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Respiratory Physiology & Neurobiology 150 (2006) 233–239

Sexual dimorphism of human ribs


François Bellemare a,∗ , Tambwe Fuamba a,1 , André Bourgeault b
aLaboratoire du Sommeil, Centre Hospitalier de l’Université de Montréal (CHUM) - Hôtel-Dieu,
3840 St.-Urbain, Montréal (Qué.), Canada H2W 1T8
b Laboratoire de Sciences Judicières et de Médecine Légale, 1701 Rue Parthenais, Montréal (Qué.), Canada H2K 3S7

Received 2 December 2004; received in revised form 1 April 2005; accepted 1 April 2005

Abstract

The volume of the rib cage is about 10% smaller in females than in males having the same height although the reason for
this is presently unclear. The cranio–caudal inclination of ribs is greater in females than males but the length of ribs has not
previously been compared between the sexes. In 23 males and 23 females studied at necropsy, body length, the length of the
upper and lower limbs and the length of the thoracic spine were all smaller in females but the ratios of upper and lower limb
lengths to body length and of thoracic spine length to body length were not different. By contrast, the lengths of the third, sixth
and ninth ribs were not significantly different between males and females and the ratios of rib length to body length were all
significantly greater in females. We conclude that in females the ribs grow longer in relation to the axial skeleton than in males.
© 2005 Elsevier B.V. All rights reserved.

Keywords: Chest wall; Gender; Rib cage; Lung volume

1. Introduction has been attributed to a lower rate of alveolar multipli-


cation (Thurlbeck, 1982), although in adults, smaller
Normal prediction equations for lung volume in distending pressure at full active lung inflation may
non-smokers predict values in females that are 10–12% also contribute (Colebatch et al., 1979; Knudson et al.,
smaller than in males who have the same height and 1977).
age (Crapo et al., 1982). The smaller lung volume of Recent studies have shown that not only is there
females is established in the first few years of life and a difference in the volume of lungs between males
and females having the same height, but the volume
of the rib cage is also smaller (Bellemare et al., 2003,
∗ Corresponding author. Tel.: +1 514 890 8000x14730; 2001). The finding of relatively smaller rib cage volume
fax: +1 514 412 7178. in females is surprising since the rib cage contribution
E-mail addresses: bellemaf@colba.net (F. Bellemare), to inspiratory pressure swings is apparently greater and
drjyf1@hotmail.com (T. Fuamba),
andre.bourgeault@msp.gouv.qc.ca (A. Bourgeault).
the contribution of the diaphragm smaller in females
1 Present address: Department of Anatomy, Faculty of Medicine, than males (Bellemare et al., 2003). The reason for
University of Ottawa, Ottawa, Canada the relatively smaller rib cage volume in females than

1569-9048/$ – see front matter © 2005 Elsevier B.V. All rights reserved.
doi:10.1016/j.resp.2005.04.002
234 F. Bellemare et al. / Respiratory Physiology & Neurobiology 150 (2006) 233–239

males is presently unclear. The volume of the rib cage is


determined by the length of ribs and their geometry as
well as by their cranio–caudal inclination relative to the
spine. In a previous study, the cranio–caudal inclination
of ribs was found to be greater in females than males
(Bellemare et al., 2003). However, the length of ribs has
not previously been compared between the sexes. The
primary objective of this investigation, therefore, was
to compare the lengths of ribs in representative groups
of males and females.

2. Methods

2.1. Study population


Fig. 1. Ratio of thoracic spine length/body length.
Studies were conducted in 46 fresh cadavers (23
adult males and 23 adult females). All were cau-
casians less than 60 years of age and 42 were of of the lower limb from the iliac crest to the lateral
French–Canadian descent. Forty-one died by suicide malleolus, with a metric tape.
and five from alcohol intoxication. All were free of tho- Other measures: Height and weight were noted from
racic deformities. Studies were conducted in the Lab- the pathology report.
oratoire de sciences judicières et de médecine légale,
Government of Quebec. 2.3. Statistical analysis

