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Evaluating maternal recovery from labor and delivery: bone and levator ani injuries

      Objective

      We sought to describe occurrence, recovery, and consequences of musculoskeletal (MSK) injuries in women at risk for childbirth-related pelvic floor injury at first vaginal birth.

      Study Design

      Evaluating Maternal Recovery from Labor and Delivery is a longitudinal cohort design study of women recruited early postbirth and followed over time. We report here on 68 women who had birth-related risk factors for levator ani (LA) muscle injury, including long second stage, anal tears, and/or older maternal age, and who were evaluated by MSK magnetic resonance imaging at both 7 weeks and 8 months’ postpartum. We categorized magnitude of injury by extent of bone marrow edema, pubic bone fracture, LA muscle edema, and LA muscle tear. We also measured the force of LA muscle contraction, urethral pressure, pelvic organ prolapse, and incontinence.

      Results

      In this higher-risk sample, 66% (39/59) had pubic bone marrow edema, 29% (17/59) had subcortical fracture, 90% (53/59) had LA muscle edema, and 41% (28/68) had low-grade or greater LA tear 7 weeks’ postpartum. The magnitude of LA muscle tear did not substantially change by 8 months’ postpartum (P = .86), but LA muscle edema and bone injuries showed total or near total resolution (P < .05). The magnitude of unresolved MSK injuries correlated with magnitude of reduced LA muscle force and posterior vaginal wall descent (P < .05) but not with urethral pressure, volume of demonstrable stress incontinence, or self-report of incontinence severity (P > .05).

      Conclusion

      Pubic bone edema and subcortical fracture and LA muscle injury are common when studied in women with certain risk factors. The bony abnormalities resolve, but levator tear does not, and is associated with levator weakness and posterior-vaginal wall descent.

      Key words

      See related editorial, page 121
      Childbirth is arguably one of the most dramatic musculoskeletal (MSK) events the human body undergoes. Passage of the newborn through the pelvis and its muscles requires an exceptional degree of soft-tissue stretch.
      • Lien K.C.
      • Mooney B.
      • DeLancey J.O.
      • Ashton-Miller J.A.
      Levator ani muscle stretch induced by simulated vaginal birth.
      Childbirth exerts remarkable stresses on maternal pelvic bones from the pressures of the fetal head and the forces of abdominal muscles used during maternal pushing that originate from the pelvic bones. Such stretch and stress may produce injury in some women.
      In the last decade, new imaging techniques have brought important new insights into understanding the mechanisms of soft-tissue and bony injury.
      • DelGrande F.
      • Santini F.
      • Herzka D.
      • et al.
      Fat-suppression techniques for 3-T MR imaging of the musculoskeletal system.
      Special sequences in MSK magnetic resonance imaging (MRI) offer advantages over other imaging techniques for studying deep bony and soft-tissue changes. Fluid-sensitive sequences have the best combined specificity and sensitivity for revealing areas of injury and edema. Hence, they are the recommended diagnostic imaging test for stress injuries.
      • Nattiv A.
      • Kennedy G.
      • Barrack M.
      • et al.
      Correlation of MRI grading of bone stress injuries with clinical risk factors and return to play: a 5-year prospective study in collegiate track and field athletes.
      • Datir A.
      • Saini A.
      • Connell A.
      • Saifuddin A.
      Stress-related bone injuries with emphasis on MRI.
      These sequences are commonly applied in evaluation of sports-related injury to allow for detection of injuries not seen with other MRI sequences or imaging modalities.
      • DelGrande F.
      • Santini F.
      • Herzka D.
      • et al.
      Fat-suppression techniques for 3-T MR imaging of the musculoskeletal system.
      • Nattiv A.
      • Kennedy G.
      • Barrack M.
      • et al.
      Correlation of MRI grading of bone stress injuries with clinical risk factors and return to play: a 5-year prospective study in collegiate track and field athletes.
      • Plewes D.
      • Kuscharczyk W.
      Physics of MRI, a primer.
      • Bley T.
      • Wieben O.
      • Francois C.
      • Brittain J.
      • Reeder S.
      Fat and water magnetic resonance imaging.
      • Kiuru M.
      • Pihlajamaki H.
      • Ahovuo J.
      Fatigue stress injuries of the pelvic bone and proximal femur: evaluation with MRI imaging.
      However, MSK-MRI fluid-sensitive sequences have only recently been applied to reveal the scope of childbirth-related pelvic injuries.
      • Miller J.M.
      • Brandon C.
      • Jacobson J.A.
      • et al.
      MRI findings in patients considered high risk for pelvic floor injury studied serially after vaginal childbirth.
      • Brandon C.
      • Jacobson J.
      • Low L.
      • Park L.
      • DeLancey J.O.
      • Miller J.
      Pubic bone injuries in primiparous women: magnetic resonance imaging in detection and differential diagnosis of structural injury.
      • Low L.K.
      • Zielinski R.
      • Brandon C.
      • Galecki A.
      • Tao Y.
      • Miller J.
      Predicting birth-related levator ani tear severity in primiparous women: evaluating maternal recovery from labor and delivery (EMRLD study).
      • Betschart C.
      • Kim J.
      • Miller J.M.
      • Ashton-Miller J.A.
      • DeLancey J.O.L.
      Comparison of muscle fiber directions between different levator ani muscle subdivisions: in vivo MRI measurements in women.
      Soon after beginning a study of levator ani (LA) muscle injury following vaginal birth, it became evident we should add these standard MSK-MRI fluid-sensitive sequences to our existing protocol of anatomical MRI sequences to better characterize the full scope of possible injuries and pattern of recovery.
      The purpose of this study is to report on the occurrence and severity of bony and LA muscle injuries observed and how magnitude of tissue trauma relates to clinical consequences in the first 8 months’ postpartum. Fluid-sensitive sequences are necessary for 3 of 4 indicators of bone and muscle injury evaluated in our study. The sequences show: (1) increased signal that indicates edema (extracellular fluid) in bone; (2) matched linear signal changes in bone that indicate a fracture; or (3) increased signal that indicates edema in muscle. The fourth indicator of injury, visual discontinuity of muscle seen with muscle tear, does not require fluid-sensitive sequences. However, use of fluid-sensitive sequences makes detection of tears and their magnitude much easier. The precision of these measures offered opportunity to assess more precisely the relationship between injury magnitude and relative consequences seen clinically in the first 8 months’ postpartum.

