Gastrocnemius-Soleus Muscle Tendon Unit Changes Over the First 12 Weeks of Adjusted Age in Infants...

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Gastrocnemius-Soleus Muscle Tendon Unit Changes Over the First 12 Weeks of Adjusted Age in Infants Born Preterm Marybeth Grant-Beuttler, Robert J Palisano, Debra P Miller, Barbara Reddien Wagner, Carolyn B Heriza, Patricia A Shewokis Background and Purpose. Differences in the gastrocnemius-soleus muscle and tendon have been documented shortly after birth in infants born preterm compared with infants born at term. Knowledge of muscle tendon unit lengths at term age to 12 weeks of age in infants born preterm may be useful in understanding motor development. Participants and Method. Gastrocnemius-soleus muscle tendon unit lengths were compared at term age, at 6 weeks of age, and at 12 weeks of age (preterm adjusted age) in 20 infants born full term and 22 infants born preterm. Results. Significant differences were found between the 2 groups on taut tendon, relaxed muscle length (A O ); taut tendon, stretched muscle length (A Max ); and muscle stretch (A O to A Max ). Infants born preterm demonstrated measures of A O and A Max in positions of greater plantar flexion compared with infants born full term. Significant differences in measurements of A O were found between term age and 12 weeks of age, indicating that the tendon lengthens during this period for both groups. Discussion and Conclusion. These results provide knowledge of musculo- skeletal development of the gastrocnemius-soleus muscle and tendon. Differences in musculoskeletal measurements are consistent with uterine confinement in the last weeks of full-term gestation. These findings have implications when examining the musculoskeletal system in infants born preterm who are demonstrating functional changes. For an Invited Commentary and the Author Response, visit www.ptjournal.org. M Grant-Beuttler, PT, PhD, PCS, is Assistant Professor, Depart- ment of Physical Therapy, Chap- man University, One University Dr, Orange, CA 92866 (USA). Address all correspondence to Dr Grant-Beuttler at: beuttler@ chapman.edu. RJ Palisano, PT, ScD, is Professor, Department of Physical Therapy and Rehabilitation Sciences, Drexel University, Philadelphia, Pennsylvania. DP Miller, PT, DPT, is Assistant Di- rector of Clinical Education, De- partment of Physical Therapy, University of Scranton, Scranton, Pennsylvania. B Reddien Wagner, PT, DPT, MHA, is Director of Clinical Education, Department of Physical Therapy, University of Scranton. CB Heriza, PT, EdD, FAPTA, is Pro- fessor, Doctor of Science Program, Pediatric Therapy, Rocky Moun- tain University of Health Profes- sions, Provo, Utah. PA Shewokis, PhD, is Associate Professor, College of Nursing and Health Professions and the School of Biomedical Engineering, Sci- ence and Health Systems, Drexel University. [Grant-Beuttler M, Palisano RJ, Miller DP, et al. Gastrocnemius- soleus muscle tendon unit changes over the first 12 weeks of adjusted age in infants born preterm. Phys Ther. 2009;89:136 –148.] © 2009 American Physical Therapy Association Research Report Post a Rapid Response or find The Bottom Line: www.ptjournal.org 136 f Physical Therapy Volume 89 Number 2 February 2009

Transcript of Gastrocnemius-Soleus Muscle Tendon Unit Changes Over the First 12 Weeks of Adjusted Age in Infants...

Gastrocnemius-Soleus Muscle TendonUnit Changes Over the First 12 Weeksof Adjusted Age in Infants BornPretermMarybeth Grant-Beuttler, Robert J Palisano, Debra P Miller,Barbara Reddien Wagner, Carolyn B Heriza, Patricia A Shewokis

Background and Purpose. Differences in the gastrocnemius-soleus muscleand tendon have been documented shortly after birth in infants born pretermcompared with infants born at term. Knowledge of muscle tendon unit lengths atterm age to 12 weeks of age in infants born preterm may be useful in understandingmotor development.

Participants and Method. Gastrocnemius-soleus muscle tendon unit lengthswere compared at term age, at 6 weeks of age, and at 12 weeks of age (pretermadjusted age) in 20 infants born full term and 22 infants born preterm.

Results. Significant differences were found between the 2 groups on taut tendon,relaxed muscle length (AO); taut tendon, stretched muscle length (AMax); and musclestretch (AO to AMax). Infants born preterm demonstrated measures of AO and AMax inpositions of greater plantar flexion compared with infants born full term. Significantdifferences in measurements of AO were found between term age and 12 weeks ofage, indicating that the tendon lengthens during this period for both groups.

Discussion and Conclusion. These results provide knowledge of musculo-skeletal development of the gastrocnemius-soleus muscle and tendon. Differences inmusculoskeletal measurements are consistent with uterine confinement in the lastweeks of full-term gestation. These findings have implications when examining themusculoskeletal system in infants born preterm who are demonstrating functionalchanges.

For an Invited Commentary and the Author Response,visit www.ptjournal.org.

M Grant-Beuttler, PT, PhD, PCS,is Assistant Professor, Depart-ment of Physical Therapy, Chap-man University, One UniversityDr, Orange, CA 92866 (USA).Address all correspondence to DrGrant-Beuttler at: [email protected].

RJ Palisano, PT, ScD, is Professor,Department of Physical Therapyand Rehabilitation Sciences,Drexel University, Philadelphia,Pennsylvania.

DP Miller, PT, DPT, is Assistant Di-rector of Clinical Education, De-partment of Physical Therapy,University of Scranton, Scranton,Pennsylvania.

B Reddien Wagner, PT, DPT, MHA,is Director of Clinical Education,Department of Physical Therapy,University of Scranton.

CB Heriza, PT, EdD, FAPTA, is Pro-fessor, Doctor of Science Program,Pediatric Therapy, Rocky Moun-tain University of Health Profes-sions, Provo, Utah.