2.2. Measurements Descriptive statistics are reported as mean ± 1S.D.


In addition to the measures just described, the ratios
The following dimensions were measured on the of all dimensions with body length and thoracic spine
right side of the body: length were calculated. As shown in Fig. 1 for the ratio
Length of ribs: The length of the third, sixth and ninth of thoracic spine length to body length, the distribution
ribs was measured with a lead wire 1 mm in diame- of these ratios closely approximate the normal distribu-
ter and molded to fit the internal aspect of each rib. tion. Between group comparisons were carried out us-
Because the ribs were sectioned at thoracotomy, the ing the independent sample t-test or the Mann–Whitney
lengths of the two sections were measured separately U-test, depending on Levene’s test for equality of vari-
and the two measures added to obtain rib length. Mea- ance of the two samples. Linear regression techniques
surements were taken from the cut end of each rib to based on the least square principle were also employed.
the head of the rib on one side, and to the costal car- All statistical computations were conducted with com-
tilage on the other. These limits were marked on the mercially available software (SPPS v10 for Windows,
lead wire with a felt pen, and the inter-marker distance SPSS, Chicago, IL).
was measured with the lead wire laid flat on a ruler.
Length of thoracic spine: The length of the thoracic
spine was measured with the lead wire technique from 3. Results
the superior limit of the first thoracic vertebra to the
base of the 12th. 3.1. Subjects characteristics
Bisacromial distance: The distance between the
acromions was measured with a pelvic caliper. As shown in Table 1, height and weight were sig-
Limb length: The length of the upper limb was mea- nificantly lower in females than in males whereas age
sured from the acromion to the wrist, and the length was comparable.
F. Bellemare et al. / Respiratory Physiology & Neurobiology 150 (2006) 233–239 235

Table 1
Anthropometric characteristics in males and females
Males Females Mann–Whitney U-test
Age (years) 32.35 ± 9.57 35.91 ± 7.52 181
Height (cm) 177.17 ± 8.98 160.22 ± 3.41 24.5***
Weight (kg) 76.46 ± 11.79 53.12 ± 1.55 2***
Values are means ± 1S.D.
*** Significant difference between males and females with p < 0.001.

3.2. Sex differences in linear dimensions limbs and the length of the sixth rib all correlated sig-
nificantly with body length. In most instances, how-
As seen in Table 2, the lengths of the thoracic spine ever, these correlations are dependent on the inclusion
and of the upper and lower limbs as well as bisacromial of male series. When considering female series, we de-
distance were all significantly smaller in females than tected no significant correlation between the lengths of
in males. By contrast, the lengths of the ribs were not ribs and body length, upper and lower limb length or
significantly different. bisacromial distance. It is noteworthy, however, that
the lengths of the third, sixth and ninth ribs were inter-
3.3. Sex differences in bodily proportions correlated with each other, in both male and female se-
ries. The lengths of the upper and lower limbs were sim-
As noted in Table 3, the ratio of bisacromial dis-
ilarly inter-correlated both in male and female series.
tance to body length was significantly greater in males
than in females whereas the ratios of upper and lower
limb length to body length and of thoracic spine length 4. Discussion
to body length were not different. By contrast, the ra-
tios of rib lengths to body length were all significantly This study revealed that females have relatively
greater in females. Similar results were obtained when longer ribs than males and that, in contrast to males,
the lengths of the ribs were reported against thoracic the length of the ribs in females is not significantly re-
spine length rather than body length. lated to the length of the axial skeleton, suggesting that
different factors govern the growth of ribs in males and
3.4. Bivariate correlations between outcome females.
measures
4.1. Critique of the methods
As enumerated in Table 4, for the groups we found
significant correlations between the length of the tho- Rib length constitutes the primary outcome vari-
racic spine and all other variables. In addition, the able. Despite their complex geometry, the ribs on their
bisacromial distance, lengths of the upper and lower internal aspect facing the pleural space present a con-

