle was 9. was on average 2.08 higher (1.10 higher to 3.06 higher). Abbreviations: MD: mean difference; SD: standard deviation; PFD: pelvic ﬂoor dysfunction; CI: Conﬁdence interval. * 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) study (30). Issues related to exposure and outcome assessments, follow-up period and cointerventions. b 2 There may not be considerable heterogeneity (I o50%). c 2 There is considerable heterogeneity (I 475%). Included studies with only one PFD. 95% Conﬁdence interval for absolute effects include clinically important signiﬁcance and no signiﬁcance. CLINICS 2019;74:e1319 Cocontraction of the PFMs and abdominal muscles Vesentini G et al. increase in intra-abdominal pressure that, added to the 6. Sapsford RR, Hodges PW. Contraction of the pelvic floor muscles during abdominal maneuvers. Arch Phys Med Rehabil. 2001;82(8):1081-8. insufficient PFM contraction, would increase the PFD. https://doi.org/10.1053/apmr.2001.24297 Pereira et al. (45) proposed a theory explaining the 7. Sapsford R. The Pelvic Floor: A clinical model for function and rehabili- synergism between the TrA and PFM. The abdominopelvic tation. Physiotherapy. 2001;87(12):620-30. https://doi.org/10.1016/S0031- 9406(05)61107-8 cavity has a static function of containment of the viscera 8. Sapsford RR, Hodges PW, Richardson CA, Cooper DH, Markwell SJ, Jull and interacts with the PFMs. The fibers from the TrA are GA. Co-activation of the abdominal and pelvic floor muscles during prolonged by the transverse perineal muscle because these voluntary exercises. Neurourol Urodyn. 2001;20(1):31-42. https://doi. org/10.1002/1520-6777(2001)20:1o31::AID-NAU543.0.CO;2-P muscles belong to the same muscle chain. This is an impor- 9. Madill SJ, McLean L. Relationship between abdominal and pelvic floor tant conclusion for rehabilitation therapy, since numerous muscle activation and intravaginal pressure during pelvic floor muscle studies focus only on TrA strengthening to induce greater contractions in healthy continent women. Neurourol Urodyn. 2006;25(7): 722-30. https://doi.org/10.1002/nau.20285 contractile strength of PFMs (22,27,35,36). Knowledge of 10. Nambiar AK, Bosch R, Cruz F, Lemack GE, Thiruchelvam N, Tubaro A, the synergism among PFMs and AbMs may be useful for et al. EAU Guidelines on Assessment and Nonsurgical Management of assessing PFMs and teaching women how to perform PFM Urinary Incontinence. Eur Urol. 2018;73(4):596-609. https://doi.org/ 10.1016/j.eururo.2017.12.031 exercises. 11. Qaseem A, Dallas P, Forciea MA, Starkey M, Denberg TD, Shekelle P, et al. Our results show a synergism between AbMs and PFMs in Nonsurgical management of urinary incontinence in women: a clinical women with and without PFD in different positions of practice guideline from the American College of Physicians. Ann Intern evaluation. However, the studies included in this review had Med. 2014;161(6):429-40. https://doi.org/10.7326/M13-2410 12. Sapsford R. Rehabilitation of pelvic floor muscles utilizing trunk stabili- no standardized methods for selecting the participants, zation. Man Ther. 2004;9(1):3-12. https://doi.org/10.1016/S1356-689X(03) sample size, EMG, and US measurement, which limits the 00131-0 reliability of the findings. Very low-quality evidence suggests 13. Bø K, Herbert RD. There is not yet strong evidence that exercise regimens other than pelvic floor muscle training can reduce stress urinary incon- an association between the cocontraction of the AbMs when tinence in women: a systematic review. J Physiother. 2013;59(3):159-68. PFMs contract either in women with a normal pelvic floor or https://doi.org/10.1016/S1836-9553(13)70180-2 in women with PFD and should be interpreted with caution. 14. Moher D, Liberati A, Tetzlaff J, Altman DG; PRISMA Group. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA Further research is needed to provide a better understanding statement. Ann Intern Med. 2009;151(4):264-9, W64. https://doi.org/ of the cocontraction between the PFMs and AbMs. 10.7326/0003-4819-151-4-200908180-00135 15. Stroup DF, Berlin JA, Morton SC, Olkin I, Williamson GD, Rennie D, et al. Meta-analysis of observational studies in epidemiology: a proposal for ’ ACKNOWLEDGMENTS reporting. Meta-analysis Of Observational Studies in Epidemiology (MOOSE) group. JAMA. 2000;283(15):2008-12. https://doi.org/10.1001/ This study was supported by grants from FAPESP/Brazil (#2016/09710- jama.283.15.2008 9). Giovana Vesentini