PA Shewokis, PhD, is AssociateProfessor, College of Nursing andHealth Professions and the Schoolof Biomedical Engineering, Sci-ence and Health Systems, DrexelUniversity.

[Grant-Beuttler M, Palisano RJ,Miller DP, et al. Gastrocnemius-soleus muscle tendon unit changesover the first 12 weeks of adjustedage in infants born preterm. PhysTher. 2009;89:136–148.]

© 2009 American Physical TherapyAssociation

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Motor development in infantstraditionally has focused onmaturation of the central ner-

vous system, and less focus has beenplaced on posture of the infant andexamination of the musculoskeletalsystem. Posture in infants born pre-term, both those at low risk andthose at high risk for developmentalissues, is generally characterized bymore extension1,2 and, specifically,by increased trunk extension,3 de-creased elevation of the hips in aprone position,3–5 and lateral (exter-nal) rotation of the hips3–5 comparedwith infants born full term. Pro-longed positioning in extension hasthe potential to alter the musculo-skeletal system over the long term.6–8

Davis and colleagues9 found in-creased lateral rotation range of mo-tion and increased foot angle duringgait in children 3 to 4.5 years of agewho had been born preterm and de-fined as either low risk or high risk.These authors suggested that thesechanges in range of motion at the hipand in gait are related to a “frog-leg”positioning in the neonatal intensivecare unit (NICU).9 Heriza10 exam-ined supine kicking and reportedmore dorsiflexion at peak leg flexionin infants born full term comparedwith infants at low risk born pretermat 40 weeks of gestation. Althoughthe ankle difference was greater than25 degrees, the statistical power ofthis analysis was low and differencesdid not reach significance in thatstudy. The degree of ankle motionduring supine kicking found in in-fants born preterm may potentiallybe explained by changes in muscu-loskeletal system development at theankle.

Posture and positioning observed atbirth have been reported to gradu-ally change as infants at low riskand infants at high risk born pretermapproach term age (40 weeks of ges-tation).3,4,11 Palmer and colleagues2

found that differences in arm recoil,arm traction, and leg recoil, which

were significantly different at birthbetween infants born preterm andinfants born full term, were no longersignificant when the infants bornpreterm reached term age. By termage, infants born preterm demon-strated increased flexion in their pos-ture. These changes in posture werefound to be strongest in infants bornpreterm with higher birth weights,fewer medical interventions, andlater gestational age at birth.2

Harris and colleagues11 suggestedthat, over the first year, ankle dorsi-flexion decreases a mean of 10 de-grees in infants with very low birthweight born before 35 weeks ofgestation. Their findings of increasedextension at the ankle were consis-tent with those of Desmond et al12

and Grenier,13 who suggested thatextension increases during the pe-riod between birth and term age dueto positioning in extension and theforce of gravity on the joints. Infantsborn full term also demonstrated adecrease in dorsiflexion range of mo-tion after birth, perhaps as a conse-quence of gravity.2,14,15 Hoffer14 sug-gested that these changes in range ofmotion at the ankle in infants bornfull term were complete by 3 monthsof age.

Specific changes in the muscle ten-don unit (MTU) as a result of posi-tioning could depend on the age ofthe infants when positioning occursand not necessarily where thesechanges occur, in utero or out ofutero. Tardieu et al6 and Williamsand Goldspink7 documented struc-tural changes in the MTU when pro-longed shortening or lengthening oc-curred differently in very youngversus adult animals.6,7 In very youngrabbits6 and mice,7 tendon lengthen-ing occurred when a muscle was im-mobilized (18–21 days) in either alengthened or shortened position,whereas the number of sacromeresdecreased in both scenarios.6,7 Thesefindings were in contrast to those of

adolescent or adult animals that un-derwent decreased sarcomere num-ber with prolonged immobilizationin a shortened position and in-creased sarcomere number with im-mobilization in a lengthened posi-tion. During the last 4 weeks (28days) of gestation, the human fetus isconfined in a tight uterine space,which decreases the amount of fetalmovement and promotes dorsiflex-ion, putting the gastrocnemius-soleus muscle in a position of pro-longed lengthening.16,17

Tardieu et al18 developed a reliableand valid method of measuring MTUlength and muscle belly stretch in thegastrocnemius-soleus muscle that hasbeen applied to infants born pretermand infants born full term.19 Theirmethod of measuring MTU length re-quires 2 goniometric measures. Thefirst measure, AO, requires palpationof the Achilles tendon while measur-ing the ankle range with the goniom-eter.18 The measurement is recordedat the first point of maximal Achillestendon tension while the muscle isrelaxed. This measure has been sug-gested by Tardieu, et al18 to be thepoint of full tendon lengthening witha relaxed muscle belly. AMax is a mea-sure of full tendon and muscle bellylengthening. This measurement istaken when the muscle and tendonare moved to maximal stretch, thesame way a physical therapist wouldmeasure maximum dorsiflexion atthe ankle.18 Grant-Beuttler et al19

found interrater reliability (intraclasscorrelation coefficient [ICC (2,2)])of .95 to .86 for AMax and .96 to .97for AO and test-retest reliability (ICC[3, 2]) of .91 to .97 for AMax and .97to .98 for AO in infants born pretermand infants born full term.

In previous research using thesemethods of measuring MTU length,Grant-Beuttler and Shewokis20 foundthat when infants born preterm wereexamined soon after birth, they dem-onstrated less maximum dorsiflexion

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compared with infants born fullterm. Twenty infants at low risk bornbetween 26 and 36 weeks of gesta-tion demonstrated a shorter taut ten-don, relaxed muscle length (AO) fol-lowing birth compared with 21infants born full term measuredwithin 48 hours of birth. Althoughdifferences in both AO and AMax

reached significance, muscle bellystretch (AO to AMax) did not reachsignificance. These results suggestthat there is a difference in thegastrocnemius-soleus MTU lengthbetween infants born preterm andinfants born full term. However,MTU length and muscle belly stretchhave not been measured over timeto determine whether differencesfound immediately after birth persistat term age, at 6 weeks of age, orat 12 weeks of age, when the full-term infant’s ankle range of motionstabilizes.

