2024 Volume 132 Issue 2 Pages 105-115
This article describes the skeletal remains of a 20th-century individual diagnosed with poliomyelitis in childhood who suffered from atrophy and muscle weakness as an adult. The study provides a detailed analysis of both the primary effects of polio in the skeleton and the secondary effects across a lifetime, and contributes to the future identification of this pathology in osteoarchaeological assemblages. A skeleton of an 82-year-old male with poliomyelitis, from Tierra de la Reina, León (Spain) was submitted to bone densitometry, morphological, metric, cross-sectional, and palaeopathological analyses. Conventional X-rays and computed tomography scans were also performed. Skeletal alterations were categorized as directly and indirectly related to polio. The latter were probably acquired during life, resulting from mobility problems, malposition, and/or advanced age. Discrepancies in size, primarily related to polio, were observed between the right and left sides of the skeleton, with the left side being smaller and more gracile. However, while the asymmetry of the upper limbs is mainly in robustness, in the lower limbs the differences are in both robustness and length. This paper illustrates the skeletal alterations that may be present with poliomyelitis, demonstrating the complexity of diagnosing this pathology in an individual who lived a long life. In fact, many of the observed alterations can be found in other pathological conditions. Therefore, it is concluded that extreme caution be taken when analysing archaeological skeletal remains that are not as complete and well-preserved as this individual. The present work contributes to the diagnosis of poliomyelitis in human remains and underscores its impact in human history. Destructive methods were not authorized; medical records were no longer available. In the future, 3D reconstruction analysis/micro-computed tomography may add new and valuable information.
Poliomyelitis, also known as infantile Heine–Nadin paralysis (Zimerman, 2012), is an acute highly infectious disease caused by enterovirus of the Picornaviridae family (Baicus, 2012). The virus, commonly known as poliovirus, is transmitted person-to-person, mainly through the faecal–oral route or by a common vehicle (e.g. contaminated food or water), and multiplies in the intestine. While the prodrome displays typical flu-like symptoms with occasional muscle pain and stiffness, in some cases the infection affects the brain stem or spinal cord, causing the associated muscles to become irreversibly paralysed (Aufderhide and Rodríguez-Martín, 1998; Tesorieri, 2016; Berner et al., 2021). In this situation, the effect on the skeleton will be related to the age at which the virus was contracted. If contracted when the skeleton is still developing, the affected limbs will be shorter and more gracile than the unaffected ones. If the disease is contracted in adult life, there will be no differences in the length of the affected limbs, but only atrophy (Waldron, 2009).
Although it was first described only in 1860 by Heine, poliomyelitis is probably a very old disease. In fact, there are ancient Egyptian artworks showing a shortening of a lower limb in a child, which has been interpreted by some authors as evidence of polio (Baicus, 2012). But it was not until the beginning of the 20th century that polio outbreaks gradually became more severe, frequent, and widespread throughout Europe and the United States. An epidemic of polio was first reported in 1890, after 44 cases were identified in Stockholm during the summer of 1887 (Baicus, 2012). Around 1906, a poliomyelitis epidemic in Europe had a mortality rate of about 10% (Baicus, 2012; Berner et al., 2021); in the 1950s–1960s, it was the most common cause of disability amongst children (Ratnasingam et al., 2016). In Spain, polio also became an important public health problem due to the progressive increase in patients who annually suffered from paralytic poliomyelitis (average cases per year: 1950–1954, 1103; 1955–1959, 1494; 1960–1963, 1770) (Pérez Gallardo et al., 2013). Epidemics persisted until the beginning of vaccination (in the province of León in May 1963) (Rodríguez-Sánchez and Seco-Calvo, 2009; Pérez Gallardo et al., 2013). Until then, only general prophylactic measures were used (Ballester and Porras, 2012). In Spain, poliomyelitis was rarely fatal, but it frequently paralysed and incapacitated the victims. It was not until the 1940s that postural orthopaedic therapy begun to be used to treat polio patients (Martínez-Pérez, 2009).
While poliomyelitis is estimated to have affected more than one million people worldwide, there are only a few possible cases described in the osteoarchaeological literature (e.g. Winkler and Großschmidt, 1988; Umbelino et al., 1996; Kozlowski and Piontek, 2000; Roca de Togores et al., 2001; Roberts and Manchester, 2010; Zimerman, 2012; Novak et al., 2014; Thompson, 2014; Schrenk et al., 2016; Tesorieri, 2016; Ciesielska and Stark, 2019; Berner et al., 2021). Several factors may be responsible for this, one of which is the fact that human remains are frequently incomplete or poorly preserved, making it difficult to have a holistic vision of the skeleton and its alterations, which is crucial for the diagnosis of such a complex disease as poliomyelitis. Another factor is the lack of a solid baseline of skeletal alterations caused by polio against which to compare any suspected case.