received a Brazilian Research Council (FAPESP) 16. Higgins JPT, Green S (editors). Cochrane Handbook for Systematic Reviews scholarship (#2014/26852-6). Regina El Dib received a Brazilian Research of Interventions Version 5.1.0 [updated March 2011]. The Cochrane Colla- Council (CNPq) scholarship (#310953/2015-4). Marilza Vieira Cunha boration, 2011. Available from: www.handbook.cochrane.org 17. Guyatt GH, Busse JW. Modification of Ottawa-Newcastle to assess risk of Rudge received a Brazilian Research Council (CNPq) scholarship bias in nonrandomized trials. http://distillercer.com/resources/ (#302284/2014-1). We thank Vinicius Sepúlveda for his help with the s 18. Guyatt GH, Oxman AD, Vist GE, Kunz R, Falck-Ytter Y, Alonso-Coello P, WebPlotDigitizer (v. 3.8) for Windows. et al. GRADE: an emerging consensus on rating quality of evidence and strength of recommendations. BMJ. 2008;336(7650):924-6. https://doi. org/10.1136/bmj.39489.470347.AD ’ AUTHOR CONTRIBUTIONS 19. Guyatt GH, Oxman AD, Kunz R, Brozek J, Alonso-Coello P, Rind D, et al. GRADE guidelines 6. Rating the quality of evidence--imprecision. J Clin Vesentini G, El Dib R and Rudge MVC were involved in the conception Epidemiol. 2011;64(12):1283-93. https://doi.org/10.1016/j.jclinepi.2011. and design of the review. Vesentini G and El Dib R developed the search 01.012 strategy. Vesentini G and Righesso LAR performed the study selection and 20. Guyatt GH, Oxman AD, Kunz R, Woodcock J, Brozek J, Helfand M, et al. data collection. Vesentini G, El Dib R, Righesso LAR and Rudge MVC GRADE guidelines: 7. Rating the quality of evidence--inconsistency. J Clin Epidemiol. 2011;64(12):1294-302. https://doi.org/10.1016/ were involved in the data analysis. Vesentini G, El Dib R, Rudge MVC and j.jclinepi.2011.03.017 Barbosa AMP were involved in the interpretation and discussion of results. 21. Guyatt GH, Oxman AD, Kunz R, Woodcock J, Brozek J, Helfand M, et al. Vesentini G drafted the manuscript, and El Dib R, Piculo F, Marini G, GRADE guidelines: 8. Rating the quality of evidence--indirectness. J Clin Ferraz GAR, Calderon IMP, Barbosa AMP and Rudge MVC contributed Epidemiol. 2011;64(12):1303-10. https://doi.org/10.1016/j.jclinepi.2011. to the drafting of the review. All authors approved the ﬁnal version of the 04.014 22. Tajiri K, Huo M, Maruyama H. Effects of Co-contraction of Both Trans- manuscript for publication. verse Abdominal Muscle and Pelvic Floor Muscle Exercises for Stress Urinary Incontinence: A Randomized Controlled Trial. J Phys Ther Sci. 2014;26(8):1161-3. https://doi.org/10.1589/jpts.26.1161 ’ REFERENCES 23. 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(Women OR woman OR female OR Women’s Groups OR Women’s Group OR Women Groups OR Women Group OR healthy women OR healthy woman OR incontinent OR incontinent women OR incontinent woman OR urinary incontinence in women OR Female Urinary Incontinence OR continent OR continent women OR continent woman OR urgency urinary incontinence OR Urinary Stress Incontinence OR stress urinary incontinence OR stress urinary OR UUI OR SUI OR MUI OR Urinary Urge Incontinence OR Urinary Reﬂex Incontinence OR Urge Incontinence OR mixed urinary incontinence OR Urinary Bladder Disease OR Urinary Bladder Diseases OR Urinary Reﬂex Incontinence) AND ((Pelvic Floor OR Pelvic Diaphragm OR Pelvic Diaphragms OR Pelvic Floor Disorders OR Pelvic Floor Disorder OR Pelvic Floor Disease OR Pelvic Floor Diseases OR pelvic ﬂoor dysfunction OR pelvic ﬂoor dysfunctions OR Pelvic Floor muscle OR Pelvic Floor muscles OR Urinary Incontinence OR abdomino-pelvic musculature OR perineal musculature OR Perineum OR perineums OR perineal function OR pelvic ﬂoor contraction OR pelvic ﬂoor muscle contractions OR co-contraction OR muscle synergism OR muscle co-contraction OR co-activity OR co-activity muscle) AND (Abdominal Muscles OR Abdominal Muscle OR Abdomen OR Abdomens OR abdomino-pelvic musculature OR transversus abdominis OR Rectus Abdominis OR Rectus Muscle of Abdomen OR Abdomen Rectus Muscle OR Abdomen Rectus Muscles OR external obliques OR external oblique OR internal obliques OR internal oblique OR abdominal muscle contractions OR synergistic co-contraction of abdominal muscles OR synergism co- contraction of abdominal muscles OR co-contraction OR muscle synergism OR muscle co-contraction OR co-activity OR co-activity muscle))
Clinics – Pubmed Central
Published: Nov 19, 2019
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