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1 s2.0 S1530891X20481868 Main
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Rutie Mamlok Sherf, MD1; Dror Cantrell, MD2,3; Karen Or, MD1,2;
Efrat Marcus, MD2; Alex Shapira, MD4; Carlos Benbassat, MD2,5;
Sophia Ish-Shalom, MD6; Ronit Koren, MD2,5
Copyright © 2020 AACE ENDOCRINE PRACTICE Vol 26 No. 11 November 2020 1277
1278 Bone Fragility and Poliomyelitis, Endocr Pract. 2020;26(No. 11) Copyright © 2020 AACE
bariatric surgery).
first fracture was 57 years. The rate of recurrent falls was
BMD and Osteoporosis in 39.2%, and up to 62.8% of PPS patients with recurrent falls
Post-Poliomyelitis Patients sustained at least one fracture. From the 82 patients expe-
BMD was evaluated in only 25.8% of our cohort. In riencing bone fractures, the affected limb was the fracture
36.6% of them, BMD was done only after experiencing site in 73.2%, compared to 26.8% fractures in the unaffect-
the first fracture. The mean age at first BMD evaluation ed (P = .001). The distribution of fractures by site was as
was 61.9 years. As shown in Table 2, a diagnosis of osteo- follows: femoral neck 16.4%, ankle 13.2%, radius 11.7%,
porosis was recorded for only 20.6% of PPS patients with tibia 10.1%, foot 10.1%, femur other than neck 7.8%, knee
available data. As expected, the mean BMD T-score (Tsc) 7.8%, ribs 5.4%, spine 4.6%, pelvis 4.6%, hands 4.6%, and
tended to be lower in the femoral neck of the affected limb humerus 3.1%. Antiresorptive medications were given to
(Tsc −1.64) compared to the unaffected one (Tsc −1.19), 22 of 31 patients having been diagnosed with osteoporosis;
with an intra-individual difference (delta Tsc) of −0.45, however, it was initiated only after their first fracture in
lower in the affected limb (P = .06). 47.3% of them. Four patients experienced their first frac-
ture while already on treatment, all of whom were post-
Bone Fractures in Post-Poliomyelitis Patients menopausal women taking bisphosphonates for an aver-
Data regarding bone fractures are shown in Table 2. age of 2.7 years. In 3 patients, the time interval between
A history of bone fractures was recorded in 52.2% of PPS treatment initiation and first fracture was not available. No
patients with available data, for a total of 131 fractures and fractures occurred in the remaining 31.5% of osteoporotic
an average of 1.59 fractures per patient. The mean age at treated PPS patients.
1280 Bone Fragility and Poliomyelitis, Endocr Pract. 2020;26(No. 11) Copyright © 2020 AACE
Gender Differences in Bone Health however, BMI was similar among both sexes. As expected,
Among Post-Poliomyelitis Patients there were more BMD data available for women (36.7%
When comparing clinical characteristics and fractures vs. 12.5%; P = .002), which was performed at a younger
by gender (Table 3), the height and weight of men were age compared with men (60.9 years vs. 65.5 years; P =
not surprisingly higher as compared to women (P<.001); .042). No significant differences were seen in BMD at the
Table 2
Osteoporosis and Fractures in Post-Poliomyelitis Patients
1st Bone Mineral Density an = 37 P value
Age 1st assessment, mean ± SD (years) 61.9 ± 6.6
median (range) 62 (49-74)
Lumbar Spine, T-score an = 34
mean ± SD −1.03 ± 1.35
median (range) −0.9 (−3.6 to +1.7)
FN affected, T-score an = 30
mean ± SD −1.64 ± 1.10
median (range) −1.4 (−3.5 to +0.4)
FN unaffected, T-score an = 19
mean ± SD −1.19 ± 0.77
median (range) −1.0 (−2.2 to +0.4)
FN affected vs. unaffected, T-score (delta) −0.45 .065
Bone Fractures
Patients with recurrent falls, n (%) 80/204 (39.2%)
Osteoporosis, n (%) 31/150 (20.6%)