Given the opportunity to analyse in detail the skeleton of an individual who was known to have suffered from poliomyelitis, the aim of this work is to facilitate future differential diagnosis of this condition and distinguish it from other paralytic diseases that lead to similar skeletal changes in ancient human remains. To this end, the skeletal alterations associated with the disease and those suffered due to mechanical malfunctioning and/or age will be described in detail.
The individual examined in this study was temporarily ceded by his family to the Department of Physical Anthropology of the University of León (Spain) with the agreement that the skeletal remains would be analysed and then returned at the end of the study.
The individual was an 82-year-old male (1908–1990) from Tierra de la Reina region (province of León, northwestern Spain), who had contracted poliomyelitis at the age of 5 years. Despite suffering from atrophy and muscle weakness since then, no orthopaedic support was provided throughout childhood. Only at the age of 60 years did he start using a walking cane as a mobility aid. Unfortunately, after his death, of cardiorespiratory arrest, all clinical records were destroyed (in accordance with Spanish Law 41/2002, article 17, which establishes only a minimum of five years of conservation from the date of death). Nonetheless, no doubts persist about the fact that he suffered from poliomyelitis.
The individual was buried in a niche, and with the family’s permission, was exhumed 20 years later for this research. Unfortunately, during the exhumation process, the sixth thoracic vertebra, patellae, carpals, and metacarpals were not recovered. The remaining skeleton showed no significant taphonomic alterations and was in a good state of preservation.
All bones were macroscopically and carefully observed for any alteration. Entheseal changes (ECs) were examined following the methodology of Mariotti et al. (2004, 2007), indicating the absence of differences between the right and left sides, the less marked insertion surfaces (right side versus left side), as well as the complete absence of ECs on one side. Furthermore, the presence of osteoarthritis (OA) was recorded following the methodology of Buikstra and Ubelaker (1994).
The bones were also measured, in millimetres (mm), with a digital calliper, osteometric board, and a flexible tape measure, following Buikstra and Ubelaker (1994). The percentage asymmetry of the bones was calculated according to Lieverse et al. (2008): [% asymmetry = 100 × (maximum – minimum)/minimum)]. The femur Rochet’s angle was assessed in degrees with a Powerfix digital protractor.
A radiological study was performed using Sedecal X-ray equipment to observe the internal structure of femurs, tibiae, and hip bones. Both femurs and both tibiae were also scrutinized by computed tomography (CT) using a GE Healthcare Optima CT540, to confirm the macroscopically observed change in orientation with respect to the main axis of the affected limb. The CT images were visualized using the commercially available software package Mimics (Materialise NV, Belgium).
Midshaft cross-sectional analysis of the femora and tibiae was performed with Moment-Macro for ImageJ (https://www.hopkinsmedicine.org/fae/mmacro.html), following Ruff and Hayes (1983). More specifically, the cortical area relative to total area (%CA) was used as a surrogate of diaphyseal robusticity and resistance to axial loads (body mass) and reflects the differential subperiosteal deposition and endosteal resorption of bone, principally during development (Ruff and Hayes, 1983). Ix/Iy is showing the diaphyseal shape and bone distribution in femora and tibiae, respectively, being Ix and Iy the anteroposterior, and mediolateral second moments of area, assessing bending rigidity in the anatomical planes; finally Zp represents the cross-sectional torsional strength.
Post-polio syndrome leads to paralysis, and as a consequence of muscle atrophy, this will imply less muscle tension in the affected limb, resulting in lower bone mineral density (BMD) (Grados et al., 2015), in addition to the prevalence of osteoporosis in those individuals who have suffered from poliomyelitis (Mohammad et al., 2009; Lo and Robinson, 2018). Therefore, the densitometric differences between the hip bone, femur, tibia, calcaneus, and talus of the left side (affected by poliomyelitis) and those of the right side (unaffected) were analysed. The densitometric study was carried out using a General Electric Lunar Prodigy Primo dual-energy X-ray absorptiometry system (kindly provided by the Faculty of Physical Activity and Sport Sciences, University of León).
The individual under study was diagnosed with poliomyelitis in childhood, at the age of 5 years. The most striking feature of the skeleton is the marked difference in size and robustness between the right and the left side, the latter being smaller and more gracile (Table 1). In addition, other bone alterations were observed that can be linked to this pathology, such as deformation of the hip, clubfoot, scoliosis, and the absence of ECs in the affected limbs and osteoporosis, among others.