Documenting changes in preterm in-fants at low risk is especially impor-tant secondary to fewer medical is-sues occurring in these infants anddocumentation of motor issues oc-curring at later ages of development.Fewer medical complications andmedical interventions increase thelikelihood that motor differences aredue to preterm birth. In addition,when motor issues are documented,they are found after specific skillshave developed in an infant bornfull term and may not be detectedwith simple observation.21–25 Detect-ing subtle motor changes is chal-lenging and requires sophisticatedsystems used in laboratories.21–25

Subtle motor issues in infants at lowrisk are more likely to be missed dur-ing a standard physical therapy ex-amination and evaluation, especiallyearly in motor development beforeskills have developed. Finding a rel-evant assessment method to detectchanges early will increase the like-lihood that physical therapy willidentify and intervene with subtle is-sues that may persist.

Examination and evaluation of thegastrocnemius-soleus MTU may beimportant to detect differences thatcould alter development of a lower-extremity coordination pattern. Dur-ing supine kicking, a coordinatedlower-extremity movement patternis learned through repetition.10,25,26

This coordinated movement patternwill include increased plantar flexionif the MTU is shortened. As docu-mented by Heriza,10 an infant at lowrisk born preterm may be repeatingmore plantar flexion during kicking.When the infant is developing a newskill, such as walking, this alteredmovement pattern may be used.27

An altered ankle movement patternis consistent with the increased fre-quency of toe-touch foot contactduring walking, as documented byCioni and colleagues.28 The relation-ship between decreased dorsiflexionand persistent toe-walking in infantsborn preterm also is suggested in thework of Georgieff and associates.29

Evaluating the MTU may be useful tophysical therapists for predictingwhich infants born preterm are atrisk for altered ankle movementsduring lower-extremity kicking andactive movement during walking.

The purpose of this study was tocompare passive gastrocnemius-soleusMTU measurements at the ankle ob-tained at birth and at 6 weeks and 12weeks of age between infants bornpreterm and infants born full term toidentify: (1) whether differences inMTU length and muscle belly stretchexist between infants born pretermand infants born full term; (2)whether differences are present inthe tendon or the muscle belly, orboth; and (3) at what ages changes inthe tendon length or the musclebelly, or both, are found. Based onpilot work by Grant-Beuttler andShewokis,20 we hypothesized thatdifferences in the gastrocnemius-soleus MTU would be observed atterm age. Whether differences in theMTU between the infants born pre-

term and the infants born full termare present at 6 weeks of age and at12 weeks of age is less clear. Ferrariet al30 presented evidence that by 12weeks of age, infants at low risk bornpreterm without neurological im-pairment demonstrate extremitymovements that are similar to move-ments observed in infants born fullterm. These observations were basedon “general movement assessment,”and specific lower-limb kinematicswere not measured quantitatively.However, differences in ankle kine-matics and the delay in age of walk-ing that have been reported9,30–32

suggest that differences in gastroc-nemius-soleus MTU length and mus-cle belly stretch may be present at 12weeks after term age.

MethodParticipantsSample size estimates were madeprospectively based on a significancecriterion of .05, a power of .80, andthe lowest meaningful effect size (d)of 1.59 for AO and 1.63 for AMax

using G-power (version 2.0) statisti-cal software.33 Effect size estimatesfor measures of muscle length werebased on data from the pilot study byGrant-Beuttler and Shewokis.20 Asample of 40 infants, with 20 in-fants born preterm and 20 infantsborn full term, was required forthis study’s repeated-measures, lon-gitudinal design.

All infants were recruited to partici-pate while in a hospital setting. Fam-ilies of infants born full term wererecruited from 3 local hospitals. Fam-ilies of infants born preterm wererecruited from NICUs in 2 of the 3local hospitals. The third local hospi-tal did not have an NICU.

Forty-two infants were included inthis study. Twenty infants born fol-lowing full-term gestation of 38 to41 weeks were included in a full-term group. Twenty-two infants bornfollowing premature birth at 26 to 36

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weeks of gestation were included ina preterm group. Data collection ofinfants from preterm births waslarger than the original 20 infantssecondary to inclusion of infantsfrom multiple births. All infants hadnormal newborn examinations, withno orthopedic, genetic, or neurolog-ical impairments.

Gestational age, birth weight, sex,and method of delivery for bothgroups of infants are described inTable 1. Mean gestational age for theinfants born full term was 39 weeks3 days (SD�6.44 days, range�38weeks 2 days–41 weeks 0 days), andmean birth weight was 3,342 g(SD�456.21, range�2,750–4,720).Eleven of the infants born full termwere male, and 9 were female. Fiveof the infants born full term wereborn via cesarian section, and 15were born via normal vaginal deliv-ery. All infants in the full-term groupwere singleton pregnancies.

Mean gestational age for the infantsborn preterm was 32 weeks 3 days(SD�1 week 5.43 days, range�26weeks 3 days–34 weeks 5 days),and mean birth weight was 1,854 g(SD�463.14, range�794–2,608).Fourteen of the infants born pretermwere male, and 8 were female. Four-teen of the infants born pretermwere born via cesarian section, and8 were born by vaginal delivery.Eleven infants born preterm weresingleton pregnancies, 3 infants bornpreterm were a triplet pregnancy,and 8 infants born preterm weretwin pregnancies. The infants in thepreterm group were eligible to par-ticipate in the study if the neonatol-ogist classified them as low risk for amovement disorder. Classification oflow risk included limited time onventilator support, no evidence oforthopedic or genetic impairment,no evidence of neurological compli-cations, and a benign medical courseduring their stay in the NICU. All in-fants born preterm were discharged

with no indication of continuedmedical problems.

