oRIgINAL PAPERS

original papers
Adv Clin Exp Med 2012, 21, 2, 143–150
ISSN 1899–5276
© Copyright by Wroclaw Medical University
Michał Szpinda, Anna Szpinda
Normative Growth Data for the External Diameters
of the External and Internal Iliac Arteries in Human
Fetuses – An Anatomical, Digital and Statistical Study
Normatywne dane na temat wzrostu średnic zewnętrznych tętnic
biodrowych zewnętrznych i wewnętrznych u płodów ludzkich – badanie
anatomiczne, cyfrowe i statystyczne
Department of Anatomy, Ludwik Rydygier Collegium Medicum in Bydgoszcz, Nicolaus Copernicus University,
Bydgoszcz, Poland
Abstract
Background. Normative data on the diameters of the aorto-iliac segment are extremely useful in the diagnosis and
monitoring of prenatal arterial variants and pathologies.
Objectives. The present study describes age-specific reference intervals and normal growth curves for the external
diameters of the external and internal iliac arteries.
Material and Methods. Using anatomical dissection and digital-image analysis, the normal growth of the external
diameters of the external and internal iliac arteries was studied in 124 spontaneously aborted human fetuses, aged
15–34 weeks.
Results. Neither sex differences nor laterality differences were found. The external diameters of the external iliac
arteries increased from 0.31 ± 0.06 to 1.41 ± 0.31 mm on the right, and from 0.29 ± 0.04 to 1.37 ± 0.24 mm on the
left, and generated the following growth curves of best fit: y = 0.665 – 0.056 x Age + 0.002 x Age2 ± 0.143 (R2 = 0.82)
and y = 0.612 – 0.052 x Age + 0.002 x Age2 ± 0.118 (R2 = 0.86), respectively. The external diameters of the internal
iliac arteries were found to be statistically larger than those of the external iliac arteries (p = 0.0000). The external
diameters of the internal iliac arteries ranged from 0.44 ± 0.07 to 2.04 ± 0.43 mm on the right, and from 0.44 ±
0.06 to 1.83 ± 0.43 mm on the left, and modeled the following quadratic functions: y = 1.524 – 0.127 x Age + 0.004
x Age2 ± 0.242 (R2 = 0.74), and y = 1.391 – 0.117 x Age + 0.004 x Age2 ± 0.220 (R2 = 0.76), respectively. The right
external iliac arteries (in 71% of the cases) and the right internal iliac arteries (in 65.3% of cases) were larger in
external diameter.
Conclusions. The values of the external diameters of the external and internal iliac arteries are independent of sex.
A strong trend towards higher values for the right external and internal iliac arteries is noted. The external diameter of the internal iliac artery is nearly 1.5 times greater than that of the external iliac artery. Surprisingly, normal
growth of the external diameters of the external and internal iliac arteries follows quadratic functions (Adv Clin
Exp Med 2012, 21, 2, 143–150).
Key words: external diameter, external iliac artery, internal iliac artery, human fetuses, quadratic regression.
Streszczenie
Wprowadzenie. Dane normatywne dotyczące średnic segmentu aortalno-biodrowego są bardzo użyteczne w rozpoznaniu i monitorowaniu wariantów i patologii tętnic w okresie prenatalnym.
Cel pracy. Praca ta opisuje specyficzne dla wieku przedziały wartości i krzywe normalnego wzrostu średnic
zewnętrznych tętnic biodrowych zewnętrznych i wewnętrznych.
Materiał i metody. Za pomocą dysekcji anatomicznej i cyfrowej analizy obrazu zbadano prawidłowy wzrost średnic zewnętrznych tętnic biodrowych zewnętrznych i wewnętrznych u 124 płodów człowieka pochodzących z poronień samoistnych i porodów przedwczesnych.