Measurements of the preserved bones belonging to the studied skeleton from Tierra de la Reina, León (northwestern Spain)
| Bone | Measurement | Right (mm) | Left (mm) | Asymmetry (%) |
|---|---|---|---|---|
| Temporal | Mastoid width | 24.2 | 22.7 | 6.6 |
| Mandible | Maximum ramus height | 76.4 | 76.6 | 0.2 |
| Maximum ramus breadth | 40.1 | 44.4 | 10.7 | |
| Clavicle | Max length | 160.0 | 156.0 | 2.6 |
| AP diameter at midshaft | 11.7 | 11.7 | 0.3 | |
| V diameter at midshaft | 12.2 | 12.6 | 3.4 | |
| Scapula | Scapular height | 177.0 | 182.0 | 2.8 |
| Glenoid cavity width | 30.0 | 27.0 | 11.1 | |
| Glenoid cavity length | 43.0 | 42.0 | 2.4 | |
| Humerus | Max length | 308.0 | 305.0 | 1.0 |
| Physiological length | 302.0 | 300.0 | 0.7 | |
| Epicondylar breath | 72.3 | 75.5 | 4.5 | |
| Max vertical diameter of head | 49.7 | 49.7 | 0.2 | |
| Max diameter at midshaft | 25.1 | 26.3 | 4.9 | |
| Min diameter at midshaft | 20.7 | 21.3 | 2.9 | |
| Radius | Max length | 232.0 | 227.0 | 2.2 |
| Physiological length | 220.0 | 218.0 | 0.9 | |
| AP diameter at midshaft | 13.4 | 13.3 | 0.8 | |
| T diameter at midshaft | 18.5 | 17.9 | 3.2 | |
| Ulna | Max length | 258.0 | 254.0 | 1.6 |
| Physiological length | 224.0 | 216.0 | 3.7 | |
| Minimum circumference | 43.0 | 42.0 | 2.4 | |
| AP diameter at midshaft | 16.0 | 21.0 | 31.3 | |
| T diameter at midshaft | 20.0 | 19.0 | 5.3 | |
| Hip bone | Coxal height | 213.0 | 174.0 | 22.4 |
| Ilium breath | 155.0 | 140.5 | 10.3 | |
| Max ischiopubic diameter | 87.0 | 72.0 | 20.8 | |
| Cotyloid cavity diameter | 64.0 | 54.0 | 18.5 | |
| Femur | Max length | 407.0 | 403.0 | 1.0 |
| Physiological length | 406.0 | 400.0 | 1.5 | |
| AP diameter at midshaft | 30.0 | 21.0 | 42.9 | |
| T diameter at midshaft | 24.0 | 22.0 | 9.1 | |
| AP subtrochanteric diameter | 29.2 | 21.9 | 33.7 | |
| T subtrochanteric diameter | 32.0 | 23.0 | 39.1 | |
| Circumference at midshaft | 90.0 | 70.0 | 28.6 | |
| Max epicondylar width | 85.0 | 78.0 | 9.0 | |
| Max diameter of head | 52.0 | 46.0 | 13.0 | |
| Tibia | Max length | 336.0 | 317.0 | 6.0 |
| Max distal epicondylar breadth | 54.4 | 51.2 | 6.2 | |
| AP diameter at nutrient foramen | 29.8 | 18.3 | 62.6 | |
| T diameter at nutrient foramen | 26.6 | 24.2 | 9.8 | |
| Circumference at nutrient foramen | 92.0 | 71.0 | 29.6 | |
| Fibula | Max length | 332.0 | 304.0 | 9.2 |
| AP diameter at midshaft | 12.2 | 9.1 | 33.8 | |
| T diameter at midshaft | 13.1 | 10.5 | 24.5 | |
| Calcaneus | AP length | 73.2 | 72.1 | 1.5 |
| T width | 45.5 | 40.1 | 13.5 | |
| Talus | AP length | 57.3 | 51.9 | 10.6 |
| T width | 45.8 | 40.1 | 14.2 | |
| Navicular | Max length | 44.1 | 36.5 | 20.6 |
| Max width | 32.3 | 23.0 | 40.7 | |
| Cuboid | Max height | 34.5 | 34.4 | 0.2 |
| Max width | 25.4 | 21.8 | 16.5 | |
| 1st Cuneiform | Max height | 24.6 | 25.1 | 2.1 |
| Max width | 33.9 | 25.8 | 31.6 | |
| 2nd Cuneiform | Max height | 22.4 | 22.5 | 0.7 |
| Max width | 23.0 | 22.3 | 3.1 | |
| 3rd Cuneiform | Max height | 16.8 | 17.6 | 5.1 |
| Max width | 23.0 | 18.1 | 27.5 | |
| 1st Metatarsal | Max length | 60.1 | 58.0 | 3.5 |
| AP diameter at midshaft | 14.6 | 10.3 | 41.3 | |
| T diameter at midshaft | 16.0 | 10.2 | 56.2 | |
| AP diameter of the base | 31.9 | 24.4 | 31.1 |
Max, maximum; AP, anteroposterior; V, ventral; T, transversal.
