Received: 10 February 2021 Revised: 23 September 2021 Accepted: 4 October 2021 DOI: 10.1002/oa.3057 RESEARCH ARTICLE Pathological and normal variability of foot bones in osteological collections from Catalonia (Spain) and Lazio (Italy) Eduardo Saldías1,2 | Albert Isidro3 | Cristina Martínez-Labarga4 | Alfredo Coppa5 | Mauro Rubini6 | Bernardo Vila7 | Assumpcio  Malgosa1 1 Anthropology Unit, Department of Animal Biology, Plant Biology and Ecology, Abstract Autonomous University of Barcelona, A wide number of factors can affect the structure of the bones in the foot. In bio- Barcelona, Spain 2 archaeology, few studies about foot anomalies include population comparisons and Department of Anthropology, University of Chile, Ñuñoa, Chile changes across time. We aimed to identify normal and pathological variability that 3 Orthopedic and Trauma Surgery Department, affected the foot in the recent history of West Mediterranean populations. Thus, we Sagrat Cor University Hospital, Barcelona, Spain analyzed change in occurrence of rare variants, pathological lesions, entheseal mor- 4 Department of Biology, University of Rome phology, and their probable causes. We studied 518 pairs of skeletonized feet dated Tor Vergata, Rome, Italy from the 2nd–20th centuries CE, from Catalonia (Spain) and the region of Lazio 5 Department of Environmental Biology, Sapienza University of Rome, Rome, Italy (Italy). Moreover, a Neolithic series from Oman has been analyzed for contrast. We 6 Anthropology Service of the S.A.B.A.P.-LAZ, found that calcaneal spur, hypertrophic peroneal trochlea of calcaneus, periosteal Superintendence for Archaeological Heritage reaction of talar neck, alteration of articular surface to lateral cuneiform, displaced of Lazio, Rome, Italy 7 talar neck to medial plane, osteophytes in cuneiform-navicular joint, fused phalanges, Department of Anthropology, Sanisera Archaeology Institute, Sharjah, and forefoot eburnation showed significant differences among countries. Contrasting United Arab Emirates by countries and dates, we noticed an increase in the frequencies of these variables Correspondence from Spain over the centuries. Conversely, there are no temporal differences among Eduardo Saldías, Department of Anthropology, the Italian series. The period encompassing the 10th–19th centuries CE demon- University of Chile, Ignacio Carrera Pinto 1045, Ñuñoa 6850331, Chile. strated the highest differences between countries. Lifestyle, occupations, footwear, Email: edusaldiasvergara@gmail.com and geography could be the origin of variability. Funding information  d’Ajuts Universitaris i de Agència de Gestio KEYWORDS Recerca, Grant/Award Number: foot diseases, paleopathology, population studies, skeletal variability 2017SGR1630; CONICYT PAI, Grant/Award Numbers: CONICYT PAI/2014-73130722 (ES), 2014-73130722 [Correction added on 24 December 2021, after first online publication: affiliation section has been modified in this version]. 1 | I N T RO DU CT I O N physical anthropology, archaeology, medicine, molecular biology, histology, and genetics. To understand pathological processes and to Paleopathology is the science that studies diseases in the past. It is an gain information about etiology, we look at the biological profile interdisciplinary science that involves various disciplines such as (i.e., age-at-death, sex, etc.), morpho-anatomical variants, affected This is an open access article under the terms of the Creative Commons Attribution-NonCommercial-NoDerivs License, which permits use and distribution in any medium, provided the original work is properly cited, the use is non-commercial and no modifications or adaptations are made. © 2021 The Authors. International Journal of Osteoarchaeology published by John Wiley & Sons Ltd. Int J Osteoarchaeol. 