Patients with fractures, n (%) 82/157 (52.2%)
All fractures (average per patient) 131/82 (1.59)
one Fx, n (%) 49/82 (59.7%)
more than 1 Fx, n (%) 33/82 (40.3%)
with 2 Fx, n (%) 19/82 (23.1%)
with 3 Fx, n (%) 12/82 (14.6%)
with 4 Fx, n (%) 2/82 (2.4%)
Patients with Fx of affected limb 60/82 (73.2%) b.001
femoral neck and lumbar spine among sexes. Interestingly, more prone to recurrent falls (44.9% vs. 32.6%; P>.05) and
the age at first BMD examination in men was younger fractures (57.4% vs. 45.7%; P>.05). The average number
than expected. of fractures per patient was similar between sexes, as was
Women were diagnosed with osteoporosis more the age at first fracture (56.8 and 57.1 years, men and
frequently than men (30.1% vs. 8.9%; P = .003) and were women, respectively). There was no difference between
Table 3
Comparison of Post-Poliomyelitis Patients by Gender
Women, n = 109 (53.4%) Men, n = 95 (46.5%) P value
Age at polio diagnosis, mean ± SD (months) 24.8 ± 25.7 (an = 27) 18.7 ± 17.6 (an = 38) >.05
Age at study entry, mean ± SD (years) 64.8 ± 6.0 65.0 ± 6.2 >.05
Height, mean ± SD (cm) 158.1 ± 5.9 (an = 30) 169.8 ± 7.4 (an = 18) <.001
Weight, mean ± SD (kg) 65.5 ± 13.0 (an = 31) 81.4 ± 15.4 (an = 18) <.001
Body mass index, mean ± SD 26.5 ± 5.2 (an = 30) 28.0 ± 4.7 (an = 18) >.05
Bone Mineral Density an = 29 an =8 .002
Age at 1st BMD
mean ± SD 60.9 ± 5.9 65.5 ± 7.9 .042
Lumbar Spine, T-score an = 28 an =6
mean ± SD −1.09 ± 1.0 −0.75 ± 1.87 >.05
FN affected FN, T-score an = 22 an =8
mean ± SD −1.56 ± 1.20 −1.85 ± 0.84 >.05
FN unaffected FN, T-score an = 15 an =4
mean ± SD −1.24 ± 0.86 −1.02 ± 0.21 >.05
FN affected-unaffected, T-score, deltab −0.32 (P>.05) −0.83 (P = .076) >.05c
Bone Fractures
Patients with fractures, n (%) 50/87 (57.4%) 32/70 (45.7%) >.05
Age 1st fracture, mean ± SD (years) 57.1 ± 8.9 56.8 ± 8.4 >.05
Recurrent falls, n (%) 49/109 (44.9%) 31/95 (32.6%) .098
Osteoporosis, n (%) 25/83 (30.1%) 6/67 (8.9%) .003
Fractures per patient, average 82/50 (1.64) 49/32 (1.53) >.05
1 Fx, n (%) 28/50 (56%) 21/32 (65.6%) >.05
>1 Fx, n (%) 22/50 (44%) 11/32 (34.3%) >.05
with 2 Fx 13/50 (26%) 6/32 (18.7%)
with 3 Fx 8/50 (16%) 4/32 (12.5%)
with 4 Fx 1/50 (2%) 1/32 (3.1%)
Fractures of affected limb, n (%) 51/80 (63.7%) 34/48 (71%) >.05
Patients with Fx of affected limb, n (%) 35/50 (70.0%) 25/32 (78.1%) >.05
Site of fracture, n (%) an = 82 an = 49 −
Lower limb 55 (67%) 35 (71.4%) >.05
Upper limb 18 (21.9%) 7 (14.2%) >.05
Spine 3 (3.6%) 3 (6.1%) >.05
Ribs 5 (6.1%) 2 (4%) >.05
Unknown 1 (1.2%) 2 (4%) >.05
Abbreviations: BMD = bone mineral density; FN = femoral neck; Fx = fracture.
aPatients with available data.
bDelta, intra-individual affected vs. unaffected BMD differences.
cComparison of delta between women and men.
1282 Bone Fragility and Poliomyelitis, Endocr Pract. 2020;26(No. 11) Copyright © 2020 AACE
sexes regarding the incidence of bone fractures except for Bone formation occurs during childhood and adoles-
a higher, but not significant, tendency in men to have more cence until reaching peak bone mass (PBM) up to the
fractures in the affected limb (71% vs. 63.7%; P>.05). As beginning of the third decade of life (18). We assumed that
seen in Table 3, this could be partially explained by men PPS patients who suffered from APP at a young age would
having a larger intra-individual delta BMD between affect- not have reached an optimal PBM in the affected limb.
ed and unaffected limbs, compared to women (delta-Tsc Furthermore, we expected the unaffected limb to have a
−0.83 vs. −0.32, respectively; P>.05). higher BMD due to compensatory overuse; however, a
poor functional status could affect bones at all sites (10,15).
