Ultrasound measurement of fetal limb bones JOH\J T. Ql;EE:\ AN
CREeORY D. O'BRIE!\ STL',\RT CAYIPBELL London. England A study was made of 41 patients with known menstrual dates in whom the duration of gestation, as
determined by physical examination and ultrasound scan, corresponded \•lith those dates. Examination of the fetal limb lengths was done every 1 to 3 weeks, starting at 8 weeks' gestation. A Kretz Combison 100 ultrasound sector scanner with a 2.5 MHz transducer (velocity = 1,540 meters per second) was used. A freeze frame was used when the full bone length was visualized, and then electronic calipers were employed to measure its full length. Serial measurements of the humerus and femur and the radius-ulna and tibia-fibula complexes were made. The values were expressed as means ± 2 standard deviations for each week of gestation. The growth of the fetal limb bones was linear from 12 through 22 weeks' gestation, but the various bones appeared to grow at different rates. The femur was the first to be well defined and the easiest to measure with reproducibility. All of the limb bone lengths correlate with gestational age and may serve as indicators of skeletal dysplasia. A patient who was delivered of an infant affected with diastrophic
dwaifism syndiome was diagnosed at 16 weeks' gestation to have a fetus affected with this problem. Two other patients whose pregnancies were at risk for skeletal dysplasias were correctly diagnosed to be norma!. (AM. J. 0BSTET. GYNECOL. 138:297, 1980.)
WITH THE ;..;EWER focused real-time ultrasound scanners it is possibie to visuaiize and measure fetai bones accurately in early pregnancy. During this period, the fetus is extremely active, 1 but despite this mobility, the limb bones can be defined in full outline by the usc of real-time scanning and freeze-frame. A standard curve for limb bone measurements in early pregnancy is described, thus providing a new parameter for studying fetal development.
Material and methods
Forty-one pregnant patients were studied. The menstrual dates were known, and the duration of gestation, determined bv physicai examination and uitrasound scan, corresponded with those dates. Examination of the feral limb bones was done every I ro 3 weeks, starting at 8 weeks' gestation. When possible, bilateral measuremems were obtained. From the Department of Obstetrics and Gynecology, King's Colle!ie Hospital. Remvedj(Jr publication April II, I980. Arceptfli May I. I980. Reprint requests: john T. Queenan, M.D., Department of Obs!Rtrirs and Gynecology, Georgetown Unir•ersity School of Medicine, 3800 Resm'oir Road, N. W., Washington, D. C 2000i. 0002-9378/801!902!!7+06$00.60/0
©
19HO The C. V. Mosby Co.
The ultrasound examinations were done with a Kretz Combison 100 sector scanner with the use of a 2.5 MHz transducer (velocity = 1.540 meters per second). A freeze-frame was used when the full fetal limb bone length was visualized, and then electronic calipers were employed to measure its length. Serial measurements of the humerus and temur, and of the radius-ulna and tibia-fibula complexes were made. Each bone had to be examined in snerJ.l planes and from different angles in order to ensure that the ultrasound image of the entire bone had been visuaiized, and that only rhat bone had been mciuded in the measurements. Errors in both directions, shortening or lengthening, were possible if angulation of the transducer took a tangential section of the hone or superimposed adjacent bones. The femur was the earliest to be well defined and was the easiest to measure with excellent rcproducibilitv 2 (Fig. I). Often, the iliac bone would be superimposed. and it was necessary to distinguish this borw so that it would not he included in measurement of the femur. The femur was identified from 8 weeks' gestation and could be measured accurately from LO weeks' gestation. Mild physiologic "bowing" of the femur Vias also observed quite often after 18 weeks' gestation. The tibiafibula ancl the radius-ulna were measured as "com297
October I. l Y80 Am . J. ()b;t~t. Gynecol.
298 Queenan, O'Brien, and Campbell
Fig. 1. Ultrasound scan of a fetal fernur at 22 weeks' gestation
(arrmil.l).