2022;32:215–228. wileyonlinelibrary.com/journal/oa 215 216 SALDÍAS ET AL. zone, and temporal/geographical frame. Among anatomical areas, feet The Spanish collection consists of 215 remains from four archaeo- are some of the least analyzed. They are susceptible to undergo logical sites in Catalonia, which are as follows: the Esglésies de Sant changes within either the soft tissue or the skeletal mass by different Pere, Casserres, Castell de Termens and Avinganya. A documented col- lifestyle factors, possibly leading to issues in their functionality and lection from the Universitat Autònoma de Barcelona (UAB) that gathers gait (Brewer, 2017). Chronic and progressive pathological conditions 32 contemporary individuals with an average age of over 70 years from such as osteoarthritis can occur with age, among other factors the cemetery of Granollers (Barcelona) (Table 1) was also included. (White & Folkens, 2005). In addition, traumatisms, obesity, congenital Excluding the modern collection, the remainder correspond to series and neurological diseases, infections, and cultural factors can change with ecclesiastic or rural lifestyles (2nd–9th/10th–19th centuries CE). the normal form of the feet (Lee et al., 2005). The first Spanish group (2nd–9th centuries CE) consists of two During the last two decades, some scholars (Albee, 2020; collections from different contexts: Casserres and the first period of Anderson, 2004; Burnett & Wilczak, 2012; Case & Heilman, 2005; St. Pere (St Pere I). According to historical documents, Casserres Chiavegatti et al., 2018; Isidro et al., 2015; Jashashvili et al., 2010; comes from a rural settlement from the 7th–9th centuries CE, Laffranchi et al., 2015; Vikatou et al., 2017; Weiss, 2012) have studied whereas the Sant Pere I necropolis belongs to an Episcopal Seat bioarchaeological collections to understand the lifestyle of the past necropolis (4th–8th centuries CE) related to bishops and the upper through foot health (Mays, 2005). Nonetheless, not all populations are social class, whom led the society (Ferran, 1987; Vives, 1990). affected in the same manner, nor do they have the same anatomical The second Spanish group (10th–19th centuries CE) also includes variations. For example, foot pathologies are less common in barefoot the necropolis of St Pere (St Pere II: 9th–12th centuries CE). After the populations (Balint et al., 2003; Isidro et al., 2015), whereas over 70% Muslim invasion, the socio-political relevance of the St Pere churches of individuals from modern populations suffer pain and possess foot decreased in status, effectively becoming a parish (Jordana deformities (Balint et al., 2003; Kapandji, 1998). et al., 2010). This Spanish period also involved an ecclesiastic and a This research aims to analyze the existence of normal and patho- rural necropolis (Avinganya and Termens, respectively). Avinganya logical variabilities of foot bones and their changes across time in two (13th–17th centuries CE) was a Trinitarian Monastery (Fuentes- sets of skeletal remains from two Western Mediterranean regions Sánchez et al., 2016; Montes et al., 2021), and Termens was a necrop- (2nd–19th centuries CE). Acknowledging that most of the osteological olis located near Termens castle, whose individuals are dated between collections belong to current territories from Spain and Italy, we iden- 1830 and 1860 A. D. and correspond to an agricultural population. tified cultural variations and other factors (genetics, life expectancy, The Italian series includes 216 analyzed individuals from geography, etc.) that could have influenced the occurrence and mor- 10 archaeological sites of the Lazio region: Guidonia, Monterotondo phology of features. Additionally, the probable etiology and causes of CAR, San Ercolano, Crypta Balbi, Villa Gordiani, Castro dei Volsci, the differences between each series were taken into consideration Colonna, Leopoli-Cencelle, Aquino, and Allumiere (Table 1). when conducting the study. The collections from the 2nd–9th centuries CE include eight to 35 individuals. They are a mixture of different lifestyles under the final 2 | MATERIALS AND METHODS years of the Roman and Byzantine Empires, located