Infants born full term were recruitedwithin 2 days of birth. Infants bornpreterm were recruited prior to dis-charge from the NICU. Posters adver-tising the project were present inboth NICUs and the maternity areasin the 3 hospitals. Nurses in all of theareas were aware of the project andprovided with letters for parents thatdescribed the project.

Of the 120 families of infants bornfull term that were contacted by theresearchers, 21 families agreed toparticipate. The family of one infantborn full term dropped out prior todata collection. All other infantsborn full term were measured 3times, with no attrition in the group.

Of the 33 families of infants bornpreterm that were contacted by theresearchers, 18 families (23 infants, 5multiple-birth groups) agreed to par-ticipate. One family could not becontacted to schedule the first ses-sion. The remaining 22 infants in thepreterm group were measured 3times, with no attrition in the group.

InstrumentationA 10.16-cm-diameter (4-in-diameter)goniometer* was used to measureankle range of motion. The goniom-eter had line designations for eachdegree. Dorsiflexion measurementswere documented as positive angles,and plantar-flexion measurementswere documented as negative angles,with a 90-degree angle between thetibia and the lateral foot designatedas a neutral position, or 0 degrees.

ProcedureInformed consent was obtained froma parent prior to data collection,which occurred in the Physical Ther-apy Movement Laboratory at the Uni-

versity of Scranton. Each infant inthe full-term group was scheduledfor data collection within 7 days afterbirth, at 6 weeks, and at 12 weeks.Each infant in the pre-term groupwas scheduled for data collectionwithin 7 days of term age, at 6 weeksadjusted age, and at 12 weeks ad-justed age. Families were offered aride with a professional driving ser-vice to and from the laboratory for all3 visits.

In order to accurately measuregastrocnemius-soleus muscle lengthand muscle belly stretch, the infant’sgastrocnemius-soleus MTU must berelaxed. If the infant was asleepwhen he or she came to the labora-tory, all attempts were made to allowthe infant to continue to sleep. If theinfant was not asleep, all attemptswere made to relax the infant. In anattempt to relax the infant, a parentwas asked to cuddle or swaddle himor her in a blanket. In addition, thelaboratory was kept warm with asmall room heater. All infants weremeasured when in behavioral state 1(deep sleep), state 2 (light sleep), orstate 4 (quiet, alert)34,35 because theywould most likely have relaxed limbsand less movement when in thesestates. If any tension was palpated inthe limb during measurement, thefoot was moved into and out of dor-siflexion and plantar flexion, andmeasurements were delayed untilthe infant relaxed. All infant statesdemonstrated during the measure ofmuscle length are reported in Table2 for both groups. Infants were notmeasured in behavioral state 3(drowsy), 5 (active, alert), or 6 (cry-ing).34,35 If an infant moved into anundesired state, the mother or theresearchers assisted the infant inmoving into a desired state. No in-fants were removed from this studybecause of an inability to get theminto or keep them in the desiredbehavioral state.

* Pro-Med Products, 6445 Powers Ferry Rd,#199, Atlanta, GA 30339.

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Table 1.Sex, Gestational Age, Method of Delivery, and Birth Weight for Infants Born Full Term and Infants Born Preterma

Participant Sex Gestational Age (wk) Method of Delivery Birth Weight (g)

FT-01 M 38 3/7 NVD 3,572

FT-02 M 40 NVD 3,345

FT-03 F 39 NVD 2,862

FT-04 F 38 5/7 NVD 3,402

FT-05 F 40 2/7 NVD 3,615

FT-06 M 40 1/7 NVD 3,062

FT-07 M 39 2/7 NVD 3,827

FT-08 F 39 5/7 NVD 2,750

FT-09 M 40 3/7 NVD 4,026

FT-10 F 40 4/7 NVD 4,720

FT-11 F 38 3/7 C 4,267

FT-12 M 38 2/7 NVD 3,445

FT-13 F 38 3/7 C 3,260

FT-14 M 40 5/7 NVD 3,856

FT-15 M 40 4/7 NVD 4,082

FT-16 M 38 6/7 C 3,118

FT-17 M 38 3/7 C 3,232

FT-18 F 38 6/7 C 3,230

FT-19 M 39 1/7 NVD 3,175

FT-20 F 41 C 3,827

PT-01b F 31 3/7 C 1,191

PT-02b F 31 3/7 C 1,446

PT-03b F 31 3/7 C 794

PT-04 M 32 4/7 NVD 2,410

PT-05 F 32 1/7 C 2,353

PT-06 M 30 4/7 NVD 1,474

PT-07c M 33 3/7 NVD 2,410

PT-08c M 33 3/7 NVD 2,155

PT-09 M 32 3/7 C 1,616

PT-10 M 34 1/7 NVD 2,155

PT-11 M 26 3/7 NVD 1,049

PT-12c M 33 5/7 C 2,126

PT-13c M 33 5/7 C 2,296

PT-14c M 34 1/7 NVD 1,899

PT-15c M 34 1/7 C 2,041

PT-16 M 31 4/7 C 1,588

PT-17c M 32 6/7 C 1,928

PT-18c M 32 6/7 C 1,673

PT-19 F 32 4/7 C 2,070

PT-20 F 31 C 1,219

PT-21 F 34 5/7 NVD 2,608

PT-22 F 33 4/7 C 2,296

a FT�full term, PT�preterm, M�male, F�female, NVD�normal vaginal delivery, C�cesarean section.b Triplet birth.c Twin birth.