      Materials and Methods

      Study design

      The parent study Evaluating Maternal Recovery from Labor and Delivery (EMRLD) is an institutional review board–approved (University of Michigan Institutional Review Board HUM00051193) longitudinal cohort study following up primiparous women with recent history of childbirth. In this article, we report on those with higher-risk factors for LA injury. The first published reports from this work included: (1) details on EMRLD’s sampling strategies and a Strengthening the Reporting of Observational Studies in Epidemiology diagram; (2) specifics of using MSK-MRI methods; (3) ensuing anatomical detail of pelvic floor structures at rest, during dynamic activity, and by LA muscle subdivision and line of action; and (4) predominant demographic or obstetric variables associated with LA tear when evaluated early postpartum.
      • Miller J.M.
      • Brandon C.
      • Jacobson J.A.
      • et al.
      MRI findings in patients considered high risk for pelvic floor injury studied serially after vaginal childbirth.
      • Brandon C.
      • Jacobson J.
      • Low L.
      • Park L.
      • DeLancey J.O.
      • Miller J.
      Pubic bone injuries in primiparous women: magnetic resonance imaging in detection and differential diagnosis of structural injury.
      • Low L.K.
      • Zielinski R.
      • Brandon C.
      • Galecki A.
      • Tao Y.
      • Miller J.
      Predicting birth-related levator ani tear severity in primiparous women: evaluating maternal recovery from labor and delivery (EMRLD study).
      • Betschart C.
      • Kim J.
      • Miller J.M.
      • Ashton-Miller J.A.
      • DeLancey J.O.L.
      Comparison of muscle fiber directions between different levator ani muscle subdivisions: in vivo MRI measurements in women.
      • Yousuf A.A.
      • DeLancey J.O.
      • Brandon C.J.
      • Miller J.M.
      Pelvic structure and function at 1 month compared to 7 months by dynamic magnetic resonance after vaginal birth.
      EMRLD data collection occurred from June 13, 2005, through March 14, 2012, collecting data at approximately 7 weeks after a first vaginal birth and again at about 8 months after first vaginal birth. In this article, we report the 7 weeks to 8 months’ postpartum longitudinal findings.

      Sample

      The enriched sampling relied on inclusion criteria of heuristically determined risk factors for LA tear (eg, prolonged second stage, anal sphincter tear, higher maternal age, forceps delivery) suggestive in 2005, the time of the study’s start.
      • Kearney R.
      • Miller J.
      • Ashton-Miller J.
      • DeLancey J.O.
      Obstetric factors associated with levator ani muscle injury after vaginal birth.
      Women were excluded from EMRLD if aged <18 years, spoke a primary health care language other than English, delivered at <36 weeks’ gestation, birthed >1 infant, or if the infant was admitted to neonatal intensive care.
      Of the 90 women originally recruited into EMRLD, 22 women did not have a second MRI at 8 months’ postpartum. Our analysis was based on the 68 women with MRI data at both 7 weeks and 8 months’ postpartum.
      • Brandon C.
      • Jacobson J.
      • Low L.
      • Park L.
      • DeLancey J.O.
      • Miller J.
      Pubic bone injuries in primiparous women: magnetic resonance imaging in detection and differential diagnosis of structural injury.

      MRI

      MRIs were completed on a 3-T Philips Achieva (Philips Medical System, Eindhoven, The Netherlands) with an 8-channel cardiac coil positioned over the pelvis. The lower pelvis was imaged in the coronal, axial, and sagittal planes with proton density-weighted (PD) sequences; repeat time (TR) = 2107 milliseconds; echo time (TE) = 30 milliseconds; number sequence averages = 2; slice thickness = 4 mm, gap = 1 mm; and field of view (FOV) = 20 cm, matrix = 256 × 256. For better definition of the anterior pelvic floor anatomy, additional tailored imaging (slice thickness = 2 mm, gap = 0.2 mm; FOV = 18 cm, matrix = 256 × 256) included 3 planes of PD sequences and axial and coronal planes, either PD fat saturation (TR = 2355 milliseconds; TE = 30 milliseconds) or short tau inversion recovery (STIR) (TR = 5987 milliseconds; TE = 60 milliseconds; number sequence averages = 2) sequences. A single sacral PD fat saturation sequence was obtained in the axial plane (slice thickness = 4 mm, gap = 1 mm; FOV = 20 cm, matrix = 256 × 256).
      The complete MRI protocol has been discussed in previously published reports.
      • Miller J.M.
      • Brandon C.
      • Jacobson J.A.
      • et al.
      MRI findings in patients considered high risk for pelvic floor injury studied serially after vaginal childbirth.
      • Brandon C.
      • Jacobson J.
      • Low L.
      • Park L.
      • DeLancey J.O.
      • Miller J.
      Pubic bone injuries in primiparous women: magnetic resonance imaging in detection and differential diagnosis of structural injury.
      MRIs were reviewed by 2 board-certified, fellowship-trained MSK radiologists who were blinded to details of an individual woman’s birth data and risk category. They were aware if the woman was having her initial 7 weeks or 8 months’ postpartum visit since the postpartum uterus was obvious in the pelvic MRI study.
      We used standard MSK-MRI radiology grading categories to evaluate edema and fractures in bone and muscle injuries so our data could be compared across time and studies in the radiology literature.
      • Nattiv A.
      • Kennedy G.
      • Barrack M.
      • et al.
      Correlation of MRI grading of bone stress injuries with clinical risk factors and return to play: a 5-year prospective study in collegiate track and field athletes.
      • Kiuru M.
      • Pihlajamaki H.
      • Ahovuo J.
      Fatigue stress injuries of the pelvic bone and proximal femur: evaluation with MRI imaging.
      • Mueller-Wohlfahrt H.W.
      • Haensel L.
      • Mithoefer K.
      • et al.
      Terminology and classification of muscle injuries in sport: the Munich consensus statement.
      When there was a difference in scoring between the 2 radiologists, the scans were reviewed together and graded by consensus, consistent with standard procedures in radiology. The radiologists measured and scored 4 sites of likely MSK injury.