Post-Poliomyelitis Patients With this background, BMD and osteoporosis in PPS
With and Without Bone Fractures patients may differ significantly from that of the general
The clinical characteristics of PPS patients with and population in pathogenesis, fracture risk, and therapeutic
without fractures are shown in Table 4. As expected, the approach. Accordingly, their limited mobility, advanced
fracture group had higher rates of recurrent falls (53.6% age, and low PBM may lead to a higher incidence of osteo-
vs. 34.6%; P = .05) and osteoporosis (30.9% vs. 9.4%; P = porosis and osteoporotic fractures (19).
.002). The tendency to a much lower BMD in the affected The assessment of BMD in PPS patients is quite prob-
limb compared to the unaffected one within the fracture lematic. On the one hand, aBMD tends to underestimate
group (Tsc −1.9 vs. −1.2; P = .06) could partially explain the small femurs of the affected limb (17); on the other
the higher risk of breaking the affected limb (73.2%) that hand, muscle weakness, poor ambulation, and skeletal
was discussed before. deformities impact all bones, irrespective of the affected
limb. As previously mentioned, the use of vBMD would
Post-Poliomyelitis Patients be more appropriate in these patients. Because this was a
According to Functional Status retrospective study, bone density was measured following
While comparing patients according to their function- real-world practice, where aBMD is routinely used; there-
al status, patients with assisted ambulation (76.4%) had fore, our results should be taken cautiously. We could have
higher rates of recurrent falls as compared to those with applied the Katzman formula (20) to convert aBMD into
nonassisted ambulation (45.4% vs. 19.0%, respectively; P bone mineral apparent density, but besides its poor preci-
= .002). Although BMD was similar between the assisted sion, we are not aware of any validated reference values.
and nonassisted ambulation groups, the assisted group A different approach could have been to use qCT machines
showed a tendency to a higher intra-individual difference (14), but qCT is not routinely available in clinical practice.
between affected and unaffected limbs, compared to the Furthermore, we are not aware of any study investigating
nonassisted group (delta Tsc −0.6 vs. −0.02, respective- the usefulness of trabecular bone score in PPS patients
ly; P>.05). Surprisingly, the difference in fracture events (21). All the above makes it easy to understand the pecu-
between groups was not statistically significant (55.6% vs. liarities and difficulties to be confronted when assessing
38.2%; P>.05). Nevertheless, a trend towards fractures at the true BMD in PPS patients, which remains a subject
an earlier age was nearly significant in the assisted-ambu- of research.
lation group (56.4 years vs. 59.8 years; P = .065). Although some studies examined the prevalence of
osteoporosis in the PPS population (15-17), very little is
DISCUSSION known about its prevalence in Israel. We found that BMD
in the affected limb tended to be lower compared to the
In this study, we analyzed the clinical characteris- unaffected. Similar results were reported by others (4,15).
tics of 204 Israeli patients with PPS to estimate the risk A cross-sectional study from Montréal found that lower
of osteoporosis and bone fractures. Most studies on PPS BMD in the affected limb correlated to lower muscle
patients addressed the issue of neuromuscular weakness, strength (16). Chang et al (22) found BMD in PPS men to
its functional and skeletal deformities consequences, and be 23% lower in the affected limb and 13% lower in the
treatment (1-6), but very few investigated the connection unaffected limb, compared to healthy controls. This data
between poliomyelitis, osteoporosis, and bone fractures suggests that in PPS men, a low BMD is not exclusive for
(15-17). We noticed that bone metabolism profession- the affected site, although it was 11.3% lower in the affect-
als in real practice play a marginal role in the care of PPS ed versus unaffected PPS limb.
patients, at least within the Israeli PPS population. We also In the present study, more than half of our PPS patients
found that the only guidelines published do not address the experienced at least one fracture at an early age, with multi-
risk of bone fractures but rather focus on muscle weakness, ple fractures reported in 40.3% of them. Of the overall 131
ambulatory balance, and skeletal deformities (6). Under fractures recorded among 82 PPS patients, 68.7% occurred
these circumstances, physicians are challenged by the in the lower limbs (16.4% at the femoral neck). Though our
specific characteristics inherent to this population regard- study did not include a control group, the 52.2% incidence
ing bone health assessment, indications and timing of treat- of fractures in our cohort was much higher than the 31.4%
ment, and the prevention of bone fractures. reported by Goerss et al (19), with a total of 161 fractures
Copyright © 2020 AACE Bone Fragility and Poliomyelitis, Endocr Pract. 2020;26(No. 11) 1283
recorded among 277 PPS patients. In a case-control study, much younger age (56.8 years) than expected (24). To the
Wu et al (23) corroborated Goers’ results, showing a frac- best of our knowledge, this is the first study comparing the
ture incidence of 26.3% (106/403) among PPS patients. risk of bone fracture in PPS patients according to gender.