The greatest asymmetry in terms of long bone length was recorded in the lower limbs (Figure 1A), namely, the fibulae and tibiae. However, as shown in Table 1, the asymmetry was even greater in the diameters of the femurs, tibias, and fibulae. Differences were also found in the dimensions of the two hip bones, with the left being much smaller than the right. Because of this asymmetry, the lesser pelvis was oriented towards the left side (Figure 2). In addition, the left femur was characterized by a less thick neck and a greater Rochet angle (140°) with respect to the right femur (135°) (Figure 1B, C), which is consistent with coxa valga.
(A) Atrophy and shortening of the left lower limb compared to the right one (white dotted lines indicate the location of the cross-sectional analysis at the midshaft of the tibia). (B) Right femoral neck, anterior view. (C) Left femoral neck, anterior view. In (B) and (C), the white arrows indicate Rochet’s angle, and the black arrows indicate the thickness of the femoral neck. The right femoral neck is thicker than the left.
Superior view of the pelvic girdle. The right hip bone is larger than the left. The lesser pelvis is asymmetric and has shifted towards the left.
Regarding the bones of the feet (Table 1), all left foot bones were atrophied and undersized compared with the right ones. The reduced size of the bones was most apparent in their widths and diameters. The asymmetries recorded in the lengths of the upper long bones (Table 1) were much smaller. Interestingly, the greatest asymmetries noticed in the upper limb were recorded in the robusticity, with the left side being more robust. In addition, the scapular height is somewhat greater on the left side than the right.
In the cranium, the right mastoid process was larger than the left. In contrast, the mandible’s maximum ramus breadth was 10.7% larger on the left side.
X-ray, CT and bone densitometry analysisX-ray analysis shows cortical thinning in the left femur and tibia, as well as an evident decrease in BMD in the left hip bone (Figure 3).
Radiological images. (A) Right hip bone. (B) Left hip bone with loss of bone mass. Close up of the (C) right proximal femur and (D) left proximal femur. (E) Right femur and tibia showing higher bone densities than (F). left femur and tibia.
In the CT analysis of the left and right tibiae and femora (Figure 4), it should be noted that the left tibia is twisted, with the main axis more ML oriented than expected.
CT cross-sectional differences in the left and right femora (upper row) and tibiae (lower row). A, anterior; P, posterior; L, lateral; M, medial.
Cross-sectional analysis at the midshaft of the femur and tibia (Table 2) also revealed an asymmetry in the geometric parameters, with the right side presenting a higher percentage of cortical area compared with the left one.
Cross-sectional parameters and laterality index of the femur and tibia of the individual from Tierra de la Reina, León (northwestern Spain)
| Bone | % CA | Ix/Iy | Zp | % CA laterality index | Ix/Iy laterality index | Zp laterality index |
|---|---|---|---|---|---|---|
| Right femur | 0.7 | 1.6 | 2375.8 | 66.7 | 36.9 | 70.5 |
| Left femur | 0.2 | 1.0 | 700.7 | — | — | — |
| Right tibia | 0.6 | 1.6 | 1712.9 | 8.6 | 64.6 | 43.8 |
| Left tibia | 0.6 | 0.6 | 962.9 | — | — | — |
% CA, Percentage of cortical area; Ix/Iy, diaphyseal shape; Zp, section moduli at midshaft (see Material and methods section for explanation). Laterality indexes are calculated as [(unaffected – affected)/unaffected] × 100.
Differences were also found in both BMD and bone mineral quantity (BMQ) between the two lower limbs (Table 3). The most striking differences were observed in the weight and BMQ of the analysed bones, although, in the case of the tibia, it was the BMD that presented the greater difference.