      Pubic bone marrow evaluation for edema

      Bone marrow edema was assessed by grading signal intensity (none, mild, moderate, or intense) within the bone marrow of each pubic bone (right, left) as compared with the ischial tuberosity and other bones in the FOV.
      • Nattiv A.
      • Kennedy G.
      • Barrack M.
      • et al.
      Correlation of MRI grading of bone stress injuries with clinical risk factors and return to play: a 5-year prospective study in collegiate track and field athletes.
      • Datir A.
      • Saini A.
      • Connell A.
      • Saifuddin A.
      Stress-related bone injuries with emphasis on MRI.
      • Kiuru M.
      • Pihlajamaki H.
      • Ahovuo J.
      Fatigue stress injuries of the pelvic bone and proximal femur: evaluation with MRI imaging.
      • Paajanen H.
      • Hermunen H.
      • Karonen J.
      Effect of heavy training in contact sports on MRI findings in the pubic region of asymptomatic competitive athletes compared with non-athlete controls.
      The spectrum of bone stress injuries has been correlated with clinical findings in athletes and military recruits and is graded 0-4, based on the degree of bone marrow edema according to the MSK-MRI scale with STIR or fat-suppressed sequences.
      • Nattiv A.
      • Kennedy G.
      • Barrack M.
      • et al.
      Correlation of MRI grading of bone stress injuries with clinical risk factors and return to play: a 5-year prospective study in collegiate track and field athletes.
      • Datir A.
      • Saini A.
      • Connell A.
      • Saifuddin A.
      Stress-related bone injuries with emphasis on MRI.
      • Kiuru M.
      • Pihlajamaki H.
      • Ahovuo J.
      Fatigue stress injuries of the pelvic bone and proximal femur: evaluation with MRI imaging.
      • Fredericson M.
      • Bergman A.G.
      • Hoffman K.L.
      • Dillingham M.S.
      Tibial stress reaction in runners: correlation of clinical symptoms and scintigraphy with a new magnetic resonance imaging grading system.
      • Arendt E.
      • Agel J.
      • Heikes C.
      • Griffiths H.
      Stress injuries to bone in college athletes: a retrospective review of experience at a single institution.
      • Niva M.H.
      • Mattila V.M.
      • Kiuru M.J.
      • Pihlajamäki H.K.
      Bone stress injuries are common in female military trainees: a preliminary study.
      Grade 0 is no abnormal signal. Grades 1-3 are mild, moderate, and intense bone marrow edema. Grade 4 is a true stress fracture with a line of increased signal (STIR or fat-suppressed sequences) with matching linear decreased signal on T1.

      Pubic bone evaluation for fracture

      Evidence of pubic bone fractures in the cortical or trabecular bone was assessed as matching lines of increased and decreased signal on the fluid-sensitive and standard T1 sequences visible in 2 imaging planes.
      • Nattiv A.
      • Kennedy G.
      • Barrack M.
      • et al.
      Correlation of MRI grading of bone stress injuries with clinical risk factors and return to play: a 5-year prospective study in collegiate track and field athletes.
      • Kiuru M.
      • Pihlajamaki H.
      • Ahovuo J.
      Fatigue stress injuries of the pelvic bone and proximal femur: evaluation with MRI imaging.
      Fractures were recorded as none, subcortical, or cortical fractures for both pubic bones.

      LA evaluation for edema

      The LA was evaluated for the presence and location of increased signal, indicating edema consistent with stress or injury, as compared with other pelvic muscles, including the obturator internus. Grading classification categories were none, mild, moderate, or intense for each side.

      LA evaluation for tear

      The LA was evaluated for discontinuity of muscle observed as loss of visible muscle in an area where it is known to occur, indicating muscle tear. Grading classifications were: 0% to <20% (none to subtle), 20% to <50% (low grade), or ≥50% (high grade) for each side. Based on previous pelvic floor imaging experience, it was assumed that normal muscles should be symmetric and that each should have the same morphological configuration as muscles seen in nulliparous controls reported in other studies.
      • DeLancey J.O.
      • Kearney R.
      • Chou Q.
      • Speights S.
      • Binno S.
      The appearance of levator ani muscle abnormalities in magnetic resonance images after vaginal delivery.
      • Morgan D.M.
      • Umek W.
      • Stein T.
      • Hsu Y.
      • Guire K.
      • DeLancey J.O.
      Interrater reliability of assessing levator ani muscle defects with magnetic resonance images.