Wyniki. Nie stwierdzono różnic związanych z płcią płodu i stroną ciała (P > 0,05). Średnice zewnętrzne tętnic
biodrowych zewnętrznych wzrastały od 0,31 ± 0,06 do 1,41 ± 0,31 mm po stronie prawej i od 0,29 ± 0,04 do 1,37 ±
0,24 mm po stronie lewej, generując krzywe wzrostu o najlepszym dopasowaniu odpowiednio: y = 0,665 – 0,056 x
144
M. Szpinda, A. Szpinda
Wiek + 0,002 x Wiek2 ± 0,143 (R2 = 0,82) i y = 0,612 – 0,052 x Wiek + 0,002 x Wiek2 ± 0,118 (R2 = 0,86). Średnice
zewnętrzne tętnic biodrowych wewnętrznych były istotnie większe (P = 0,0000) niż tętnic biodrowych zewnętrznych. Średnice zewnętrzne tętnic biodrowych wewnętrznych wahały się od 0,44 ± 0,07 do 2,04 ± 0,43 mm po stronie
prawej i od 0,44 ± 0,06 do 1,83 ± 0,43 mm po stronie lewej, generując odpowiednio następujące funkcje kwadratowe: y = 1,524 – 0,127 x Wiek + 0,004 x Wiek2 ± 0,242 (R2 = 0,74) i y = 1,391 – 0,117 x Wiek + 0,004 x Wiek2 ± 0,220
(R2 = 0,76). Tętnice biodrowe wewnętrzne (65,3%) i zewnętrzne (71%) były silniejsze po stronie prawej.
Wniosek. Wartości średnic zewnętrznych tętnic biodrowych zewnętrznych i wewnętrznych nie zależą od płci.
Obserwuje się silny trend w kierunku większych wartości prawych tętnic biodrowych zewnętrznych i wewnętrznych. Średnica zewnętrzna tętnicy biodrowej wewnętrznej jest ok. 1,5 raza większa niż tętnicy biodrowej zewnętrznej. Prawidłowy wzrost średnic zewnętrznych tętnic biodrowych zewnętrznych i wewnętrznych następuje niespodziewanie zgodnie z funkcją kwadratową (Adv Clin Exp Med 2012, 21, 2, 143–150).
Słowa kluczowe: średnica zewnętrzna, tętnica biodrowa zewnętrzna, tętnica biodrowa wewnętrzna, płody człowieka, regresja kwadratowa.
It has been reported that the diameters of the
human aorto-iliac segment increase quasi-linearly
during gestation [1–11]. However, the current authors’ studies on the common iliac arteries [12] indicate that the external diameters increase in a quadratic fashion rather than growing proportionally.
To date, neither anatomical studies nor Doppler
ultrasonographic studies of normal growth curves
for the external and internal iliac arteries have been
reported in the medical literature.
Thus, the objectives of the present study were
to establish the following:
−− age-specific reference intervals for the
external diameters of the external and internal iliac
arteries;
−− normal growth curves for each external
diameter studied; and
−− the influence of sex and laterality (left-right)
on the value of the external diameters examined.
As described in a previous article [11], the arterial bed was filled with white latex LBS 3060 through
a catheter Stericath (diameter of 0.5–1 mm), introduced by lumbar access into the abdominal aorta.
The arterial bed filling was performed under controlled pressure of 50–60 mm Hg, using a SEP 11S
syringe infusion pump (Ascor, Warsaw, Poland).
All specimens were immersed in 10% neutral formalin solution for 4–24 months for fixation, and
then dissected at a magnification of 10 using a stereoscope with a Huygens ocular. Each fetus was
dissected to expose its aorto-iliac segment. In situ,
the common, external and internal iliac arteries
were placed with a millimeter scale perpendicular
to the optical lens axis, and then recorded using
a Nikon Coolpix 8400 camera, digitalized to TIFF
images (Fig. 1) and evaluated by a digital image-
Material and Methods
The examinations were carried out on 124
human fetuses of Caucasian origin of both sexes
(60 males, 64 females) derived from spontaneous
abortions or stillbirths, as described in a previously published paper [11]. The legal and ethical
aspects of the study were approved by the Nicolaus
Copernicus University Research Ethic Committee
(KB/217/2006). The sample was comprised of fetuses that were the outcome of intra-uterine growth
restriction; the fetuses had no visible cardiovascular anomalies. The fetal ages, which ranged from 15
to 34 weeks of gestation (Table 1), were accurately
established on the basis of the following criteria: 1)
the gestational age, based on measurements of the
crown-rump length [13]; 2) the date of the beginning of the last maternal menstrual period; and 3)
a combination of abdominal circumference, femur
length and biparietal diameter, ascertained in early
second-trimester ultrasound scans.