Interestingly, Wu et al compared PPS patients to healthy Our finding that most PPS patients who suffered from
controls and found that PPS men had a 6-times higher inci- bone fractures broke the affected limb (73.2%) is in line
dence of fractures than expected, while it was only mildly with previous studies (15,19). Though this may seem obvi-
elevated among PPS women. Furthermore, fractures in ous, considering the lower PBM of the affected limb, we
PPS men occurred 13 years earlier than healthy controls. found these facts and their consequences to be frequently
Though the prevalence of fractures among the general overlooked, with more focus put on the muscle weak-
Israeli population has not been well established, one study ness and gait disorder, as well as the degenerative skeletal
in healthy Israelis reported the fracture rate at 80/1,000 in changes (1-6).
women and 20/1,000 in men; thus, by extrapolation, PPS Fall risk is an important issue because it represents a
men in our cohort showed a higher incidence of fractures significant health problem, especially among the elderly.
than expected. Also, the first fracture in men occurred at a At least one self-reported fall has been reported in 62 to
Table 4
Characteristics of Post-Polio Patients With and Without Fractures
Fractures, n = 82 No fractures, n = 75 P value
Women, n (%) 50 (60.9%) 43 (57.3%) >.05
Age at entry, mean ± SD (years) 65.7 ± 5.9 63.5 ± 6.6 .061
Age at polio diagnosis, month an = 22 an = 29
mean ± SD 19.9 ± 21.1 19.2 ± 17.3 >.05
Height, cm an = 29 an = 18
mean ± SD 161.6 ± 7.8 164.1 ± 10 >.05
Weight, kg an = 30 an = 18
mean ± SD 71 ± 16.2 72.9 ± 15.4 >.05
Body mass index, kg/m2 an = 29 an = 18
mean ± SD 27 ± 4.3 27.5 ± 6.1 >.05
Menopausal status -
Postmenopausal, n (%) 49/49 (100%) 35/37 (94.6%) >.05
HRT anytime, n (%) 11/41 (26.8%) 6/29 (20.6%) >.05
Age at menopause, years an = 24 an = 18 -
mean ± SD 50.7 ± 4.8 51 ± 3.9 >.05
1st Bone Mineral Density
Age at 1st BMD, years an = 19 an = 15 -
mean ± SD 61.7 ± 7.2 61.7 ± 5.9 >.05
Lumbar Spine T-score an = 20 an = 13 -
mean ± SD −1.13 ± 1.23 −1.0 ± 1.5 >.05
FN affected T-score an = 15 an = 13 -
mean ± SD −1.90 ± 1.10 −1.2 ± 0.9 .062
FN unaffected T-score an =8 an =9
mean ± SD −1.25 ± 0.84 −1.18 ± 0.84 >.05
FN affected-unaffected T-score, deltab −0.65 (P = .09) −0.02 (P = .417) .071c
Recurrent falls, n (%) 44/82 (53.6%) 26/75 (34.6%) .052
Osteoporosis, n (%) 22/71 (30.9%) 7/74 (9.4%) .002
Abbreviations: BMD = bone mineral density; FN = femoral neck; HRT = hormone replacement
therapy.
aPatients with available data.
bDelta, intra-individual affected vs. unaffected BMD differences.
cComparison of delta between fracture and no-fracture groups.
1284 Bone Fragility and Poliomyelitis, Endocr Pract. 2020;26(No. 11) Copyright © 2020 AACE
68% of PPS patients during a time-span of 1 year (12,13). may not have happened were endocrinologists and bone
However, in our study, recurrent falls were much lower metabolism specialists more involved in the care of PPS
(39.2%). The discrepancy may be explained by having patients. Nevertheless, our study suggests that in osteo-
our research based on medical records rather than self- porotic PPS patients, treatment should be considered at
questionnaires. Data from the U.S. show that up to 25% an early stage. Whether anabolic agents could be more
of people older than 65 sustain a fall each year, with 20 effective than antiresorptive agents has yet to be investi-
to 30% of them suffering moderate to severe injuries gated. The low PBM in this specific population suggests
such as bruises, hip fractures, or head trauma (25,26). that anabolic agents may have a role as first-line treat-
The increased morbidity and poor prognosis associated ment, including the recently approved sclerostin anti-
with hip fractures make these findings even more rele- body drugs, which might add some improvement in bone
vant (27,28). Furthermore, it has been reported that PPS microarchitecture (34).