Fig. 2. Ultrasound scan of a fetal humerus at 15 weeks' gestation (arrows). Note the proximity of the scapula (S).
Volume I \H :\ umhcr :~
Ultrasound measurement of fetal lirnb bones
299
Table I. Comparison of ultrasound measurements with x-ray me>asurements, taken to the ne,ttTst mlllimettT. of the limb lengths of aborted fetuses (;!'stational age
!1/
IS I9 20 2:3
Ultrasound
ji'/UI
19 :l2 :l4
wk wk and :1 davs wk and Ida) wk and :1 days
47
20 :13
:H 46
Ultrasound
19 30 32 42
Table II. Femur Arithmetir mean (mm!
II
10.2
1.8
12 1:-1 14 15
12.5
2.4 4.5
lti
14.8 17.9 20.8 24.1
1..,
()k
11
A
4\.J-"1:
18 19 20 21 22
29.4 32.~3
:36.1 3Y.7 42.8
No. of determinations
19 :11 32 40
I :1
2H
15 29
:-Ill
~~1
:\'l
41
:~.7
:3.1 3.6 <)()
"·"' 2.3
3.0 3.8 3.5 3.4
W eek1' !if.llation
--------
.Vo. of
.4n'thmetir mnzn (mm)
II
drtnminatirm 1 l.'i
q
:\.2 :I.H 4 _,-,
15
12 1:\ 14 15 16
9.2 11.1 12.9 16.4 19.8 22.H
1Q HJ
1"7
OA
n
'1 I ,,.r
I5 2I 17 I4 I2
18 19 20 2I 22
27.1 29.5 33.H
:\.0 :Ul
9 15 17 15 20 I6
J I
...:."1".;:7
.u 2.!~
!(j
1:1
IH
I,, '" '"
14
4.ti
]!I 1:-\
:Fi.O
:lA
10
38.7
:I.H
10
Table V. Tibia-fibula
Table III. Humerus Weeks' gestation
Arithmetic mean (mm)
11 12 I:l 14 I5
9.7 12.0 15.1 18.0 20.6
1'-' IU
,4'1:.\J
IH I9 20
17 29 31..') 42
19 32 33 43
l 1/tra.ll!und
Table IV. Radius-ulna
Week,· gntation
li
Ultrasound
ClA 1\
26.0 28.7 :ll.O
21
34.9 36.4
22
40.4
1.5 3.1 5.9 3.4 4.2 Q n .:J,.::;
3.5 2.0 3.9 3.9 4.3 3.6
.Vo. oj
No. of determinations
Weeks' gestatzon
Arithmetic mean (mm)
IO I4 17 13 17
11 I2 1:1 14 15
9.0 Il.I I2.I 14.1 I7.8
·t.l
l.'i
12
llJ
II.::.
Cl/1 ll .::;\},..::,
~.0
u
I I !I
:UI
f:)
II I3 I7 14 12
20 21
23.4 25.2 28.:1 30.7 3:1.9
9
22
:l7.:~
plexes" because it was difficult to measure a single hone. The ulna appeared to be slightly longer than the radius, and, thus, difficult to measure independent of it. The radius-ulna and tibia-fibula complexes were easier to measure in the early stages of pregnancy, but as the gestational age increased, the extreme mobility of these distal hones made difficult the measurement of the full length of the complex. The humerus was the bone most difficult to detine accuratelv, because of its proximitY to the chest wall and its apparent continuity with the ~capula and clavicle (Fig. 2). On each occasion, several measurements were made
17 18 19
dtterminations
2.9 2.9 4.H 2.8 I
6 10 12 10
:1.7
9
49
l:l
2.:)
II li
4.q 4.2
12
on each limb until three doselv corresponding results were obtained within a ~-mm range. An average of the three was then used. Each examination took approximate~\; 15 minutes, although with a ven :u·ti,,e fetus it could take longer. To substantiate the ,·aliditv of our technique. we scanned four patients who were undergoing induced abortion with normal pregnancies at known gestations from 15 to 23 weeks. The period of gestation was confirmed bv ultrasound biparietal diameter, and then measurements of' the limbs were made. Roentgenograms of the aborted fetuses were performed, and
300
Queenan, O'Brien, and Campbell Am.