inside the current city of Rome and the surrounding area. For instance, Crypta Balbi is A total of 518 pairs of skeletonized feet from different bio- an archaeological complex located in Rome, originally built around archaeological contexts (2nd–19th centuries CE) in current territories year 13 BCE as a theater (Sagui, 1998), whose building and its terri- of Spain and Italy have been analyzed and include sex and age range tory were reused for different purposes. Another, Villa Gordiani, a estimation (Table 1). A contemporary series from Granollers monumental site composed of mortuary structures and a religious and (Catalonia, Spain) and a Neolithic collection from the Sultanate of residential complex, is also located in Rome and, based on archaeolog- Oman were included into the overall study as well. ical evidence, has been associated with Roman Imperial families To contrast the changes across time between countries and (Palombi & Leone, 2008). series, we chronologically divided these collections into two sub- The remainder of the series corresponds to populations located groups while also considering cultural changes that could have outside the current city of Rome (Guidonia, Monterotondo, San influenced lifestyle and foot health. These factors are related to the Ercolano, Colonna) whose lifestyle largely consisted of animal hus- system of government and its impact on religion, migrations/inva- bandry and agriculture (Baldoni et al., 2016; Baldoni, Ferrito, & sions, economy, and occupational activities. Taking this all into Martinez-Labarga, 2018; Rothschild et al., 2004; Rubini & account, we designated the 10th century CE as the marker to divide Mogliazza, 2005). Additionally, the necropolis of Castro dei Volsci our collections based on cultural, archaeological, and lifestyle shifts in (Frosinone province, Lazio) corresponds to victims of the Justinian Europe during this era (Echevarría-Arsuaga & Rodríguez-García, 2013; Plague (Yersinia pestis), a pandemic that affected a large part of the Mitre, 2011; O'Malley, 2009; Romero, 1949; Soldevilla, 1962). Utiliz- world population of that period. ing this approach, the first group comprises all sites dated between The Italian series from the 10th–19th centuries includes two col- the 2nd–9th centuries CE, whereas the second group consists of lections. Leopoli-Cencelle (4th–15th centuries CE) (Baldoni, 2019) is a those dated between the 10th and 19th centuries CE. Both groups medieval city located atop of a hill, between Allumiere and Tarquinia. from these countries have a balanced number of individuals (Table 1). Archaeological findings revealed activities in warehouses, taverns, TABLE 1 Number of individuals from every collection divided by country, considering their historic period, estimation of sex, and age range % of the total Country Period Centuries Series % of estimated sex Age range estimate References N sample SALDÍAS ET AL. Spain 4th–9th CE Sant Pere I ♂ 58.8 18–39: 41.2%, 40–69: 44.1%, Jordana et al. (2010) 34 6.5 ♀ 41.2 Ind: 14.7% 2nd–9th centuries 7th–9th CE Casserres ♂ 67.2 18–39: 44.8%, 40–69: 51.7%, Cascante and Farguell (2007) 58 11.2 CE ♀ 32.8 +70: 3.4% 10th–14th CE Sant Pere II ♂ 65.5 18–39: 38.2%, 40–69: 54.6%, Jordana et al. (2010) 55 10.6 ♀ 34.5 Ind: 7.3% a a 10th–19th centuries 9th–14th CE Avinganya Fuentes-Sánchez et al. (2016), 47 9 CE Montes et al. (2021, no published) 18th–19th CE Termens ♂ 52.4 18–39: 71.5%, 40–69: 19%, Alesan et al. (1996) 21 4 ♀ 47.6 Ind: 9.5% Contemporary 20th CE Granollers ♂ 53.1 18–39: 3.1%, 40–69: 37.5%, Saldías et al. (2016) 32 6.2 ♀ 46.9 +70: 50.0%, Ind: 9.4% Italy 2nd–3rd CE Guidonia ♂ 71.4 18–39: 21.4%, 40–69: 71.4%, Baldoni, Ferrito, and Martinez- 14 2.7 ♀ 28.6 Ind: 7.1% Labarga (2018) 2nd–3rd CE Monterotondo ♂ 33.3 18–39: 22.2%, 40–69: 55.5%, Rubini and Mogliazza (2005) 11 2.1 CAR ♀ 55.6 Ind: 22.2% Ind: 11.1 b 4th–5th CE San Ercolano ♂ 40.0 Rothchild et al. (2004) 15 2.9 ♀ 50.0 Ind: 10.0 2nd–9th centuries 5th–6th CE Villa Gordiani ♂ 