Dual-energy X-ray absorptiometry analysis showing lower BMD and BMQ values in the left side versus the right side
| Bone | Left | Right | Difference (%) | ||||||||||||||
|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
| Weight (g) | BMD (g/cm2) | SD BMD | BMQ (g) | SD BMQ | Weight (g) | BMD (g/cm2) | SD BMD | BMQ (g) | SD BMQ | Weight (g) | BMD (g/cm2) | SD BMD | BMQ (g) | SD BMQ | |||
| Hip bone | 65 | 0.5 | 0.01 | 12.2 | 0.43 | 217 | 0.9 | 0.03 | 55.6 | 4.16 | 70.1 | 39.1 | 0.02 | 78.2 | 2.30 | ||
| Femur | 146 | 0.7 | 0.01 | 31.6 | 2.79 | 291 | 1.0 | 0.01 | 47.6 | 9.86 | 49.8 | 34.0 | 0.01 | 33.7 | 6.32 | ||
| Tibia | 98 | 0.7 | 0.02 | 18.7 | 4.46 | 164 | 0.9 | 0.03 | 22.2 | 8.12 | 40.2 | 30.9 | 0.03 | 15.6 | 6.29 | ||
| Calcaneus | 11 | 0.4 | 0.02 | 2.2 | 0.36 | 28 | 0.7 | 0.02 | 6.6 | 2.17 | 60.7 | 41.0 | 0.02 | 66.8 | 1.27 | ||
| Talus | 7 | 0.4 | 0.02 | 1.4 | 0.50 | 15 | 0.7 | 0.03 | 4.6 | 1.40 | 53.3 | 46.6 | 0.02 | 69.4 | 0.95 | ||
BMD, bone mineral density; BMQ, bone mineral quantity.
The absence or tenuous imprinting of the muscle attachments observed in the left lower limb and hip bone are asymmetry indicators between the two sides. In Table 4, a detailed account of the ECs observed in the coxal and lower limbs of this individual is given, namely, which entheses look the same in the right and left sides, which ones were reduced in size or appeared less marked (and in which side), and which entheses were not present at all (and in which side).
Detailed account of the entheseal changes of the individual from Tierra de la Reina, León (northwestern Spain)
| Bone | Entheses | No difference between the two sides | Less marked on one side (which one) | Not present in one side (which one) |
|---|---|---|---|---|
| Coxal | Origin of the psoas major | ✓ (Left) | ||
| Origin of the iliacus | ✓ (Left) | |||
| Origin of the sartorius | ✓ (Left) | |||
| Origin of the rectus femoris | ✓ | |||
| Origin of the semimembranosus | ✓ (Left) | |||
| Origin of the biceps femoris and semitendinosus | ✓ (Left) | |||
| Origin of the adductor magnus | ✓ (Left) | |||
| Origin of the obturator internus | ✓ (Left) | |||
| Origin of the obturator externus | ✓ (Left) | |||
| Origin of the adductor longus | ✓ | |||
| Origin of the adductor brevis | ✓ | |||
| Origin of the gluteus maximus | ✓ (Left) | |||
| Origin of the gluteus medius | ✓ (Left) | |||
| Origin of the gluteus minimus | ✓ (Left) | |||
| Femur | Insertion of the obturator externus | ✓ (Left) | ||
| Origin of the quadriceps femoris | ✓ (Left) | |||
| Insertion of the gluteus medius | ✓ (Left) | |||
| Insertion of the gluteus minimus | ✓ (Left) | |||
| Insertion of the gluteus maximus | ✓ (Left) | |||
| Insertion of the iliopsoas | ✓ (Left) | |||
| Insertion and origin of the linea aspera muscles | ✓ (Left) | |||
| Insertion of the pectineus | ✓ (Left) | |||
| Origin of the medial and lateral heads of the gastrocnemius | ✓ (Left) | |||
| Origin of the vastus lateralis | ✓ (Left) | |||
| Origin of the vastus medialis | ✓ (Left) | |||
| Origin of the popliteus | ✓ (Left) | |||
| Tibia | Insertion of the popliteus | ✓ (Left) | ||
| Origin of the soleus | ✓ (Left) | |||
| Origin of the tibialis posterior | ✓ (Left) | |||
| Origin of the flexor digitorum longus | ✓ (Left) | |||
| Insertion of the iliotibial tract | ✓ (Left) | |||
| Insertion of the patellar ligament | ✓ (Left) | |||
| Origin of the tibialis anterior | ✓ (Left) | |||
| Fibula | Insertion of the biceps femoris | ✓ (Left) | ||
| Origin of the fibularis longus | ✓ (Left) | |||
| Origin of the extensor digitorum longus | ✓ (Left) | |||
| Origin of the fibularis brevis | ✓ (Left) | |||
| Origin of the fibularis tertius | ✓ (Left) | |||
| Origin of the flexor hallucis longus | ✓ (Left) | |||
| Calcaneus | Insertion of the triceps surae (Achilles tendon) | ✓ (Left) |