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As shown in Table 2, infants in thefull-term group exhibited more sleepstates (states 1 and 2) during theterm measurement period and morealert states (states 4 and 5) by the12-week measurement period. Theinfants in the preterm group dem-onstrated similar trends toward sleepstates in the term measurement pe-riod, and most infants demonstratedalert states in the 12-week measure-ment period. Infants born pretermdemonstrated an ability to regulatetheir states in a manner similar tothat of the infants born full term.This ability of the infants born pre-term to maintain and regulate theirstates is another indication of theirphysiological stability. No infants ineither group demonstrated state 6(crying), and no infant spent morethan brief periods in state 5 (active,alert). Documentation of the states byboth groups of infants suggests thatmeasurement could be completedwhen the infant was in a relaxedstate at all ages.

Each infant’s ankle was passivelymoved through the available rangeof motion before taking measure-ments in an attempt to ensure theinfant was relaxed. Ankle range ofmotion was measured as describedby Norkin and White.36 Figures 1 and

2 illustrate measurement of MTUlength. The first measurement, AO, isthe angle between the foot and theleg when the foot is moved fromplantar flexion to dorsiflexion andthe palpation of the Achilles tendonreveals the first point of maximum

Table 2.Behavioral States Exhibited by Infants Born Full Term (n�20) and Infants Born Preterm (n�22) During Measurement of MuscleLength at Each Age Measureda

Behavioral States

Term Age 6 wk of Age 12 wk of Age

Full-termGroup

PretermGroup

Full-termGroup

PretermGroup

Full-termGroup

PretermGroup

1 1 (5%)

2 2 (10%) 3 (13.5%) 2 (9%) 1 (5%)

4 1 (4.5%) 8 (40%) 10 (46%) 15 (75%) 16 (73%)

1, 2 12 (60%) 12 (55%) 3 (15%) 2 (9%)

1–3 1 (5%) 1 (4.5%)

1, 2, 4 1 (5%)

2, 3 2 (10%) 3 (13.5%) 1 (4.5%)

2, 4 1 (4.5%) 1 (5%)

2–4b 1 (4.5%) 1 (5%) 4 (18%)

2–5 1 (5%)

3, 4 1 (4.5%) 3 (15%) 1 (4.5%) 1 (4.5%)

3–5c 1 (5%) 2 (9%)

4, 5 1 (5%) 2 (10%) 1 (4.5%) 4 (20%) 3 (13.5%)

a Number of infants in each group of behavioral states listed, with percentage of infants in parentheses.b Primarily in behavioral states 2 and 4.c Primarily in behavioral state 4.

Figure 1.Measurement of AO muscle length. The AO goniometric measurement is recorded whenthe Achilles tendon becomes taut. This measure represents slack removed from thetendon, with a relaxed muscle belly.

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tautness (Fig. 1). This measurementreflects the point in ankle rangewhere slack is removed from theAchilles tendon and the muscle bellyof the gastrocnemius-soleus muscleis relaxed. A second measurement,AMax, then was taken after the footwas gently moved into maximumdorsiflexion (Fig. 2). When the footwas moved into maximum dorsiflex-ion, the infant’s behavior was closelymonitored to ensure no discomfortresulted from this movement. Thismeasurement reflected a fully length-ened Achilles tendon and maximalstretch in the muscle belly of thegastrocnemius-soleus muscle. Theknee was positioned into maximumextension during measurement ofboth AO and AMax.

Knee extension limitations can bepresent in newborn infants who aredevelopmentally normal, and havebeen documented as a mean of�15.3 degrees37 to �21.4 degrees.15

Brown and Swenson38 examineddorsiflexion in newborns with kneeextension and knee flexion to 90 de-grees. In girls, dorsiflexion was 60degrees with the knee extendedand 63 degrees with the knee flexed.The difference between dorsiflexionwith and without knee flexion was

57 and 59 degrees, respectively, inboys. Based on the data from Brownand Swenson38 and knowing kneeextension limitation is less than 45degrees, we suggest the change inthe MTU length measures with theknee extended as far as possiblewould be a difference of no morethan half of that found with 90 de-grees of knee flexion,38 or 1 to 1.5degrees. The accepted standard formeasuring ankle range of motion inthe newborn is to extend the knee asfar as possible.11,14,15,37 Applying thisclinical standard to this study al-lowed greater ease in transferring ap-plications into clinical practice.

Each measurement was taken twiceby 2 examiners who were blinded tothe other examiner’s measurements.For each measurement, the infant’sfoot was placed in a plantar-flexedposition, moved toward dorsiflexionfor the measurement of AO, and thenmoved into maximum dorsiflexionfor the measurement of AMax. Thefoot was returned to a plantar-flexedposition, and then the second mea-surements were taken in the samemanner. Only one examiner mea-sured at a time, and the examinersdid not watch each other measure.Each examiner recorded 2 measures

of AO and AMax on a sticky note thatwas added to the research folder foreach infant after measurements werecomplete. If the examiner recorded2 measurements for either AO orAMax that were more than 4 degreesdifferent, a third measurement wastaken, and the examiner recordedthe 2 measurements that were mostsimilar. A third measurement was ob-tained during 15% of the measure-ments for both examiners on eitherAO or AMax. Once the measurementswere complete, each infant wasdressed, and the next session wasscheduled. Blinding of infant gesta-tional age group was not possiblebecause each examiner was able tovisually distinguish among infants ineach group based on experience,particularly at term age. The ICC(2,1) for reliability of AO betweenthe 2 raters on 100 of the 126 mea-surements was .99 (95% confidenceinterval�.98–.99). The ICC (2,1) forreliability of AMax between the 2 rat-ers on 99 of the 126 measurementswas .95 (95% confidence interval�.93–.97).