Table 2
Comparison of bodily dimensions in males and females
Males Females t Mann–Whitney U-test
Thoracic spine (cm) 27.32 ± 1.75 (23.5–30.5) 24.76 ± 1.65 (20.7–28) −5.1*** 76.5***
Upper limba (cm) 61.07 ± 4.94 (52–68) 53.86 ± 2.68 (48–58) 52***
Lower limb (cm) 96.07 ± 5.13 (86–106) 86.34 ± 3.27 (80–91) −7.67*** 27***
Bisacromiala (cm) 39.05 ± 3.66 (33–47) 32.69 ± 1.32 (31–35) 14***
Third rib (cm) 25.73 ± 1.22 (23–27) 26.07 ± 1.42 (24–29) 0.88 230
Sixth rib (cm) 31.73 ± 1.74 (30–35) 30.80 ± 1.54 (27–34) −1.92 190.5
Ninth rib (cm) 28.13 ± .89 (26–29) 28.00 ± 1.29 (25–30) −0.41 258
Values are means ± 1S.D. Values in parentheses are minimums and maximums.
a Variable did not satisfy Levene’s test for equality of variance of the two samples.
*** Significant difference between males and females with p < 0.001.
236 F. Bellemare et al. / Respiratory Physiology & Neurobiology 150 (2006) 233–239

Table 3
Comparisons of bodily proportions between males and females
Num. Deno. Males Females t

Mean S.D. Mean S.D.


TS H 0.154 1.059E−02 0.155 1.085E−02 0.069
BA TS 1.433 0.142 1.327 0.121 −2.734**
H 0.220 1.523E−02 0.204 7.789E−03 −4.555***
Third rib TS 0.944 4.965E−02 1.056 6.779E−02 6.383***
H 0.145 6.819E−03 0.163 8.850E−03 7.456***
Sixth rib TS 1.164 7.125E−02 1.248 9.414E−02 3.419***
H 0.179 1.055E−02 0.192 9.766E−03 4.313***
Ninth rib TS 1.033 5.432E−02 1.134 7.134E−02 5.424***
H 0.159 8.253E−03 0.174 8.035E−03 6.529***
LL TS 3.523 0.174 3.502 0.278 −0.304
H 0.543 2.666E−02 0.539 1.975E−02 −0.547
UL TS 2.238 0.159 2.184 0.184 −1.064
H 0.345 2.210E−02 0.336 1.354E−02 −1.59
Values are group means ± 1S.D. for the ratios of measured lengths (in cm) over thoracic spine length (TS) or body length (H) in cm. Num.,
numerator; deno., denominator; BA, bisacromial distance; third rib, third rib length; sixth rib, sixth rib length; ninth rib, ninth rib length; LL,
lower limb length; UL, upper limb length.
** Denotes a significant difference between males and females at p < 0.01.
*** Denotes a significant difference between males and females at p < 0.001.

tinuous and smooth surface, well delineated on each females. We consider this bias sufficiently small to be
side by the intercostal muscles. Furthermore, when all neglected.
intra-thoracic and intra-abdominal organs are removed, In preliminary experiments, the error associated
as in our study, the head of the ribs is easily identified with the lead wire technique was estimated as the dif-
by displacing the cut end manually. The costo-chondral ference between the predicted and measured lengths
articulation is also easily identified, both visually and of circular arcs having a known diameter of 19.3 and
by palpation. The lead wire technique employed in our 23.5 cm. Measured lengths differed from predicted
study is well suited to measure the length of a curved lengths by 3%. The coefficients of variation for five re-
structure, such as a rib. However, because the skeletons peated measurements of the same rib were in all cases
of males are generally sturdier than those of females, less than 5%. We, therefore, considered the method
this method may have introduced a bias in favour of to be valid. Radiographic techniques have also been
females. Indeed, if the ribs were thicker in males, their employed to measure rib length in humans (Cassart
lengths measured along the inside would be smaller et al., 1996; Dansereau and Stokes, 1988; Guignon et
than their lengths measured along the central axis. al., 1995). In general, the values obtained with these
The thickness of the ribs is a difficult parameter to techniques are comparable to those reported here, but
estimate as it varies continuously along their length a direct comparison would be warranted.
(Roberts and Chen, 1972). In a study of the sternal
end of the fourth rib, Iscan (1985) reported a thickness 4.2. Comparison between males and females
of 8.24 ± 1.17 mm in males and 6.91 ± 1.03 mm in
females, a 1.33 mm difference. Combining these The impetus for this study came from previous
values with the principal radii of curvature of the third, ones in which the radial dimensions of the rib cage and
sixth and ninth ribs reported by Roberts and Chen lungs were shown to be smaller in relation to height
(1972), we estimate that this difference in thickness in females than males (Bellemare et al., 2003, 2001).
would introduce a bias less than 1% in favour of The present study was also motivated by the lack of
F. Bellemare et al. / Respiratory Physiology & Neurobiology 150 (2006) 233–239 237