66.7 18–39: 80.0%, 40–69: 13.4%, Fornaciari et al. (1984) 15 2.9 CE ♀ 26.7 Ind: 6.7% Ind: 6.7 6th CE Castro dei Volsci ♂ 60 18–39: 78.8%, 40–69: 6.1%, Rubini (2009) 35 6.8 ♀ 40 Ind: 15.2% 8th–10th CE Colonna ♂ 48.0 18–39: 68.0%, 40–69: 20.0%, Baldoni et al. (2016) 25 4.8 ♀ 48.0 Ind: 12.0 Ind: 4.0 b 4th–5th CE Crypta Balbi ♂ 25.0 Sagui (1998) 8 1.5 ♀ 0 ?: 75.0 10th–19th centuries 9th–15th CE Leopoli-Cencelle ♂ 49.3 18–39: 26.2%, 40–69: 18%, Baldoni (2019) 61 11.8 CE ♀ 39.3 Ind: 55.7% Ind: 11.5 11th CE Aquino ♂ 100 40–69: 100% 2 0.4 ♀0 15th–16th CE Allumiere ♂ 86.7 18–39: 76.6%, 40–69: 16.7%, Baldoni, Scorrano, et al. (2018) 30 5.8 ♀ 13.3 Ind: 6.7% (Continues) 217 218 SALDÍAS ET AL. workshops, and hen houses (Stasolla, 2018). The population of Allumiere (15th–16th centuries CE), located in the area of Tolfa Work in progress. According to Montes et al. (2021, not published), who analyzed the same bioarchaeological campaign, 31.08% are male and 24.32% female, whose common age range is between 20 and % of the total Mountains, was a mining city with a high percentage of males (Baldoni, Scorrano, et al., 2018). sample 10.6 Finally, 55 pairs of feet from Ras al-Hamra 5 (RH5), a Neolithic 100 series (3700–3400 centuries BCE) of sedentary fishermen who settled along the Arabian coast, belonging to the Sultanate of Oman, were 55 518 N included (Coppa et al., 1985; Coppa et al., 1990) (Table 1). A signifi- cant number of these individuals developed different levels of spina bifida (Coppa, 2012). Our analysis considered 37 variables clustered into three feature groups (Table 2 and Supporting Information), which correspond to all the osteological features (variabilities and pathologies) that we found in the series. According to their etiology, the first group of our classifi- cation includes osteophytes, non-osteophytic alteration of facets, and Coppa (2012) bone deformation due to degenerative joint disease. The second cor- References responds to entheses, whereas the third contains bone variability, including accessory bones and facet variability. Every single foot bone — and their affected zone were analyzed using a dichotomous score 18–39: 46.1%, 40–69: 33.2%, (presence or absence). For statistical purposes, the chi-square test 18–39: 56.4%, 40–69: 25.6% was applied to compare groups and check for significant differences. +70: 3.7%, Ind: 17.0% Age range estimate 3 | RE SU LT S It is not possible estimate an age range of the individuals, due to the bad state of preservation of the human remains. Ind: 17.9% We have obtained the frequencies of all the variables for each popula- tion and grouped by country (see Tables S1–S3). The χ 2 results showed significant differences for 8 of these vari- % of estimated sex ables when the three countries were compared (Table 3). They are as follows: calcaneal spur (SPURC), hypertrophic peroneal trochlea (PERTR), periosteal reaction in the talar neck (OMANK), head/neck of Ind: 8.0 Ind: 4.6 ♂ 56.0 ♀ 36.0 ♀ 36.4 ♂ 59 talus displaced to medial plane (DISHN), osteophytes along cuboid articular surface to the lateral cuneiform (CUNOS), osteophytes along the cuneiform-navicular joint (ONCUN), forefoot eburnation (EBANT), Ras al-Hamra 5 and fused phalanges (MERGE) (descriptions in the Supporting Information). (RH5) Most of the differences (Figures 1 and 2) correspond to degener- Series ative processes (five variables), although the osteophytes in the — cuneiform-navicular joint (ONCUN) displayed the highest contingency coefficient values (Table 3). This value better explains the differences 3,400 BCE between the collections. Centuries 3,700– To carry out a comparative analysis between pairs of countries, the previous significant variables were used. The Spanish series dem- — onstrated differences with the Italian series in all variables, though no differences were displayed when compared to the Omani series. Conversely, the Italian collections demonstrated differences in four (Continued) traits (head/neck of the talus