Data AnalysisData for measurements of AO andAMax were entered into SPSS version12.0.† The 2 measurements of AO

and AMax were averaged after theywere entered into SPSS. If a thirdmeasurement was taken, the 2 mostsimilar measurements were aver-aged. A third variable, muscle bellystretch (AO to AMax), was created bysubtracting the measurement of AO

from the measurement of AMax. Thisvariable represents muscle extensi-bility, the distance the muscle bellyfibers stretched. All 3 values wereentered for each infant at each agemeasured, resulting in 126 measure-ments for each measure of MTUlength.

† SPSS Inc, 233 S Wacker Dr, Chicago, IL60606.

Figure 2.Measurement of AMax muscle length. The AMax goniometric measurement is recordedwhen the muscle belly and the tendon are stretched to their maximum. This measurerepresents slack removed from the tendon and full stretch of the muscle belly.

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Differences between infants bornpreterm and infants born full termfor each of the 3 measures (AO, AMax,and AO to AMax) were analyzed usinga 2 � 3 (term � age), mixed-modelanalysis of variance (ANOVA). In thisstatistical model, the first factor(term) was a between-subjects factorthat was a random effect, and thesecond factor (age) was a within-subjects factor that was a fixed ef-fect. Because 3 separate ANOVAswere performed to analyze thesedata, a Bonferroni adjustment wasmade to the alpha level (.05/3�.0167). Follow-up analysis for maineffects of age was performed usingthe Tukey honestly significant differ-ence test. Effect size for the main ef-fects and interactions in the ANOVAwere reported using partial eta2. Par-tial eta2 represents the amount ofthe measure and error variance thatcan be attributed to term, age, orthe interaction of these main effects.Cohen d effect sizes and 95% confi-dence interval for these effect sizeswere determined for the differencesin means between the full-term in-fants and the preterm infants usingthe Effect Size Calculator.39

Role of Funding SourceThis study was funded by the Ed-ward J. Leahy Center for Faculty Re-search Awards through the Univer-sity of Scranton. The funding fromthis grant provided transportation toand from the laboratory setting forall 3 visits, if agreed to by the family.An approved car seat was providedfor the families to use when usingthe provided transportation. Follow-ing completion of all 3 data collec-tion meetings, each family was givena gift card for a local store that soldvarious newborn items. This fundingsource in no way biased the outcomeof this investigation.

ResultsThe means and standard deviationsfor the 3 measures at term age, 6weeks of age, and 12 weeks of age

are presented in Table 3. Cohen deffect sizes ranged from 0.73 to 6.61(Tab. 3), suggesting differences inthe means between the groups weremedium-large to very large.40 Mea-surements of AO, AMax, and AO toAMax for both groups over all 3 agesare represented in Figures 3 and 4.Differences in MTU length (AO andAMax) and muscle belly stretch (AO toAMax) between infants born pretermand infants born full term were allsignificant (Tab. 4). At term age, 6weeks of age, and 12 weeks of age,infants born preterm demonstratedvalues of AO and AMax in positions ofgreater plantar flexion, with a largerrange of AO to AMax, compared withvalues in infants born full term(Tab. 3). Partial eta2 ranges were ashigh as .90 for AO, suggesting thatfull term versus preterm explained90% of the variability observed in AO

(Tab. 4).

A significant difference in the maineffect of age was found for AO (Tab. 4).As infants aged, the measure of AO wasin a position of more dorsiflexion,

representing an increase in tendonlength. A Tukey honestly significantdifference post hoc analysis revealeda significant difference in AO only be-tween term age and 12 weeks of age.

DiscussionThe results support the hypothesisthat, at term age, infants born pre-term and infants born full term differin gastrocnemius-soleus MTU lengthand muscle belly stretch and thatthese differences persist at 6 weeksand 12 weeks of age. Infants bornpreterm demonstrate less MTUlength with a taut tendon, relaxedmuscle belly (AO), and a taut tendon,stretched muscle belly (AMax) at termage and at 12 weeks of age. The in-creased range of muscle belly stretch(AO to AMax) indicates that the mus-cle belly stretched more in the in-fants born preterm from term ageto 12 weeks of age. Assuming moremuscle belly stretch is primarily theresult of a longer muscle belly withmore sarcomeres or longer sarco-mere length,6,7,18,41 the tendon maybe shorter in the infant born preterm.

Table 3.Mean Values and Standard Deviations (in Degrees) of Muscle Tendon Unit Measuresat Term Age, 6 Weeks of Age, and 12 Weeks of Agea

Measure

Full-term Group(n�20)

Preterm Group(n�22) Cohen d

(95% ConfidenceInterval)X (SD) X (SD)

AO

Term �3.7 (3.1) �17.0 (3.8) 3.82 (2.74–4.75)

6 wk �3.3 (2.0) �14.8 (4.2) 3.44 (2.43–4.32)

12 wk �2.5 (0.8) �14.1 (2.3) 6.61 (4.97–8.00)

AMax

Term 48.0 (3.8) 39.3 (6.0) 1.71 (0.98–2.39)

6 wk 46.5 (3.2) 41.1 (5.7) 1.15 (0.48–1.78)

12 wk 47.4 (3.3) 43.0 (4.7) 1.07 (0.41–1.70)

AO to AMax

Term 51.7 (4.9) 56.3 (7.4) 0.73 (0.09–1.34)

6 wk 49.8 (3.6) 55.9 (5.2) 1.35 (0.66–2.00)

12 wk 49.9 (3.3) 57.1 (5.6) 1.55 (0.83–2.21)

a Plantar flexion is denoted by negative degrees, and dorsiflexion is denoted by positive degrees.AO�taut tendon, relaxed muscle belly; AMax�taut tendon, stretched muscle belly; AO to AMax�musclebelly stretch.

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Figure 3.Measurements of taut tendon, relaxed muscle belly (AO) and taut tendon, stretched muscle belly (AMax) at term age, 6 weeks of age,and 12 weeks of age in infants born full term and infants born preterm. Plantar flexion is represented by negative degrees, anddorsiflexion is represented by positive degrees.