Fig. 1. The abdominal aorta and iliac arteries in
a female fetus aged 24 weeks: B – aortic bifurcation,
1 – abdominal aorta, 2 – right common iliac artery,
3 – left common iliac artery, 4 – right external iliac
artery, 5 – right internal iliac artery, 6 – left external
iliac artery, 7 – left internal iliac artery
Ryc. 1. Aorta brzuszna i tętnice biodrowe u płodu płci
żeńskiej w wieku 24 tygodni. B – rozdwojenie aorty,
1 – aorta brzuszna, 2 – tętnica biodrowa wspólna
prawa, 3 – tętnica biodrowa wspólna lewa, 4 – tętnica
biodrowa zewnętrzna prawa, 5 – tętnica biodrowa
wewnętrzna prawa, 6 – tętnica biodrowa zewnętrzna
lewa, 7 – tętnica biodrowa wewnętrzna lewa
145
Fetal Internal and External Iliac Arteries
Table 1. Distribution of the fetuses studied
Tabela 1. Liczebność badanych płodów
Fetal age (Wiek płodowy)
Months
(Miesiące)
4
5
6
7
8
9
weeks
(Hbd-life)
Crown-rump length
(Długość ciemieniowo-siedzeniowa )
mm
Number
(Liczba)
Sex (Płeć)
male
female
mean
SD
min
max
15
89.4
6.1
85.0
92.0
9
4
5
16
103.7
6.1
95.0
106.0
7
3
4
17
114.9
8.2
111.0
121.0
5
3
2
18
129.3
6.6
124.0
134.0
8
3
5
19
142.7
7.7
139.0
148.0
9
5
4
20
155.3
5.8
153.0
161.0
2
0
2
21
167.1
4.7
165.0
173.0
3
2
1
22
178.1
6.9
176.0
186.0
7
4
3
23
192.3
6.3
187.0
196.0
9
4
5
24
202.9
5.7
199.0
207.0
11
6
5
25
215.2
4.8
211.0
218.0
7
5
2
26
224.7
5.2
220.0
227.0
7
4
3
27
234.1
4.3
231.0
237.0
4
0
4
28
244.2
5.1
240.0
246.0
4
2
2
29
253.8
4.5
249.0
255.0
6
1
5
30
262.7
3.1
260.0
264.0
6
3
3
31
270.7
5.2
268.0
275.0
4
1
3
32
281.4
3.7
279.0
284.0
5
4
1
33
290.3
6.1
286.0
293.0
7
4
3
34
301.4
3.2
296.0
302.0
4
2
2
124
60
64
Total (Suma)
analysis system (Leica QWin Pro 16, Cambridge,
UK), which semi-automatically estimated the external diameters of the external and internal iliac
arteries. Diameter measurements were derived by
assuming that the filled iliac arteries were circular
in cross section.
For each fetus the four following external diameters were evaluated:
1, 2: external diameters of the right and left external iliac arteries, measured at their origins; and
3, 4: external diameters of the right and left internal iliac arteries, measured at their origins.
In order to minimize measurement and observer bias, all the measurements were performed
by one researcher. Each measurement was repeated three times under the same conditions but at
different times, and the mean of the three mea-
surements was then used. The differences between
the repeated measurements, as well as the intraobserver variation, were evaluated by the Wilcoxon signed-rank test.