Osteoarthritis was observed in several locations of the skeleton (Supplementary Figure 1, Supplementary Figure 2), namely: the vertebral column, temporomandibular joints, acromioclavicular joints (mostly the right), sternoclavicular and esternocostal joints, glenohumeral joints (mostly the left), trochlea of the left humerus, auricular surface of the right hip bone, left acetabulum, right femoral head, and tibiotalar joint of the left tibia. Severe OA was observed in the right facet joints of all vertebrae, being more accentuated in the cervical and thoracic vertebrae, and there was clear reactive bone formation in the vertebral body of the third cervical (Supplementary Figure 2A). Minor scoliosis was recorded, convex to the right side in the thoracic-lumbar region, and convex to the left side in the lumbar region. The spinous processes from L1 to L5 were in contact with each other (Baastrup’s syndrome) (Supplementary Figure 2B). Pseudoarthrosis was detected at the right first sternocostal synchondrosis. In addition, a partial ankylosis of the left first sternocostal joint was observed, in both cases, as a result of ossification of the costal cartilages. Schmorl’s nodes were recorded in the vertebral bodies of T7 to T11. Syndesmophyte formation was identified on the right side, with pronounced flattening of the right side of T10.
All foot bones (Supplementary Figure 3) showed a reduction of the surface area of their articular facets. As for the left talus, the head and neck were medially rotated, the lateral process was underdeveloped, and the lateral and medial tubercles had a flattened appearance. The proximal concavity of the left navicular bone was deformed. In the left calcaneus, the articular facet for the cuboid was deformed, and the lesser process was in a more superior position compared with that of the right calcaneus.
The individual also presented other skeletal alterations, namely of developmental aetiology; these are not related (directly or indirectly) to poliomyelitis, and therefore are only described in Supplementary Figure 4.
Differential diagnosisAlthough the individual under study was diagnosed with polio at an early age (5 years), it might be important, from an osteoarchaeological perspective and to aid differential diagnosis in future cases, to compare the skeletal alterations recorded with those present in other types of neuromuscular diseases that begin at an early age (in childhood) (Table 5). Among all the neuromuscular diseases considered, cerebral palsy was the one that showed more skeletal changes in common with poliomyelitis.
Guidelines for differential diagnosis of neuromuscular disorders.
| Pathological condition | Individual under study | Reference |
|---|---|---|
| Cerebral palsy | ||
| Multiple limbs affected | No | Novak et al. (2014) Thompson (2014) Schrenk et al. (2016) Berner et al. (2021) |
| Bilateral hip displasia | No | |
| Femoral head flattening | No | |
| Femoral neck anteversion | Yes | |
| Various foot deformities | Yes | |
| Low bone mineral density | Yes | |
| Multiple trauma due to seizures | No | |
| Scoliosis of the spine | Yes | |
| Spondylolysis | No | |
| Enlarged metaphysis versus diaphysis | No | |
| Guillain–Barré syndrome | ||
| Symmetric paralysis | No | Berner et al. (2021) |
| Absence of atrophy or deformities | No | |
| Rasmussen’s encephalitis | ||
| Skeletal evidence of fractures due to aggressive nature of seizures | No | Berner et al. (2021) Ciesielska and Stark (2019) |
| Progressive diseases with a shortened lifespan | No | |
| Asymmetric development of the long bones on one side of the body | Yes | |
| Duchenne muscular dystrophy | ||
| Symmetric lower limb atrophy | No | Berner et al. (2021) Tesorieri (2016) |
| Progressive diseases with a shortened lifespan (around age 20) | No | |
| Equinus foot | Yes | |
| Scoliosis | Yes | |
| Poliomyelitis | ||
| Lower limbs more often affected than the upper ones | Yes | Roberts et al. (2004) Djukic et al. (2014) Thompson (2014) Tesorieri (2016) Ciesielska and Stark (2019) Berner et al. (2021) |
| Possible lumbar scoliosis | Yes | |
| Bone thinning in the affected limbs | Yes | |
| Coxa valga | Yes | |
| Asymmetry in the lower limbs | Yes | |
| Clubfoot | Yes | |
| Shortening of the paralysed limb | Yes | |
| Osteoporosis | Yes | |
The present study describes for the first time the alterations observed in the dry skeleton of an identified individual, from Tierra de la Reina, León, Spain, who demonstrably died of poliomyelitis. It should be mentioned how difficult it is to obtain and study skeletal specimens from modern polio patients, and how valuable this case is. The individual under study is characterized by musculoskeletal alterations, some directly related to poliomyelitis, whereas others probably resulted from mobility problems caused by the disease and advanced age. Thus, it is very important to clarify which of the changes are primarily related to polio, and which were gained during life due to behaviour or age. Therefore, a checklist is provided in Table 6.