Figure 4.Measurements of muscle belly stretch (taut tendon, relaxed muscle belly [AO] to taut tendon, stretched muscle belly [AMax]) at termage, 6 weeks of age, and 12 weeks of age in infants born full term and infants born preterm.

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Our results suggest that only onemeasure (AO) demonstrated a changeover age. Lengthening of the tendonoccurred in all infants, both pretermand full term, between term ageand 12 weeks of age. This changecould be explained by numerous fac-tors, including decreased knee flex-ion contraction from term age to 12weeks of age, tendon growth, andan MTU adaptation to more kicking.Increased tendon length and de-creased knee flexion contraction arenot convincing explanations be-cause AMax also would have changedfrom term age to 12 weeks of age.42

An increase in range of dorsiflexionmovements between 6 and 9 weeksof age has been reported by Ferrariet al30 and is consistent with the in-crease in tendon length we found inpassive measures. The increase intendon length could be an adaptiveresponse to inertial forces on the an-kle during kicking between term ageand 12 weeks of age.

Group � age interactions were notstatistically significant at a level of.0167 for any of the 3 measures ofthe MTU. However, the interaction

for AMax was .035, which would havebeen accepted as significant if wehad not adjusted our alpha level.These measures are found to move inopposite directions, decreasing inthe full-term group and increasing inthe preterm group, when the meansare examined (Tab. 3), suggestingthat these measures could be movingin different patterns. The patterns ofchanges in MTU over the 3 agesshould be interpreted cautiously dueto a possible type II error. Power isreported in Table 4 and should beexamined when interpreting the re-sults of the statistical analyses andapplying the results.

The results from this study are con-sistent with the findings from ourprevious study.20 As shown in Table5 and Figure 5, our results for AO,AMax, and AO to AMax are very similarand support the reliability of ourdata using the procedure developedby Tardieu and colleagues.18 An un-expected finding was the similaritybetween the preterm infants at birthin our previous study20 and the pre-term infants at term age in the cur-rent study. Although some authors2,4

have reported postural changes frombirth to term age in infants born pre-term, we found no evidence of asimilar change in the gastrocnemius-soleus MTU. Our findings at the an-kle do not correspond with eitherthe assumption that gastrocnemius-soleus MTU changes from birth toterm age as the result of gravity caus-ing more ankle extension12,13 or theassumption that gastrocnemius-soleus MTU changes from birth toterm age as the result of increasedflexor tone causing more ankle flex-ion.2–4 The significant difference inmuscle belly stretch (AO to AMax) be-tween the 2 groups in this study dif-fers from the findings of our previousstudy.20 Post hoc statistical powerfor the previous study’s comparisonof AO to AMax between full-term in-fants and preterm infants was low(.06), suggesting the possibility of atype II error. In this study, we had asimilar number of infants, but mea-surements were repeated 3 times, re-sulting in higher statistical power.

If a goal of therapy is to re-create theMTU length observed in infants bornfull term while intervening with theinfant born preterm, the age windowfor successful therapeutic implemen-tation may be limited. The changeswe found in this study between theinfants born full term, who under-went a prolonged stretch in uteroduring the last 4 to 6 weeks of ges-tation, and the infants born preterm,who did not undergo this prolongedstretch, is the same response Tardieuet al6 and Williams and Goldspink7

found in the animal studies. Our datasuggest that the adaptation of musclein the full-term group results inlengthening of the tendon and short-ening of the muscle belly in compar-ison with the infants born preterm.Because the response in these in-fants is similar to the animal modelfor very young animals, there may bea period where the adaptation tostretch will change and an interven-tion will no longer lead to the same

Table 4.Main Effects for Term, Age, and Interaction on Analyses of Variance for 3 Measuresof the Muscle Tendon Unita

MeasureBetween

Terms Between Ages Interaction

AO F1,40�358.27 F2,39�6.23 F2,39�1.33

P�.001 P�.005 P�.28

Power�1.00 Power�.87 Power�.27

Partial eta2�.90 Partial eta2�.24 Partial eta2�.064

AMax F1,40�30.65 F2,39�2.92 F2,39�3.65

P�.001 P�.066 P�.035

Power�1.00 Power�.54 Power�.56

Partial eta2�.43 Partial eta2�.13 Partial eta2�.14

AO to AMax F1,40�25.20 F2,39�.89 F2,39�.72

P�.001 P�.42 P�.49

Power�1.00 Power�.19 Power�.16

Partial eta2�.39 Partial eta2�.044 Partial eta2�.036

a AO�taut tendon, relaxed muscle belly; AMax�taut tendon, stretched muscle belly; AO toAMax�muscle belly stretch. Power was determined retrospectively.

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adaptive change found in the veryyoung infant, but will switch to theadaptation found in adult animalsand humans. Different responses toimmobilization at different ages sug-gest that intervention to mimic thelengthening in infants born pretermshould occur as soon as possible if itis to be similar to the lengtheningthat occurs in utero in infants bornfull term.

Muscle tendon unit length measuresat the ankle should be used to docu-ment gastrocnemius-soleus musclechanges in infants born pretermfrom birth to term age and beyond.Successful dorsiflexion positioningusing a splint that limits plantarflexion and allows active dorsiflex-ion in the NICU or shortly after dis-charge should result in MTU lengthscloser to those found in the full-termgroup.43,44 The preterm infants in this

study and in our previous study20 didnot receive physical therapy posi-tioning programs in the NICU, so po-sitioning in neutral and dorsiflexedankle positions by a physical thera-pist needs to be explored. This studydoes support the idea that MTUlength and muscle belly stretch canbe used as reliable clinical measures todocument preterm MTU changes inthe NICU and during early interven-tion. In addition, to increase reliabil-ity when performing measurementsof ankle range of motion, therapistsshould repeat each measurementtwice to compare consistency, mon-itor behavioral state during measure-ments, and move the ankle throughthe full available range of motionprior to taking the measurements todecrease creep.