      Clinical symptoms and pelvic floor function evaluation

      Participants completed standardized questionnaires on symptoms of urinary and fecal incontinence at 7 weeks and 8 months’ postpartum.
      • Jorge J.M.
      • Wexner S.D.
      Etiology and management of fecal incontinence.
      • Sandvik H.
      • Hunskaar S.
      • Seim A.
      • Hermstad R.
      • Vanvik A.
      • Bratt H.
      Validation of a severity index in female urinary incontinence and its implementation in an epidemiological survey.
      • Antonakos C.L.
      • Miller J.M.
      • Sampselle C.M.
      Indices for studying urinary incontinence function in primiparous women.
      Strength of the LA was evaluated at both time points by measuring the vagina closure force at rest and during maximal pelvic muscle contraction (average of 3 attempts) using an instrumented speculum modified to not be influenced by changes in abdominal pressure.
      • Ashton-Miller J.A.
      • Zielinski R.
      • DeLancey J.O.
      • Miller J.M.
      Validity and reliability of an instrumented speculum designed to minimize the effect of intra-abdominal pressure on the measurement of pelvic floor muscle strength.
      Pelvic organ support was assessed during Valsalva in the lithotomy position using the pelvic organ prolapse quantification system.
      • Bump R.C.
      • Mattiasson A.
      • Bo K.
      • et al.
      The standardization of terminology of female pelvic organ prolapse and pelvic floor dysfunction.
      Demonstrable stress incontinence was documented in the standing position and measures made of volume of urine loss by the quantified paper towel standing stress test.
      • Miller J.M.
      • Ashton-Miller J.A.
      • Delancey J.O.
      Quantification of cough-related urine loss using the paper towel test.
      A urethral pressure profile was obtained at 8 months’ postpartum only, due to its invasive nature. These measures were made by a nurse practitioner with >5 years of experience in clinical examinations. She was blinded to the MRI findings.
      To standardize rehabilitation during the study period, at the examination, the same nurse practitioner instructed each woman in Knack technique and individually prescribed home pelvic muscle exercises per the graduated strength-training protocol.
      • Miller J.
      • Kasper C.
      • Sampselle C.
      Review of muscle physiology with application to pelvic muscle exercise.
      • Miller J.M.
      • Ashton-Miller J.A.
      • DeLancey J.O.
      A pelvic muscle precontraction can reduce cough-related urine loss in selected women with mild SUI.