The values of the external diameters were
correlated to fetal age in weeks in order to clarify
their normative growth. The results obtained were
assessed by a one-way ANOVA test for unpaired
data and a post hoc RIR Tukey test. Regression
analysis was used to derive the growth curves of
the best fit for the plot for each external diameter
against gestational age. Coefficients of determination (R2) between particular external diameters
and fetal age were calculated. Results were considered significant at p < 0.05.
146
M. Szpinda, A. Szpinda
Table 2. External diameters of the external and internal iliac arteries related to fetal age
Tabela 2. Średnice zewnętrzne tętnic biodrowych zewnętrznych i wewnętrznych w zależności od wieku płodowego
Fetal age
– weeks
(Wiek płodowy
– tygodnie)
n = 124
External diameters – mm
(Średnice zewnętrzne – mm)
external iliac artery
right
internal iliac artery
left
right
left
mean
średnia
SD
mean
średnia
SD
mean
średnia
SD
mean
średnia
SD
15
9
0.31
0.06
0.29
0.04
0.44
0.07
0.44
0.06
16
7
0.39
0.10
0.34
0.06
0.62
0.16
0.57
0.18
17
5
0.32
0.05
0.33
0.05
0.53
0.08
0.44
0.06
18
8
0.34
0.05
0.32
0.03
0.47
0.11
0.45
0.08
19
9
0.45
0.09
0.41
0.08
0.65
0.19
0.58
0.13
20
2
0.56
0.02
0.50
0.01
0.97
0.18
0.73
0.04
21
3
0.44
0.06
0.44
0.03
0.53
0.13
0.51
0.12
22
7
0.56
0.12
0.55
0.11
0.75
0.17
0.74
0.14
23
9
0.49
0.06
0.48
0.05
0.68
0.10
0.64
0.08
24
11
0.58
0.10
0.52
0.10
0.84
0.28
0.73
0.16
25
7
0.68
0.12
0.65
0.14
0.78
0.09
0.83
0.15
26
7
0.68
0.10
0.70
0.15
0.82
0.13
0.82
0.17
27
4
0.94
0.22
0.82
0.22
1.31
0.32
1.14
0.32
28
4
0.85
0.09
0.77
0.09
1.04
0.18
1.07
0.20
29
6
0.98
0.18
0.95
0.19
1.26
0.33
1.13
0.18
30
6
1.07
0.22
0.94
0.12
1.36
0.23
1.33
0.31
31
4
0.96
0.07
0.98
0.11
1.29
0.12
1.17
0.12
32
5
1.19
0.32
1.10
0.15
1.69
0.50
1.68
0.53
33
7
1.20
0.20
1.12
0.16
1.61
0.38
1.56
0.41
34
4
1.41
0.31
1.37
0.24
2.04
0.43
1.83
0.43
Results
No significant differences were found in the
evaluation of intra-observer reproducibility of the
measurements of the iliac arteries studied. Interobserver variability was not assessed because all
the measurements were carried out by the same
observer.
The results obtained are presented in Table 2
and Figures 2–5. The statistical analysis of the diameters studied showed no sex differences, so the
results are presented in Table 2 irrespective of sex.
Although the right-left differences for the
whole group were not found to be statistically significant, the results for the right and left iliac arteries are presented separately, because of their great
inter-individual variability (Table 2) and a strong
trend towards higher values on the right side.