patients with femoral fractures have a worse prognosis for The higher bone fracture risk, the lack of proper clini-
regaining their pre-injury ambulatory capacity and a higher cal guidelines (35), and the fact that 47.3% of osteoporotic
re-operation rate (29). PPS patients started treatment only after the first fracture
Only a few studies have been published addressing is good evidence of the current unawareness regarding the
the treatment of osteoporosis in PPS patients. Mohammad poor bone health and elevated risk in this population.
et al (15) studied 50 PPS patients, in whom 28 carried a The early age and higher risk for fractures in the PPS
diagnosis of osteoporosis, with 19 having a history of bone population should be a driving factor to put together clini-
fractures. Of these 19 patients, only 6 were receiving anti- cal guidelines for timely detection and intervention, irre-
resorptive therapy. The authors concluded that this popula- spective of a normal BMD at unaffected skeletal sites.
tion should be considered at high risk for fragility fractures However, the best time to start treatment remains uncer-
requiring an appropriate correction of other risk factors, an tain and is challenged by the differences in BMD among
early BMD evaluation, and a timely initiation of treatment. skeletal sites and the low PBM of this population, on top
We found only one retrospective study investigating of the evolving high bone turnover. It also poses the ques-
the response to bisphosphonates (BPs) on 144 PPS patients tion of which medication should be a first-line anabolic or
with over 5 years of follow-up (30). In that study, 54 antiresorptive agent.
BP-treated PPS patients were compared to 94 untreated PPS Our study has some strengths and limitations. The
patients. A control group was composed of 75 BP-treated main limitation is the scarce data on BMD examinations
and 37 nontreated typical osteoporotic patients. Results precluding us from performing an appropriate statistical
revealed that BP treatment in PPS patients was noninferior analysis in this regard. On the other hand, it emphasizes
compared to the control group. A subanalysis of 32 treated the need for more involvement of bone metabolic special-
PPS patients with bone fracture history showed that two- ists. Other limitations inherent to the retrospective nature
thirds of fractures occurred before and one-third during BP of our study were the lack of a control group and the fact
treatment. The benefit of preventing bone fractures in PPS that many BMDs were performed at the unaffected limb
patients was borderline significant on a conditional logistic only. Unfortunately, due to the few available data, we
regression model (P = .046) but nonsignificant on Poisson could not use the Z-scores as a surrogate for the control
regression analysis (P = .183). Based on their data, the group. As a retrospective study in a real-world scenario,
authors concluded that in PPS patients, BPs might improve selection bias for more-severe PPS patients seeking treat-
BMD; however, their benefit in preventing fractures needs ment at the outpatient clinic cannot be excluded; thus, our
further research. results may not represent the whole PPS population. The
Comparing PPS patients by gender, we confirmed study’s strengths include being the first hospital-based
the expected higher incidence of osteoporosis in women study to investigate bone health in PPS Israeli patients with
(24,31,32). However, the age and frequency of bone health access to extensive individual data, specifically related to
assessment in our cohort showed no differences among bone fractures.
sexes. Also, we found no differences in the incidence of
fractures, expected to occur 10 years later in healthy men. CONCLUSION
Although osteoporosis appeared to be delayed in our PPS
male group compared to women, it was diagnosed earlier We conclude that PPS patients are at high risk for
than expected for the healthy male population (33), with fragility fractures, which seems to be overlooked, especial-
their first BMD performed at a similar age as women. ly in men. A significant delay in diagnosis and treatment of
When comparing potential risk factors between osteoporosis and higher rates of recurrent falls with early
the fracture and nonfracture groups, only the higher age fractures all support having PPS patients included
rate of recurrent falls reached statistical significance as a high-risk group for bone fractures, together with the
(P = .05). Assessment of BMD impact on bone frac- compelling need for comprehensive clinical guidelines and
ture was precluded due to the few available data, which better awareness among the endocrine community.
Copyright © 2020 AACE Bone Fragility and Poliomyelitis, Endocr Pract. 2020;26(No. 11) 1285
DISCLOSURE 18. Weaver CM, Gordon CM, Janz KF, et al. The National
Osteoporosis Foundation’s position statement on peak bone mass
development and lifestyle factors: a systematic review and imple-
The authors have no multiplicity of interest to disclose. mentation recommendations. Osteoporos Int. 2016;27:1281-1386.
19. Goerss JB, Atkinson EJ, Windebank AJ, O’Fallon WM,
Melton LJ 3rd. Fractures in an aging population of poliomy-
elitis survivors: a community-based study in Olmsted County,
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