      Statistical analysis

      Of the 68 women with MRIs at 7 weeks and 8 months’ postpartum, 59 had fluid-sensitive sequences, and the remaining 9 women had only nonfluid-sensitive sequences. Discovery of the importance of these sequences occurred after study initiation. The missing sequences were due to early enrollment before the MSK-MRI protocol was in use. Since LA tear is readily observable without fluid-sensitive sequences, the full 68 women were retained for that analysis, but the 9 were not included in analysis of pubic bone edema, fracture, and LA edema.
      A composite score for the degree of injury for each individual was derived by collapsing “left,” “right” sides to yield ordinal-level data: for the LA tears, a composite score of “0” indicated no or subtle tear on both sides, “1” indicated a low-grade unilateral tear, “2” indicated a bilateral low-grade or unilateral high-grade tear, and a score of “3” indicated a bilateral high-grade tear. Similar composite scores were constructed for pubic bone marrow edema, pubic bone fracture, and LA edema (Table 1, Table 2, Table 3, Table 4).
      Table 1Maternal demographics and birth variables among women with 7 wks and 8 mos’ postpartum magnetic resonance images
      DemographicTotalMean (SD) or frequencyRange or %
      Maternal age, y6830.38 (5.48)19–46
      Maternal age >31 y2740
      Race66
       Black23
       White5888
       Asian35
       Other35
       Non-Hispanic/Non-Latino66100
      Education66
       High school graduate or less69
       Some college1320
       College/technical school graduate1726
       Graduate school2944
      Birth variables
       Infant weight, g673411.90 (507.12)2100–4550
       Infant head circumference, cm6634.19 (1.62)30–38
       Second stage, min67154.91 (126.58)6–518
       Second stage >150 min3146
       Active pushing, min56113.75 (84.65)6–312
       Passive second stage, min5644.45 (72.40)0–307
       Anal tear682232
       Episiotomy681421
       Vacuum6846
       Forceps6823
      Miller. Childbirth muscle/bone injury and recovery. Am J Obstet Gynecol 2015.
      Table 2Postpartum clinical variables among women with 7 wks and 8 mos’ postpartum magnetic resonance images
      Clinical variables ∼8 mo postpartumTotalMean (SD) or frequencyRange or %
      LA resting force on instrumented speculum, newtons621.92 (0.48)1–4
      LA volitional contraction (average of 3 repetitions) on instrumented speculum, newtons624.16 (1.93)1–10
      POP-Q anterior vaginal wall, cm63−2.13 (0.70)−3 to 1
      POP-Q posterior vaginal wall, cm63−2.28 (0.63)−3 to 0
      POP-Q cervix descent, cm62−7.71 (0.60)−8 to −6
      POP-Q genital hiatus, cm634.69 (0.91)2–7
      POP-Q perineal body measure, cm632.29 (0.66)1–4
      POP-Q total vaginal length, cm6211.98 (1.16)9–14
      Maximum urethral pressure, cm H2O5566.95 (19.71)24–128
      Quantified standing stress test63
       No leakage5790
       Drops (<10 cm3)35
       Some leakage (10–11 cm3)00
       A lot of leakage (>33 cm3)35
      Antonakos urinary incontinence (points, 0 = none, 8 = high)643.30 (2.57)0–8
      Sandvik urinary incontinence (points, 0 = none, 8 = high, as frequency multiplied by amount)621.24 (1.10)0–3
      Wexner fecal incontinence (points, 0 = none, 20 = high)641.58 (1.54)0–6
      LA, levator ani; POP-Q, pelvic organ prolapse quantification.
      Miller. Childbirth muscle/bone injury and recovery. Am J Obstet Gynecol 2015.
      Table 3Distribution of 7 wks and 8 mos’ postpartum magnetic resonance imaging scores across 4 outcomes
      VariableMRI score7 wk postpartum, n (%)8 mo postpartum, n (%)n (%) with different score 8 mo postpartumn (%) with same score 8 mo postpartumStuart-Maxwell statistic (P value)
      Pubic bone marrow edema (n = 59)None20 (34)51 (86)0 (0)20 (100)27.2 (< .0001)
      I = Diffuse mild6 (10)1 (2)5 (83)1 (17)
      II = Focal mild or diffuse intense21 (36)5 (8)19 (90)2 (10)
      III = Focal intense12 (20)2 (3)10 (83)2 (17)
      Total59 (100)59 (100)34 (58)25 (42)
      Pubic bone fracture (n = 59)None42 (71)57 (97)0 (0)42 (100)11.2 (.011)
      I = <5 mm unilateral or bilateral5 (8)2 (3)3 (60)2 (40)
      II = ≥5 mm unilateral or bilateral10 (17)0 (0)10 (100)0 (0)
      III = Cortical unilateral or bilateral2 (3)0 (0)2 (100)0 (0)
      Total59 (100)59 (100)15 (25)44 (75)
      Levator ani edema (n = 59)None6 (10)55 (93)0 (0)6 (100)45.1 (< .0001)
      I = Mild unilateral or bilateral2 (3)1 (2)2 (100)0 (0)
      II = Moderate unilateral or bilateral40 (68)3 (5)39 (98)1 (3)
      III = Intense unilateral or bilateral11 (19)0 (0)11 (100)0 (0)
      Total59 (100)59 (100)52 (88)7 (12)
      Levator ani tear (n = 68)None or subtle40 (59)42 (62)0 (0)40 (100)0.74 (.86)
      I = Low-grade (<50%) unilateral8 (12)6 (9)2 (25)6 (75)
      II = Low-grade (<50%) bilateral or high-grade (≥50%) unilateral13 (19)14 (21)0 (0)13 (100)
      III = High-grade (≥50%) bilateral7 (10)6 (9)1 (14)6 (86)
      Total68 (100)68 (100)3 (4)65 (96)
      MRI, magnetic resonance imaging.
      Miller. Childbirth muscle/bone injury and recovery. Am J Obstet Gynecol 2015.
      Table 4Descriptive statistics and time point differences for indicators of pelvic floor disorders by LA tear status at 7 wks and 8 mos’ postpartum
      VariableLA tear severity7 wk postpartum8 mo postpartumANOVA P value
      Repeated measures ANOVA P value from F-test adjusted for time point
      nMean (SD)nMean (SD)
      LA strength
       Force at rest, newtonsNone381.75 (0.34)341.93 (0.53).432
      I81.93 (0.26)81.88 (0.21)
      II91.59 (0.53)131.91 (0.61)
      III61.81 (0.36)71.98 (0.16)
       Force at volitional contraction, newtonsNone383.99 (1.68)344.90 (2.04).008
      I83.19 (2.02)83.51 (1.96)
      II92.46 (0.85)133.09 (1.20)
      III62.82 (1.21)73.29 (0.78)
      Pelvic organ prolapse quantification
       Anterior vaginal wall descent, cmNone39−2.12 (0.64)35−2.19 (0.56).190
      I8−2.19 (0.26)8−2.25 (0.38)
      II12−2.26 (0.48)13−2.08 (0.76)
      III7−1.57 (0.93)7−1.86 (1.35)
       Posterior vaginal wall descent, cmNone39−2.37 (0.60)35−2.33 (0.54).005
      I8−2.56 (0.18)8−2.50 (0.38)
      II12−2.29 (0.45)13−2.31 (0.69)
      III7−1.57 (1.10)7−1.71 (0.95)
       Cervix descent, cmNone39−7.64 (0.79)35−7.66 (0.67).369
      I8−7.88 (0.35)8−7.75 (0.46)
      II12−8.00 (0.00)12−7.88 (0.43)
      III7−7.71 (0.49)7−7.64 (0.63)
       Genital hiatus, cmNone394.51 (0.98)354.70 (0.96).706
      I84.50 (0.60)84.63 (0.52)
      II124.29 (0.84)134.46 (1.05)
      III74.57 (1.06)75.14 (0.75)
       Perineal body, cmNone392.40 (0.65)352.31 (0.69).921
      I82.56 (0.73)82.13 (0.69)
      II122.46 (0.66)132.42 (0.61)
      III72.57 (1.06)72.07 (0.61)
       Total vaginal length, cmNone3911.56 (1.63)3411.96 (1.28).900
      I812.00 (1.16)811.81 (1.46)
      II1211.75 (1.20)1312.19 (0.88)
      III711.36 (0.90)711.93 (0.61)
      Urethral function/incontinence
       Maximum urethral pressure, cm H2O
      Only collected at 8 mo postpartum due to invasive nature of procedure
      None3266.13 (20.89).945
      I665.83 (14.91)
      II1267.67 (16.84)
      III571.80 (27.70)
       Quantified standing stress test, cm3
      Also adjusted for interaction between LA tear severity and evaluation time point (P = .02). P value from F-test including interaction is shown.
      None390.24 (1.51)363.46 (14.76).696
      I827.52 (64.38)80.00 (0.00)
      II120.00 (0.00)133.33 (9.47)
      III77.09 (18.77)60.92 (2.24)
       Antonakos urine leakage (potential 8 points based on “yes = 1” “no = 0” across 8 items)None393.08 (2.51)363.06 (2.48).488
      I84.25 (3.06)84.00 (3.02)
      II133.85 (3.21)134.00 (2.58)
      III73.43 (3.74)72.43 (2.57)
      I816.50 (8.12)815.50 (6.80)
      II1315.85 (7.07)1315.54 (5.59)
      III715.29 (8.58)712.29 (4.92)
       Sandvik urinary incontinence (points)None391.00 (1.19)341.09 (0.97).276
      I82.00 (2.56)81.50 (1.20)
      II132.00 (2.00)131.54 (1.20)
      III71.14 (1.46)71.14 (1.46)
       Wexner fecal incontinence (points)None361.89 (1.91)361.78 (1.64).599
      I72.57 (3.99)81.00 (0.93)
      II132.15 (1.63)131.85 (1.63)
      III73.29 (3.77)70.71 (1.11)
      ANOVA, analysis of variance; LA, levator ani.
      Miller. Childbirth muscle/bone injury and recovery. Am J Obstet Gynecol 2015.
      a Repeated measures ANOVA P value from F-test adjusted for time point
      b Only collected at 8 mo postpartum due to invasive nature of procedure
      c Also adjusted for interaction between LA tear severity and evaluation time point (P = .02). P value from F-test including interaction is shown.
      Descriptive statistics were conducted only for those who completed both MRIs, comparing magnitude levels on 7 weeks and 8 months’ postpartum in the 4 MSK sites. We excluded subjects from analysis when there was missing data due to lack of follow-up or, on select analysis, lack of fluid-sensitive sequences required for a particular variable.
      The Stuart-Maxwell test was used to test for homogeneity between the marginal distributions for each of the 4 sites at the 2 evaluation times. To calculate the statistic, an inconsequential decimal (0.5) was added to each empty cell in the table.
      • Agresti A.
      Categorical data analysis.
      We used repeated measures modeling techniques to investigate the association among the 4 types of MSK injury and the clinical measures. Analyses were performed using SAS, version 9.3 (SAS Institute, Cary, NC) and R, version 2.14.1 (R Foundation for Statistical Computing, Vienna, Austria).