The gastrocnemius-soleus MTU lengthin infants born preterm may poten-

tially affect lower-extremity coordi-nated movement patterns and motorlearning. A shorter gastrocnemius-soleus MTU would lead to move-ment in more plantar flexion duringlower-extremity kicking. Use of alower-extremity kicking pattern withincreased ankle plantar flexion couldexplain, at least partially, ankle plan-tar flexion during supine kicking,10

new walkers’ initial foot contact inplantar flexion (toe touch),28 andpersistent toe walking in preterm in-fants with decreased passive dorsi-flexion.29 This method of measuringgastrocnemius-soleus MTU lengthmay be a quick method available tophysical therapists to predict whichinfants are at continued risk forchanges in learning coordinatedmovement patterns such as kicking,which ultimately could alter the de-velopment of motor skills, such aswalking, at later ages. Research is

Table 5.Means, Standard Deviations, Medians, Interquartile Ranges, and 95% Confidence Intervals (in Degrees) for 3 Measures of theMuscle Tendon Unit in Our Pilot Study20 and the Current Studya

Measure

Full term Preterm

Pilot Study Current Study Pilot Study Current Study

AO

X �6.04 �3.70 �18.05 �17.00

SD 6.92 3.12 8.17 3.77

Median �4.00 �2.75 �16.50 �16.25

Interquartile range 3.50 3.25 7.00 3.63

95% confidence interval �9.20 to �2.90 �5.16 to �2.24 �21.87 to �14.23 �18.67 to �15.33

AMax

X 49.19 48.03 37.85 39.30

SD 4.59 3.78 8.76 6.00

Median 48.00 48.75 40.00 38.75

Interquartile range 7.50 4.38 7.75 9.13

95% confidence interval 47.10 to 51.28 46.26 to 49.79 33.75 to 41.95 36.63 to 41.96

AO to AMax

X 55.24 51.73 55.90 56.30

SD 7.16 4.88 7.85 7.39

Median 54.00 51.00 55.00 56.50

Interquartile range 10.50 6.88 6.50 11.00

95% confidence interval 51.98 to 58.50 49.44 to 54.01 52.22 to 59.58 53.02 to 59.57

a AO�taut tendon, relaxed muscle belly; AMax�taut tendon, stretched muscle belly; AO to AMax�muscle belly stretch.

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146 f Physical Therapy Volume 89 Number 2 February 2009

needed to investigate changes inMTU length at later ages and the ef-fects of these changes on develop-ment of supine kicking, standing,and walking function.

There are limitations in the design ofthis study. In addition to the lack offull knee extension and the inabilityto blind the examiners to the groupsdescribed earlier, another possiblelimitation of the results of this studyis the low statistical power for themain effect of age. Our a prioripower was based on the effect sizesfound in our initial study20 with re-spect to differences between infantsborn preterm and infants born fullterm and not on changes over age.To adequately power a follow-upstudy, a minimum of 40 subjectswould be needed in each of thegroups of infants, or larger age inter-vals could be compared to increasethe likelihood of detecting a differ-ence over age. The lack of signifi-

cance found in this study over ageneeds to be interpreted with cau-tion, considering the possibility of atype II error.

Another limitation of this study is thelack of understanding of MTU lengthmeasures past the age of 12 weeks orin infants born preterm who are notlow risk. It is possible that the MTUissues resolve or continue at olderages and similar changes are found ininfants who are at higher risk fordevelopmental issues. In addition,comparison of the same infants bornpreterm from birth to term agewould be more convincing evidencethat MTU lengths from birth untilterm age did not change during thisperiod.

ConclusionsMuscle tendon unit lengths in thegastrocnemius-soleus muscle are dif-ferent between infants born fullterm and infants born preterm. In-

fants born preterm demonstrateshorter tendon length and shorteroverall tendon length and musclebelly stretch, but more muscle bellystretch. These differences are pres-ent at term age and remain until 12weeks of age (adjusted for the pre-term group). Measurements of MTUlength at term age in this study aresimilar to previous measurementsobtained in preterm infants at birth.These measures can be used reliablyto document changes in the MTUduring an infant’s stay in the NICUand during early intervention follow-up post-discharge. Additional re-search is needed to document theeffects of the MTU lengths on activemovement at these ages and beyond.

Dr Grant-Beuttler and Dr Palisano providedconcept/idea/research design. Dr Grant-Beuttler, Dr Palisano, Dr Heriza, and DrShewokis provided writing. Dr Grant-Beuttler, Dr Miller, and Dr Reddien Wagnerprovided data collection, project manage-

Figure 5.Mean values and 95% confidence intervals for measures of taut tendon, relaxed muscle belly (AO); taut tendon, stretched musclebelly (AMax); muscle belly stretch (AO to AMax) from pilot study20 and current study.

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February 2009 Volume 89 Number 2 Physical Therapy f 147

ment, and participants. All authors provideddata analysis. Dr Grant-Beuttler providedfund procurement and facilities/equipment.

This project was approved by institutionalreview boards at the University of Scranton,Scranton-Temple Residency Program, andDrexel University. It also received approvalfrom the Community Medical Center’s Exec-utive Board.

This research was presented at the Interna-tional Conference for Society for Chaos The-ory in Psychology & Life Sciences; July 27–29, 2007; Orange, California, and as a posterpresentation at the Combined SectionsMeeting of the American Physical TherapyAssociation; February 1–5, 2006; San Diego,California.

This study was funded by an Edward R LeahyJr Center Research Award.

This article was received October 9, 2007, andwas accepted November 8, 2008.

DOI: 10.2522/ptj.20070306

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