The values for external diameters of the external iliac arteries increased from 0.31 ± 0.06
to 1.41 ± 0.31 mm on the right side, and from
0.29 ± 0.04 to 1.37 ± 0.24 mm on the left side for
fetuses at the ages of 15 and 34 weeks, respectively. At first, linear patterns were generated as follows: y = –0.572 + 0.052 x Age + 0.159 (R2 = 0.78;
p = 0.0000) for the right external iliac artery,
and y = –0.553 + 0.050 x Age ± 0.135 (R2 = 0.72;
p = 0.0000) for the left external iliac artery. However, after several transformations it turned out that
quadratic regressions were much better than other
models, because the values of their coefficients of
determination attained relatively greater values:
147
Fetal Internal and External Iliac Arteries
Fig. 2. Quadratic regression for the
external diameter of the right external
iliac artery
Ryc. 2. Regresja kwadratowa dla
średnicy zewnętrznej tętnicy biodrowej zewnętrznej prawej
Fig. 3. Quadratic regression for the
external diameter of the left external
iliac artery
Ryc. 3. Regresja kwadratowa dla
średnicy zewnętrznej tętnicy biodrowej zewnętrznej lewej
Fig. 4. Quadratic regression for the
external diameter of the right internal
iliac artery
Ryc. 4. Regresja kwadratowa dla
średnicy zewnętrznej tętnicy biodrowej wewnętrznej prawej
148
M. Szpinda, A. Szpinda
Fig. 5. Quadratic regression for the
external diameter of the left internal
iliac artery
Ryc. 5. Regresja kwadratowa dla
średnicy zewnętrznej tętnicy biodrowej wewnętrznej lewej
0.82 and 0.86 respectively. Thus, the numerical
data showed that external diameters of the right
and left external iliac arteries modeled the growth
curves of best fit as: y = 0.665 – 0.056 x Age + 0.002
x Age2 ± 0.143 (R2 = 0.82) – (Fig. 2) and y = 0.612
– 0.052 x Age + 0.002 x Age2 ± 0.118 (R2 = 0.86)
– (Fig. 3), respectively. In 71% of individuals the
external diameter of the external iliac artery was
found to be larger on the right side.
In the material under examination, the external diameters of the internal iliac arteries were
found to be statistically larger (p = 0.0000) than
those of the external iliac arteries. The external diameters of the internal iliac arteries varied from
0.44 ± 0.07 to 2.04 ± 0.43 mm on the right, and
from 0.44 ± 0.06 to 1.83 ± 0.43 mm on the left in
fetuses at the ages of 15 and 34 weeks. The linear
models for their growth were: y = –0.685 + 0.067 x
Age ± 0.271 (R2 = 0.67; p = 0.0000) and y = – 0.676
+ 0.065 x Age ± 0.248 (R2 = 0.69; p = 0.0000) for
the right and left internal iliac arteries, respectively. However, the relationships between their external diameters and fetal age were much better expressed by the quadratic models: y = 1.524 – 0.127
x Age + 0.004 x Age2 ± 0.242 (R2 = 0.74) for the
right internal iliac artery (Fig. 4), and y = 1.391 –
0.117 x Age + 0.004 x Age2 ± 0.220 (R2 = 0.76) for
the left internal iliac artery (Fig. 5). In 65.3% of the
specimens the right internal iliac artery was found
to be larger in diameter.
Discussion
The present study describes the normative
growth of external diameters of the external and
internal iliac arteries in human fetuses. Because the
specimens had been fixed in neutral buffered formalin for 12–24 months before quantitative analysis, all
the measurements were taken in situ to minimize,
as much as possible, tissue shrinkage related to formalin fixation. Such shrinkage had little influence
on the measurements of the filled iliac arteries in
situ, the wall of which was mainly composed of elastic connective tissue. Similarly, in an earlier study
one of the authors found only 0.5–1.0% shrinkage
in situ in major fetal elastic arteries that had been
filled with latex and then immersed in 10% neutral
buffered formalin solution for 1–2 years [14].
Reference data for external diameters of the
internal and external iliac arteries in human fetuses is scarce [11, 15]. Moreover, in the available
literature prior to this study there is no information expressed by precise mathematical models
concerning the normal growth of the external diameters of the internal and external iliac arteries
during gestation. Therefore, in this study, a digital
image-analysis system was used to provide completely novel data on an increase in the external
diameters of developing external and internal iliac
arteries at gestational ages ranging from 15 to 34
weeks.