      Results

      Table 1, Table 2 show the obstetric, demographic, and 8 months’ postpartum clinical characteristics of the 68 women analyzed with 7 weeks and 8 months’ postpartum MRI scans (including 9 who had scans without the fluid-sensitive sequences). When compared with the 22 women without a second MRI, the group with scans at both evaluation times (n = 68) was older, more predominately white, and more highly educated. The 2 groups did not differ in terms of obstetric characteristics or distribution of MSK injury severity at 7 weeks’ postpartum. The early MRI scans were obtained on average 47.3 ± 21.0 days' postpartum; the late MRI scans were obtained 242.1 ± 60.8 days postpartum.
      Figure 1 shows one woman’s MRI findings and types of injuries observed and reported by category.
      Figure thumbnail gr1
      Figure 1High-grade bone marrow edema and bilateral LA tears, right greater than left, in 31-year-old patient
      By convention, images are presented in anatomic position and axial images as if viewed from feet. A, Initial magnetic resonance imaging (MRI) with axial short tau inversion recovery (STIR) sequence that demonstrates right pubic bone marrow edema (horizontal arrow). STIR sequence images, such as this one, always appear coarse because of poor spatial resolution inherent in acquisition of these sequences. Although most clinicians will find these images less pleasing to study than more familiar anatomic images, STIR sequences have high sensitivity to sites of edema (edema as bright white contrast) compared with anatomic images. Vertical arrows indicate bilateral LA tears (better seen in B). B, Initial MRI with axial proton density sequence showing bilateral LA tears. Vertical arrows are pointing to region where thick LA muscle should be demonstrated between vagina and internal obturator muscle, but essentially, muscle is missing. Proton density sequences such as this one will always appear with better spatial resolution compared with STIR sequence, but proton density sequences do not reveal bone marrow edema that was seen in STIR sequence of A. C, Follow-up MRI with axial proton density fat saturation sequence that demonstrates almost complete resolution of bone marrow edema. Image sequences of proton density with fat saturation appear less coarse than STIR sequences (in A) but still allow for better visualization of bone marrow edema than proton density-weighted image without fat suppression, shown in D. D, Follow-up MRI with axial proton density without fat saturation sequence showing bilateral LA tears (vertical arrows) unchanged. Arrowheads point to inner margin of muscle site.
      LA, levator ani.
      Miller. Childbirth muscle/bone injury and recovery. Am J Obstet Gynecol 2015.

      Pubic bone marrow edema

      Of the 59 women with complete MSK-MRI studies, 39 of 59 (66%) showed increased signal, indicating edema in the pubic bone marrow at 7 weeks’ postpartum. At 8 months’ postpartum, only 8 of 59 (14%) still showed increased signal (Table 3). Of the 8 women with continued marrow edema, 5 did not show any improvement, while the other 3 who all initially had the highest category of signal intensity, improved by 1 category. For 7 weeks to 8 months’ postpartum, the distribution of women’s signal intensity scores across the 4 magnitude category levels (intense, moderate, mild, no signal intensity) was statistically different (P < .0001), with a strong shift toward lower severity categories at 8 months’ postpartum, indicating resolving marrow edema (Figure 2, A).
      Figure thumbnail gr2
      Figure 2Mean magnetic resonance imaging scores at 2 evaluation times, grouped by 7 wks’ postpartum score
      Subjects were grouped by magnitude level at 7 weeks’ postpartum; magnitude levels were ordered from 0 (none) to III (intense/severe). Each group starts at its group magnitude level because all women within group have same magnitude level at 7 weeks’ postpartum. A, C, and D, Improvement over time as mean scores drop 0 (none). B, Magnitude level shows little improvement in levator ani tear, indicating toward grossly stable muscle tear to 8 months’ postpartum. Edema in levator muscle or in pubic bone marrow shows pattern of resolving over time.
      Miller. Childbirth muscle/bone injury and recovery. Am J Obstet Gynecol 2015.

      Pubic bone fracture

      Fractures in the bone marrow of the pubic bone were observed in 17 of 59 women (29%) on the 7 weeks’ postpartum scans. By 8 months’ postpartum, 2 still showed evidence of healing fractures (Table 3). Both were low grade. Distributions of women’s signal intensity scores across the 4 magnitude category levels of signal intensity compared 7 weeks to 8 months’ postpartum were significantly different (P = .01), indicating overall fracture healing (Figure 2, B).

      LA edema

      LA edema was initially observed in 53 of 59 women (90%) and was still evident in 4 women (7%) on follow-up (Table 3). Of the 4 without complete resolution of LA edema, only 1 did not show any improvement (level II magnitude at both evaluation times), while the other 3 had incomplete resolution. Similar to pubic bone marrow edema, severity for LA edema, compared 7 weeks to 8 months’ postpartum, was significantly different (P < .0001), indicating progress toward full resolution by 8 months’ postpartum. However, LA edema was faster to resolve than bone marrow edema, as only 4 women continued to have some increased signal in the LA at 8 months’ postpartum (Figure 2, C). There was no abnormal signal in the other pelvic muscles (eg, obturator internus) for any of the women, either 7 weeks or 8 months’ postpartum.