FEMUR Mean ± 2SD
J.
Octobet 1. l'ltlll Obstet. (;} nen>l.
HUMERUS Mean± 2SD
T
32 E
l:: ,__ <.:>
as
--.)
T
V1
1:[$ IJ
12
14
~
T _ Tl 1
T
l:: >-
"" ~
I.J.J
24t
--.)
20t
_L
_L
T
16t
I
16
I
18 20 GESTATION (weeks)
I
22
ill IU Yll
!2~11 8
12
14
1
1
16
18 20 GESTATION (weeks)
l
22
Fig. 3. Length of femur plotted against weeks of gestation.
Fig. 4. Length of humerus plotted against weeks of gestation.
measurements of bone lengths were made. The ultrasound measurements of the limb bones compared favorably with the limb bone lengths visualized on x-ray films. The comparison of these measurements is illustrated in Table I. In early pregnancy, these fetal limb bones are comprised of a primary ossification center (calcified) plus proximal and distal cartilaginous structures. The roentgenologic examination shows only the ossification center. It appears that ultrasound fetal limb bone lengths correspond to the ossification centers as seen on x-ray films. A subsequent eight cases confirmed the correlation of measurements of the fetal femur by ultrasound and x-ray examination. Generally, the ultrasound measurement was I to 2 mm greater than the x-ray one, perhaps because of beam-width effect and lateral loss of resolution.
As illustrated in Figs. 3 through 6, it appears that the growth of all of the limb bones was linear from 12 weeks' gestation. The different measurements of limb bone length had similar growth curves. The femur had the largest weekly increments (approximately 3 mm per week), and the tibia-fibula had the smallest at 2.5 mm per week. Measurements of the femur had generally the smallest weekly standard deviation, which thus reflects the greater ease of measurement and the better reproducibility.
Results
The measurements of the various limbs grouped according to weeks of gestation are presented in Tables II to V. The weeks of gestation indicate weeks completed from the first day of the last normal menstrual period. The data are presented as the arithmetic mean ± 2 standard deviations. The number of determinations for each week of gestation is also presented.
Comment In 1929, Scammon and Calkins~ published postmortem data after measuring limbs of fetuses between 8 weeks and term. Mahoney and Hobbins" reported data for full arm and leg lengths determined on 22 aborted fetuses. Both of these studies provided data on external measurements, which included bone and soft tissue. To date, there is little information in regard to fetal limb bone lengths in early gestation. The present study establishes ultrasound measurements specifically for fetal limb bone lengths. The measurements ± 2 SD have been determined for the bone lengths of the fetal limbs. These measurements represent the bone lengths for 95% of the normal population and provide the means to study patients who are at risk for skeletal dysplasias.
Ultrasound measurement of fetal limb bones
Volume I ~lH
301
Numher .·1
RADIUS -ULNA
44 1
40~
~ 36~
IJ1 vfl
~·
3t
1
? 2sL ~ ::r: '-
r
471
I
Mean± 2SD
~IBULA
± 2 SO
"
~-
54LI
301-E'
~ 26r-
/" ll ·r
~
l:)
l:) 24!< lJ.J
Mean
l8j
~ ::r:: ..._
~
!
TIBIA-
T
'
..L
.
1I
<: 22~ I
L
llJ
2ol~
r-
16L
141-
~
1 tT sl£!:_.L__l_L_-'---L.._j__.L._j___L__J 12
14 16 18 20 GESTATION (weeks)
22
...L...L .L .1
.L .1. .
14 16 18 7C1 CESfAT/ON (weebl
Fig. 5. Length of radius-ulna complex plotted against weeks of gestation.
Fig. 6. Length of tibia-fibula complex plotted agamst weeks of gestation.