The measurements were similar in both sexes,
in keeping with other authors in relation to the
iliac [11, 12, 15] and other fetal arteries [1–10, 16,
17]. However, significant sex differences in arterial diameter arise as late as during the postnatal
period, when the arterial diameters are found to be
larger in males [18–21].
Normal age-specific reference intervals for external diameters of the external iliac arteries were
constructed as follows: from 0.31 ± 0.06 to 1.41 ±
0.31 mm on the right, and from 0.29 ± 0.04 to 1.37
± 0.24 mm on the left for the fetuses aged 15 and
Fetal Internal and External Iliac Arteries
34 weeks, respectively. According to Özgüner and
Sulak, values for the diameter of the external iliac
artery were consistently greater on the right side,
but without significant differences: 0.44 ± 0.07 mm
versus 0.44 ± 0.07 mm in the first trimester, 0.81
± 0.1 mm versus 0.79 ± 0.1 mm in the second trimester, 1.39 ± 0.2 mm versus 1.35 ± 0.2 mm in the
third trimester, and 2.36 ± 0.2 mm versus 2.29 ±
0.2 mm at full term [15].
Surprisingly, the results of the present study
show that the normal growth of the external iliac
arteries follows quadratic functions. The authors
proved that the best fit correlation between the
diameter of the external iliac artery and the gestational age was a parabola defined by the quadratic
regressions y = 0.665 – 0.056 x Age + 0.002 x Age2
± 0.143 (R2 = 0.82) on the right, and y = 0.612 –
0.052 x Age + 0.002 x Age2 ± 0.118 (R2 = 0.86) on
the left.
In the material under examination, the values
for the diameter of the internal iliac artery were
found to range from 0.44 ± 0.07 to 2.04 ± 0.43 mm
on the right, and from 0.44 ± 0.06 to 1.83 ± 0.43
mm on the left. Thus, the present results are in
close accordance with the findings of Özgüner and
Sulak [15]. In their material, the external diameters
of the right and left internal iliac arteries were respectively: 0.68 ± 0.1 mm versus 0.61 ± 0.1 mm in
the first trimester, 1.30 ± 0.3 mm versus 1.33 ± 0.3
mm in the second trimester, 2.37 ± 0.4 mm versus
2.29 ± 0.4 mm in the third trimester, and 3.63 ± 0.4
149
mm versus 3.57 ± 0.4 mm at the full term, but with
no significant laterality differences.
The normal increase in external diameter of the
internal iliac arteries was expressed by the quadratic functions y = 1.524 – 0.127 x Age + 0.004 x Age2
± 0.242 (R2 = 0.74) on the right side, and y = 1.391
– 0.117 x Age + 0.004 x Age2 ± 0.220 (R2 = 0.76) on
the left side. These findings indicate that in human
fetuses, in contrast to adults, the external diameter of the internal iliac artery was nearly 1.5 times
larger than that of the external iliac artery, which
concurs with Özgüner and Sulak [15].
The current authors believe that a particular
strength of this study is the large number (n = 124)
of normal fetuses used to generate the growth
curves. It is noteworthy that the growth curves obtained in the study are completely new; they can
serve as a database for in utero examination of the
iliac arteries, and can be helpful in the prenatal diagnosis and monitoring of abnormalities and pathologies of the fetal iliac arteries.
The authors concluded that the values for the
external diameters of the external and internal iliac
arteries are independent of sex. A strong trend
has been found towards higher values of the right
external and internal iliac arteries. The external
diameter of the internal iliac artery is nearly 1.5
times larger than that of the external iliac artery.
Surprisingly, the normal growth of the external
diameters of the external and internal iliac arteries
follows quadratic functions.
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Address for correspondence:
Michał Szpinda
Department of Anatomy
Ludwik Rydygier Collegium Medicum in Bydgoszcz
Karłowicza 24
85-092 Bydgoszcz
Poland
Tel.: +48 52 585 37 05
E-mail: [email protected]
Conflict of interest: None declared
Received: 19.08.2011
Revised: 26.09.2011
Accepted: 29.03.2012