      LA discontinuity

      LA discontinuity was seen at 7 weeks’ postpartum in 28 of 68 women (41%). The magnitude of discontinuity for these 28 women was distributed as follows: 8 having unilateral low-grade tears, 13 having bilateral low-grade or unilateral high-grade tears, and 7 having bilateral high-grade tears. When all 68 women were evaluated at 8 months’ postpartum, no new tears were identified, and of the 28 who showed tear at 7 weeks’ postpartum, all but 3 showed the same magnitude level at 8 months’ postpartum (Table 3). Of the 3 who showed a difference, 2 dropped 1 category from unilateral low-grade tear to none-to-subtle tear and 1 dropped from bilateral high-grade tear to the category labeled as bilateral low-grade or unilateral high-grade tear (Figure 2, D). Statistically, there was no difference in the magnitude of the tears 7 weeks to 8 months’ postpartum (P = .86), indicating that tears did not resolve.

      Clinical measures at 8 months

      None of the clinical measures (prolapse, urethral pressure, incontinence, LA strength) obtained were significantly associated with higher magnitude of MRI-documented pubic bone marrow edema, pubic bone fracture, or LA edema injury. LA contraction force and the degree of descent of the posterior vaginal wall were significantly associated with higher magnitude of LA tear (P = .008 and P = .005). None of the fecal or urinary incontinence measures were associated with magnitude of LA tear scores (Table 4).