Skeletal features and alterations of the individual from Tierra de la Reina, León (northwestern Spain), divided into those primarily resulting from polio and those gained during life due to behaviour or age
| Skeletal features/alteration | Primarily related to poliomyelitis | Gained during life |
|---|---|---|
| Shorter left lower limb and smaller left coxal bone | ✓ | |
| Deformation of the hip towards the affected side (left side) | ✓ | |
| Left clubfoot | ✓ | |
| Anteversion of the left proximal femur | ✓ | |
| Coxa valga in the left femur | ✓ | |
| External torsion of the left tibia | ✓ | |
| Slight scoliosis to the right side | ✓ | |
| Greater robustness of the left upper limb | ✓ | |
| Entheseal changes | ✓ | |
| Osteoarthritis | ✓ |
Most probably directly related to poliomyelitis is the pronounced atrophy and shortening of the left lower limb, from the hip to the foot bones, the deformation/inclination of the hip towards the affected side, the anteversion of the left proximal femur as well as coxa valga, the external torsion of the left tibia, and the clubfoot on the left side. Regarding the bone lengths, the tibia and fibula were the most asymmetric bones, which is in accordance with clinical studies that have identified the tibia as the bone most affected by shortening, due to paralysis of the tibialis anterior and the tibialis posterior muscles, along with the long toe flexor muscles (Tesorieri, 2016). Current clinical studies link a high percentage of the development of osteoporosis to post-polio syndrome (Haziza et al., 2007; Mohammad et al., 2009; Ratnasingam et al., 2016; Lo and Robinson, 2018). Other clinical studies (Minaire, 1989; Miyamoto et al., 1998; Grados et al., 2015) have also linked this decrease in BMD to the loss of trabecular bone, as well as to loss of muscle in the affected leg. Similarly, Ratnasingam et al. (2016) observed decreased BMD in the polio-affected leg of a 49-year-old woman with a history of polio during childhood. In an archaeological context, the pathological changes observed in the polio-affected leg could be due to the rapid reduction of BMD (Schrenk et al., 2016). Thus, BMD and BMQ analysis of the individual under study revealed severe osteoporosis in the polio limb. In addition, reduced muscle strength in the lower limb affected by poliomyelitis has been found to be associated with regional osteoporosis of the hip (Haziza et al., 2007; Lo and Robinson, 2018). Additionally, it should be born in mind that the bone atrophy on the pathological side would lead to overloading on the unaffected side, resulting in compensatory muscular hypertrophy, more pronounced muscle insertions, and bones that are markedly more robust. The unbalanced movement itself over several decades would lead to the weakening of the affected limb, enhancing the contrast with age. According to Qin et al. (2020), this unbalanced movement would have had other consequences, such as deformation of the spine and tilting of the pelvis. In fact, such consequences, indirectly related to polio, are conspicuous in the present case.
Another observed feature directly related to polio that should be emphasized is the twisting observed at the left tibia, with the main axis more ML oriented than expected, which would affect the individual’s locomotion given the important bearing function of this bone.
In patients with poliomyelitis, some of the most affected muscles are the quadriceps, the gluteus maximus, the gluteus medius, the anterior and posterior tibialis, and the triceps surae, whose involvement causes deformities in the limb and, ultimately, may result in clubfoot (Thompson, 2014; Gordero, 2015). The left foot bones show significant alterations, compatible with clubfoot. It should be noted that in cases of poliomyelitis, acquired clubfoot, in opposition to congenital clubfoot, results from neurogenic causes (Anand and Sala, 2008; Nomura et al., 2014), being associated with osteoporosis (Wright, 2011). In the present case, although it is not possible to be sure that the clubfoot arose as a consequence of poliomyelitis, since the clinical records for this individual were destroyed, the information given by the family, who reported that the individual was born with “normal feet” and clubfoot only emerged after poliomyelitis was contracted, favours that hypothesis.
It should be noted, however, that while none of these direct alterations are pathognomonic of the disease, many, like femoral neck anteversion, coxa valga, and foot abnormalities (e.g. clubfoot, pes cavus), are often associated with this disease (Roberts et al., 2004; Djukic et al., 2014; Berner et al., 2021).