Patients who have a history of a child affected with a specific skeletal dysplasia or multiple congenital malformations can be screened during the second trimester. If a skeletal abnormality is present, it may be detected early enough for termination of pregnancy, if desired. If no skeletal abnormality is present, serial determinations of the fetal limb lengths will monitor the growth of the limbs in order to assure normal development. Subsequent to this study. three patients were examined who were at risk for skeletal dysplasias. In two, the fetuses had normal long bone measurements up to 24 weeks' gestation and were allowed to continue to term. At delivery. the babies were found to have normal limb lengths. The third patient was diagnosed as having a fetus with a limb-reduction deformity. She was a 28year-old Caucasian, gravida 2. para l, whose first child was a diastrophic dwarf. She was referred for ultrasound examination at a menstrual age of 13 weeks and 5 days. The crown-rump length was 43 mm, which corresponded to a gestational age of ll weeks. Three weeks later. an ultrasound examination of the fetal limbs was performed. The difficulty in adequately outlining the limbs at this gestational age suggested an abnormalitv. A femur length of 9 mm was recorded (normal range, 13 to 20 mm). At 1fi weeks' gestation it was possible to obtain a re-
producible femur length measurement o! !3 mm (normal range, 19 to 26 111111). This was well below the expected range for the period of gestation. A diagnosis of dwarfism was made on the basis of markedly shortened femur measurements. Because diastrophic dwarfism syndrome includes varus clubfoot, micrognathia, and cleft palate, fetoscopv was used to determine the degree of fetal malformation. It revealed that the limbs were abnormally short and curved. Fetal features were consistent with a diagnosis of diastrophic dwarfism. After discussion with the patient, the pregnancv was terminated; postmortem examination conhr·med the gross shortening of the long bones, varus deformities. micrognathia, and cleft palate.'; Since the length of the femur can be determined easily, and since the physiologic variation i> relatively small, it may be helpful in establishing the correct gestational age. The growth of the femur is linear from 12 to 22 weeks. It mav be used as an alternative to or in conjunction with the present parameters measured bv ultrasound.
We wish to express our thanks to the Deparlment of Radiology, and to Dr. Driver for pathologic review.
302
Queenan, O'Brien, and Campbell
REFERENCES l. Reinold, E.: Ultrasonics in early pregnancy; diagnostic scanning and fetal motor activity, BaseL 1976, Karger. 2. O'Brien. G. D .. Queenan. J. T .. and Campbell. S. P.: Real time ultrasound measurement of the femur length in the assessment of gestational age. In preparation. :~. O'Brien. G. D., Rodcck, C., and Queenan,]. rr.: Early prenatal diagnosis of diastrophic dwarfism by ultrasound, Br. Med.J. 280:1300, 1980.
October 1. l ~80
Am . .J. Obstet. Gynecol.
·L Scammon, R. E., and Calkins, L. A.: Developmem and
growth of the human body in the fetal period, '\linneapolis, 1929, University of Minnesota Press. :). Mahonev, :\1. 1.. and Hobbins. I. D.: Prenatal dia~rnosis of chondroect7ldermal dysplasi~· (Ellis-van Creveld svndrome) with fetoscopv and ultrasound, l\'. Engl. .f. Med. qQ..,..();'::;, tJ
"-OJf • .o;.,rp,
1(1''7 '7
1·''
1.
Copyright information The appearance of a code at the bottom of the first page of an original article in this JouRNAL indicates the copyright owner's consent that copies of the article may be made for personal or internal use, or for the personal or internal use of specific clients. This consent is given on the condition, however, that the copier pay the stated per copy fee through the Copyright Clearance Center, Inc., 21 Congress St., Salem, Mass. 01970, (617)744-3350, for copying beyond that permitted by Section 107 or 108 of the U.S. Copyright Law. This consent does not extend to other kinds of copying, such as copying for general distribution, for advertising or promotional purposes, for creating new coliective works, or for resaie. For reprint quantities of 50 or more, piease contact Pubiisher.