Table 4
Bivariate correlations between bodily dimensions
BA Third rib Sixth rib Ninth rib LL UL Height
TS
All 0.51** 0.33* 0.45** 0.43** 0.68** 0.63** 0.6**
Males 0.23 0.61** 0.5* 0.62** 0.68** 0.52* 0.38
Females −0.31 0.45* 0.2 0.43* 0.02 0.1 −0.03
BA
All 0.06 0.29* 0.09 0.71** 0.63** 0.85**
Males 0.39 0.15 0.13 0.48* 0.31 0.66**
Females 0.06 0.11 0.01 −0.37 −0.11 0.36
Third rib
All 0.59** 0.8** 0.22 0.16 0.15
Males 0.56** 0.76** 0.73** 0.62** 0.59**
Females 0.78** 0.85** 0.23 −0.03 0.21
Sixth rib
All 0.68** 0.47** 0.26 0.41*
Males 0.6** 0.56** 0.23 0.41
Females 0.81** 0.17 −0.16 0.18
Ninth rib
All 0.32* 0.21 0.21
Males 0.71** 0.49* 0.37
Females 0.16 −0.04 0.24
LL
All 0.8** 0.81**
Males 0.64** 0.6**
Females 0.5* 0.34
UL
All 0.81**
Males 0.62**
Females 0.62**
Values are correlation coefficients with their level of statistical significance. TS, thoracic spinal length; BA, bisacromial distance; third rib, length
of third rib; sixth rib, length of sixth rib; ninth rib, length of ninth rib; LL, length of lower limb; UL, length of upper limb.
* Significant correlation with p < 0.05.
** Significant correlation with p < 0.01.

relevant data in the literature on rib length or growth in As the present study shows, the ribs are longer
humans. Indeed, previous investigations on the growth in relation to height in females than in males. As
of the rib cage have relied on measurements of thoracic mentioned earlier, the size of the lungs, as reflected
dimensions using surface calipers (DeMuth et al., by its volume at a fixed distending pressure in vitro
1965) or chest X-rays (Grivas et al., 1991; Openshaw (Thurlbeck, 1982) or at total lung capacity in vivo
et al., 1984; Scammon, 1927; Simon et al., 1972). (Crapo et al., 1982) is about 25% and 12% smaller, re-
These measurements reflect the growth of the rib cage spectively, in females than in males having the same
only to the extent that the inclination of the ribs is the height. The present findings of longer ribs that are
same in all subjects, a condition, which, as was shown more inclined in females than males (Bellemare et
before (Bellemare et al., 2003), is not satisfied. Failure al., 2003) indicate the potential for a relatively greater
to account for this led to the false impression that the rib cage volume in females than males having the
growth of the rib cage, like that of the lungs, is impaired same height and, also the potential for a greater vol-
in females compared to males of the same standing ume capacity of the rib cage relative to that of the
height (DeMuth et al., 1965; Grivas et al., 1991). lungs.
238 F. Bellemare et al. / Respiratory Physiology & Neurobiology 150 (2006) 233–239