Indirectly related to polio, and probably resulting from mobility and posture problems caused by the disease as well as advanced age, several feature stand out, namely, the ECs, the OA of multiple joints, and the ankylosis of the left first sternocostal joint. In the upper limbs, the differences in robustness, the ECs (sometimes more marked on the right side), and the degenerative joint disease probably resulted from their use to compensate for the weakness of the left leg muscles (Klein et al., 2000; Roca de Togores et al., 2001; Koh et al., 2002; Tesorieri, 2016), and/or from the use of a walking cane (Owsley and Mann, 1990) in the 20 years prior to death.
In the vertebral column, the spinous processes from L1 to L5 are very close to each other, which is consistent with Baastrup’s syndrome (Philipp et al., 2016), resulting from excessive lordosis or the loss of intervertebral space (Kacki et al., 2011). A slight scoliosis was observed in both thoracic and lumbar region, although scoliosis is not pathognomonic of polio (Winkler and Großschmidt, 1988; Roberts and Manchester, 2010; Schrenk et al., 2016; Ciesielska and Stark, 2019; Berner et al., 2021). Besides, in post-polio syndrome, the paralysis and subsequent muscle atrophy lead to the alteration in the load axis of the spine (with or without scoliosis), resulting in degenerative changes (Grados et al., 2015), namely spinal OA, which may be exacerbated with age.
Regarding the pseudoarthrosis observed at the right first sternocostal synchondrosis, it can be related to three different factors: congenital anomaly, acute fracture, or even chronic stress fractures (Brower and Woodlief, 1980). On the other hand, and according to current clinical studies, pseudarthrosis of the first rib is frequent in older individuals, as progressive calcification of cartilaginous parts is common. In some cases, this leads to complete synostosis. (Schils et al., 1989; Gossner, 2016). However, it should not be ignored that stress fractures of the ribs may also occur as a consequence of the overuse of upper limbs (Mithöfer and Giza, 2004).
Overall, the lesions and skeletal alterations found in the individual studied, such as asymmetry in the lower limbs, coxa valga in the left femur, muscle atrophy in the affected limb and clubfoot, have been described in other palaeopathological cases linked to poliomyelitis (e.g. Umbelino et al., 1996; Tesorieri, 2016; Ciesielska and Stark, 2019; Berner et al., 2021).
This article describes the features observed in the skeleton of a case diagnosed with paralytic poliomyelitis. Thus, knowing that the individual suffered from this pathology, and being able to observe the skeletal alterations directly and indirectly linked to poliomyelitis can be valuable for palaeopathology. The most conspicuous skeletal changes that were directly related to poliomyelitis include limb asymmetries, mainly in robustness but also in the length of the lower limbs, deformation/inclination of the hip towards the affected side (left), anteversion of the left proximal femur, external torsion of the left tibia, and clubfoot on the left side. Although the observed non-polio-related bone changes (ECs and OA) are not pathognomonic for polio, their co-occurrence is very probable if a polio survivor lives long with paralytic poliomyelitis. Therefore, these alterations not only support the diagnosis of poliomyelitis in osteoarchaeological assemblages, but also provide clues for the serious implications for the individual’s life. The ECs (more marked on the right side) and the differences of robustness observed in upper limbs probably resulted from their overuse to compensate for the weakness of the left leg muscles. In addition, the absence or tenuous imprinting of the muscle attachments observed in the left lower limb and hip bone are asymmetry indicators between the two sides. Thus, the bone atrophy on the pathological side would lead to overloading on the unaffected side, resulting in compensatory muscular hypertrophy. The fact that the individual had clubfoot implies a deformation of the tarsal bones of the affected foot, mainly the calcaneus and talus. As a result, the individual used a cane for walking, as reported by his living relatives.
The complexity of diagnosing this disease in an individual who lived many years after contracting the virus is also highlighted, suggesting caution in future diagnoses of this disease in the osteoarchaeological record.
Taking into consideration the ethical concerns arising from analysing recent skeletons, the individual’s identity was kept anonymous. Regarding the images, only those strictly justified are presented, always with the consent of the living descendants.
Sofia N. Wasterlain was financed by national funds by FCT—Fundação para a Ciência e Tecnologia, project grant reference UIDB/00283/2020.
The authors thank the family of the analysed individual, Dr Eduardo Sánchez Compadre, Dra Humildad Rodríguez Otero, and the Veterinary Hospital and Faculty of Physical Activity and Sport Sciences of the University of León (Spain). The authors also acknowledge the anonymous reviewers whose valuable comments and suggestions improved the manuscript.