      Comment

      This study of women with risk factors for LA injury from first childbirth demonstrates that 91% of this selected sample show some form of MSK injury involving the pubic bone or LA when studied with MSK-MRI 7 weeks’ postpartum. Most of the observed injuries resolve by 8 months’ postpartum. LA muscle tears identified 7 weeks after birth in 41% of this selective sample did not resolve. Overall, 9% were high-grade lesions involving >50% of the muscle. In all of those with an LA tear, 89% had the same magnitude of levator injury 8 months’ postpartum, and for those with a change, it was by only 1 severity level.
      We speculate that torn muscle edges retract from their origin because of the significant resting tone,
      • Shafik A.
      • Doss S.
      • Asaad S.
      Etiology of the resting myoelectric activity of the levator ani muscle: physioanatomic study with a new theory.
      so that the resulting large gap prohibits healing that would retain muscle volume.
      • Askling C.
      • Tengvar M.
      • Saartok T.
      • Thorstensson A.
      Acute first-time hamstring strains during high-speed running: a longitudinal study including clinical and magnetic resonance imaging findings.
      • Connell D.
      • Schneider-Kolsky M.
      • Hoving J.
      • et al.
      Longitudinal study comparing sonographic and MRI assessments of acute and healing hamstring injuries.
      • Slavotinek J.
      Muscle injury: the role of imaging in prognostic assignment and monitoring of muscle repair.
      • Sanfilippo J.
      • Silder A.
      • Sherry M.
      • Tuite M.
      • Heiderscheit B.
      Hamstring strength and morphology progression after return to sport from injury.
      Severity of LA muscle tear was associated with degree of reduced LA force developed during a maximal contraction on instrumented speculum testing and with degree of posterior wall descent. There was no association with anterior wall descent, which differs from case-control studies when women were classified by only 2 LA tear categories (major or none) and were older.
      • Laterza R.M.
      • Schrutka L.
      • Umek W.
      • Albrich S.
      • Koelbl H.
      Pelvic floor dysfunction after levator trauma 1-year postpartum: a prospective case-control study.
      • DeLancey J.O.
      • Morgan D.M.
      • Fenner D.E.
      • et al.
      Comparison of levator ani muscle defects and function in women with and without pelvic organ prolapse.
      • Adekanmi O.A.
      • Freeman R.M.
      • Jackson S.A.
      • Puckett M.
      • Bombieri L.
      • Waterfield M.R.
      Do the anatomical defects associated with cystocele affect the outcome of the anterior repair? A clinical and radiological study.
      Figure 3 shows how various degrees of tear do or do not explain various clinical findings.
      Figure thumbnail gr3
      Figure 3Mean values of clinical and questionnaire findings at 7 wks and 8 mos’ postpartum grouped by LA tear severity at 7 wks’ postpartum
      Each panel shows trends over time for variables relating to incontinence (quantified standing stress test; Antonakos, Sandvik, and Wexner), LA force (resting and contraction measured by 1-billed speculum), and POP-Q measures. Most measures do not show meaningful differences for different levels of LA tear severity, except in case of LA contraction force (P = .008) and posterior vaginal wall descent (P = .005).
      LA, levator ani; POP-Q, pelvic organ prolapse quantification; Quant, quantified.
      Miller. Childbirth muscle/bone injury and recovery. Am J Obstet Gynecol 2015.
      Edema within the LA and pubic bone marrow and pubic bone fracture tended to recover. These observations are similar to general MSK-MRI studies where resolution of muscle strains or stress fractures found in athletes (eg, marathoners) resolve over time.
      • Nattiv A.
      • Kennedy G.
      • Barrack M.
      • et al.
      Correlation of MRI grading of bone stress injuries with clinical risk factors and return to play: a 5-year prospective study in collegiate track and field athletes.
      • Datir A.
      • Saini A.
      • Connell A.
      • Saifuddin A.
      Stress-related bone injuries with emphasis on MRI.
      • Kiuru M.
      • Pihlajamaki H.
      • Ahovuo J.
      Fatigue stress injuries of the pelvic bone and proximal femur: evaluation with MRI imaging.
      • Askling C.
      • Tengvar M.
      • Saartok T.
      • Thorstensson A.
      Acute first-time hamstring strains during high-speed running: a longitudinal study including clinical and magnetic resonance imaging findings.
      • Connell D.
      • Schneider-Kolsky M.
      • Hoving J.
      • et al.
      Longitudinal study comparing sonographic and MRI assessments of acute and healing hamstring injuries.
      • Slavotinek J.
      Muscle injury: the role of imaging in prognostic assignment and monitoring of muscle repair.
      • Sanfilippo J.
      • Silder A.
      • Sherry M.
      • Tuite M.
      • Heiderscheit B.
      Hamstring strength and morphology progression after return to sport from injury.
      The most likely explanation for persistence of LA muscle edema in 4 women (7%) at 8 months’ postpartum is that each had a high-grade LA muscle tear. In MSK-MRI studies, the magnitude of muscle and bone injury is proportional to the intensity of signal abnormalities and length of time to heal.
      • Nattiv A.
      • Kennedy G.
      • Barrack M.
      • et al.
      Correlation of MRI grading of bone stress injuries with clinical risk factors and return to play: a 5-year prospective study in collegiate track and field athletes.
      • Datir A.
      • Saini A.
      • Connell A.
      • Saifuddin A.
      Stress-related bone injuries with emphasis on MRI.
      • Kiuru M.
      • Pihlajamaki H.
      • Ahovuo J.
      Fatigue stress injuries of the pelvic bone and proximal femur: evaluation with MRI imaging.
      • Askling C.
      • Tengvar M.
      • Saartok T.
      • Thorstensson A.
      Acute first-time hamstring strains during high-speed running: a longitudinal study including clinical and magnetic resonance imaging findings.
      • Connell D.
      • Schneider-Kolsky M.
      • Hoving J.
      • et al.
      Longitudinal study comparing sonographic and MRI assessments of acute and healing hamstring injuries.
      • Slavotinek J.
      Muscle injury: the role of imaging in prognostic assignment and monitoring of muscle repair.
      • Sanfilippo J.
      • Silder A.
      • Sherry M.
      • Tuite M.
      • Heiderscheit B.
      Hamstring strength and morphology progression after return to sport from injury.
      Urethral pressure and incontinence signs and symptoms, fecal or urinary, were not sensitive indicators of magnitude of injury in any of the MSK aspects studied in the first few months after birth at this sample size. This differs from data reported in 3 studies,
      • Laterza R.M.
      • Schrutka L.
      • Umek W.
      • Albrich S.
      • Koelbl H.
      Pelvic floor dysfunction after levator trauma 1-year postpartum: a prospective case-control study.
      • Brincat C.
      • DeLancey J.O.
      • Miller J.M.
      U rethral closure pressures among primiparous women with and without levator ani muscle defects.
      • Hilde G.
      • Staer-Jensen J.
      • Siafarikas F.
      • Ellström Engh M.
      • Bø K.
      Postpartum pelvic floor muscle training and urinary incontinence: a randomized controlled trial.
      which showed that postpartum women with “major” LA tear, compared with those “without major” LA tear, experienced lower urethral pressures and more incontinence.
      Study limitations include that 22 of the original 90 women evaluated did not return for follow-up visit. The retained women were, on average, older and more frequently white; however, injury severity at 7 weeks' postpartum did not differ between those retained and those who dropped out. However, the radiologists could not be completely blinded to study design and time points, which may have introduced bias toward maximally identifying injuries. It is logical to assume from other, better-understood MSK trauma (eg, hamstring tear and sacral fractures) that symptoms such as degree of pain (which we did not measure in EMRLD) correlate with injury severity, and time needed for healing will vary accordingly.
      • Nattiv A.
      • Kennedy G.
      • Barrack M.
      • et al.
      Correlation of MRI grading of bone stress injuries with clinical risk factors and return to play: a 5-year prospective study in collegiate track and field athletes.
      • Kiuru M.
      • Pihlajamaki H.
      • Ahovuo J.
      Fatigue stress injuries of the pelvic bone and proximal femur: evaluation with MRI imaging.
      • Askling C.
      • Tengvar M.
      • Saartok T.
      • Thorstensson A.
      Acute first-time hamstring strains during high-speed running: a longitudinal study including clinical and magnetic resonance imaging findings.
      • Connell D.
      • Schneider-Kolsky M.
      • Hoving J.
      • et al.
      Longitudinal study comparing sonographic and MRI assessments of acute and healing hamstring injuries.
      • Slavotinek J.
      Muscle injury: the role of imaging in prognostic assignment and monitoring of muscle repair.
      • Sanfilippo J.
      • Silder A.
      • Sherry M.
      • Tuite M.
      • Heiderscheit B.
      Hamstring strength and morphology progression after return to sport from injury.
      • Askling C.
      • Tengvar M.
      • Tarassova O.
      • Thorstensson A.
      Acute hamstring injuries in Swedish elite sprinters and jumpers: a prospective randomized controlled clinical trial comparing two rehabilitation protocols.
      Establishing the most effective rehabilitation protocol and time when activities, eg, high-intensity exercise or sexual intercourse, should occur, will require further study.
      This study’s findings suggest we cannot rely on clinical examination to intuit the full spectrum of MSK issues associated with higher-risk birth. In select women, MSK-MRI may be warranted clinically and in research, since MSK-MRI can provide the full spectrum of MSK injuries. Consideration should be given to including MSK-MRI for evaluation of high-risk symptomatic patients. The role of MSK-MRI in evaluation of postpartum women could be expanded in situations of unexplained or prolonged pain after delivery, nonrecoverable ability to contract the LA (Kegel), or nonresolving postpartum pelvic organ descent. The differential diagnosis will suggest patient care aspects, ie, reassurance of no structural lasting injury, expected timeline of resolution, or follow-up considerations (short- or long-term) for more serious findings.
      The degree to which women with postpartum levator defects and other MSK injuries will eventually develop symptomatic urinary incontinence, fecal incontinence, or chronic pelvic organ prolapse is not known. The longitudinal EMRLD study is continuing with long-term follow-up and will help answer these questions over time.

      Acknowledgments

      The authors acknowledge the EMRLD study staff: Ruta Misiunas, Lee Park, Caroline Garcia, and Meg Tolbert, and all the women participating in EMRLD. Heather Van Doren, MFA, coordinating senior editor with Arbor Research Collaborative for Health, provided editorial assistance on this manuscript. We also gratefully acknowledge James Ashton-Miller as Core B Director of the University of Michigan Specialized Center of Research on Sex and Gender Factors Affecting Women’s Health.

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