The reason for the sex difference in rib length is should favour a greater rib cage contribution to breath-
unknown. However, other sexual dimorphisms in the ing. Both findings give credence to an old observation
morphology of bones exist that can be linked to func- suggesting that females tend to depend more on costal
tion. As shown in Table 3, bisacrominal distance was breathing than males.
greater in relation to height in males than in females. The rib cage accommodates abdominal volume dis-
This finding is consistent with longer clavicle length placements not only during breathing but also, and per-
in relation to body length in males than in females haps even more importantly, when the abdomen is dis-
(McCormick et al., 1991). This sexual dimorphism tended (D’Angelo et al., 2002; Gilroy et al., 1985). As
may reflect male adaptation for manual labour. There a result of rib cage expansion, the negative effects of
are also well-known differences in the dimensions and abdominal distention on lung volume and abdominal
shape of the pelvis between males and females (Walrath pressure are less than they would otherwise be. If there
and Glantz, 1996). This sexual dimorphism is consid- is a condition that distinguishes females from males it
ered to reflect an adaptation of females for parturition. is abdominal distension caused by pregnancy. The rel-
The functional significance of relatively longer ribs atively longer ribs in females, by allowing a greater rib
and greater rib cage volume capacity relative to the cage expansion, should thus be well-suited to accom-
lungs in females is not immediately clear but may have modate the large abdominal distension that occurs dur-
to do with the dual role of the rib cage in accommo- ing pregnancy, thereby minimising its effects on lung
dating both lung and abdominal volume displacements function and abdominal pressure (Gilroy et al., 1985).
(Mead et al., 1995). Indeed, only part of the rib cage In this way, the sexual dimorphism in human rib length
faces the lung, the other part faces the diaphragm and could be viewed as a female adaptation for pregnancy.
the peritoneal cavity. The latter part, also called ab- The genetic and/or humoral factors involved are un-
dominal rib cage, actually forms part of the abdominal known. Whether this finding can be extended to other
wall and is thus subjected to a pressure close to ab- species or whether this represents an evolutionary adap-
dominal pressure (Loring and Mead, 1982). Mead et al. tation dictated by the relatively large human foetal size
(1995) emphasized the role of the rib cage in accommo- is also unknown.
dating abdominal volume displacements, which they
considered is its major contribution to breathing: as 4.3. Study limitations
the abdominal rib cage expands, it reduces abdomi-
nal pressure and, in this way, increases the inspiratory There was little overlap in height between males and
function of the diaphragm by allowing a greater frac- females. Thus, although our sample is representative of
tion of transdiaphragmatic pressure to be applied to the each gender, caution should be exercised when extrap-
lungs. Because the diaphragm is shorter in relation to olating our results to males and females with the same
height in females than males (Bellemare et al., 2003), height. Furthermore, because of the smaller height vari-
its contribution to breathing can be expected to be less ation in the female group, a relationship between rib
than in males. In fact, gastric pressure swings during length and other bodily dimensions may be more diffi-
inspiration, a measure reflecting abdominal pressure cult to detect than in the male group. Finally, because
changes caused by the descent of diaphragm dome, all subjects were caucasians, the present findings may
was shown to be smaller in females than males. Fur- not be extrapolated to other races.
thermore, the ratio of esophageal pressure to transdi-
aphragmatic pressure swings, a measure reflecting the
relative contribution of inspiratory rib cage muscles 5. Summary
and diaphragm to inspiration (Macklem et al., 1978),
was shown to be greater in females than males, indi- In summary, this study has shown a sexual dimor-
cating an enhanced contribution of inspiratory rib cage phism in human ribs, which are longer in relation to
muscles (Bellemare et al., 2003). The finding of rel- height in females than in males. Furthermore, in con-
atively longer ribs (present finding) that are more in- trast to males, the lengths of the ribs are not significantly
clined in females than in males (Bellemare et al., 2003) correlated with body length. We hypothesise that this
provides an anatomic basis to this observation, as this sexual dimorphism in human ribs may be coupled to
F. Bellemare et al. / Respiratory Physiology & Neurobiology 150 (2006) 233–239 239

that of the pelvis and to the role of the rib cage in Gilroy, R., Lavietes, M., Loring, S., Mangura, B., Mead, J., 1985.
pregnancy. Respiratory mechanical effects of abdominal distension. J. Appl.
Physiol. 58, 1997–2003.
Grivas, T.B., Burwell, R.G., Purdue, M., Webb, J.K., Moulton, A.,
1991. A segmental analysis of thoracic shape in chest radio-
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