displaced to medial plane, osteophytes Neolithic in or along cuboid articular surface to the lateral cuneiform, fused pha- Period langes, forefoot eburnation) with the Omani series (Table 4). To understand these results, we divided the collections by country 40 years old. TABLE 1 Country and period: their incidence by sex and age (Table 5). The Spanish collec- Oman Total tion presented an increase in the frequencies of pathological lesions, entheses/musculoskeletal activity markers across time (highest b a SALDÍAS ET AL. 219 TABLE 2 Variables included in the analysis, divided in three groups according their features Musculoskeletal Degenerative processes activity markers Variability Non-osteophytic Bone deformation/ Accessory bones/ Osteophytes alteration of facets severe bone damage Entheses/others facets variability Osteophytes in cuboid-metatarsal Flattening calcaneus- Comma shape Calcaneal spur Fused Sustentaculum joint talus joint COMMAS SPURC tali facets OCCJN FLACC STFUS Osteophytes in the surface to the Lipping in talar head Fused phalanges Achilles entesopathy Cuboid facet of lateral cuneiform of cuboid LIPHD MERGE ACHIL navicular CUNOS CUBFC Osteophytes in cuboid-lateral Lipping in cuneiform Hind/midfoot joint Hypertrophic Peroneal Extended talar tail cuneiform joint facets of navicular surface eburnation trochlea EXTTT OCUCB LPCUN EBRME PERTR Osteophytes in cuneiform-metatarsal Flattening cuboid- Forefoot joint surface Altered tuberosity of Os trigonum joint metatarsal joint eburnation navicular TRIGM OCMTT FLCUC EBANT EXTUB Osteophytes in cuneiform-navicular Plantar-medial Tarsal coalition Periosteal reaction in Trigonal articulation joint sustentaculum tali COALT the talar neck of calcaneus ONCUN PMSTA OMANK TRART Osteophytic sustentaculum tali Head/neck displaced to Hallux valgus Accessory navicular OSTST medial plane HVALG NAVAC DISHN Osteophytic calcaneal-cuboid joint Avascular necrosis in Fracture CCLOS talar head FRACT NECHD Osteophytic calcaneus-talus joint Osteochondritis CTOST OCDRT Osteophytic talar tail TAILO Osteophyte in talar head OHEAD Osteophytic talar facet of navicular TFOST Note. Abbreviation codes are in bold. frequencies in 10th–19th centuries CE group) in almost all the analyzed periosteal reaction in the talar neck). The Italian series showed unifor- features, except head/neck of the talus displaced to medial plane and mity among variables. The comparison between the Spanish and Ital- fused phalanges. The Granollers series displays high frequencies for ian series exhibited further differences between the 10th and 19th most features, specifically the calcaneal spur, periosteal reaction in the centuries CE groups (Table 6). Of all variables, osteophytes in the talar neck, forefoot eburnation, and fused phalanges, all of which have cuneiform-navicular joint had the highest contingency coefficient the highest frequencies among all the series (Table 5). values (0.257, see the Supporting Information). Including the The Italian series, conversely, shows no clear temporal change of Granollers collection to the Spanish 10th–19th centuries collection the variables; the frequencies of some musculoskeletal activity markers, (hereby named the 10th–20th centuries CE collection) displayed some calcaneal spur, hypertrophic peroneal trochlea, periosteal reaction in significant differences within the Spanish series itself. When com- the talar neck, and forefoot eburnation are higher in the 2nd–9th cen- pared with the data found within the Italian 10th–19th centuries CE turies CE group. Hypertrophic peroneal trochlea (PERTR) was present collection, significant differences increased in all variables apart from in all the populations. Despite low sample numbers (N = 55), Ras al- DISHN (Table 6). Hamra 5 demonstrated higher values than some Italian series (head/ neck of the talus displaced to medial plane, osteophytes along the cuboid articular surface to the lateral cuneiform, osteophytes in 4 | DI SCU SSION cuneiform-navicular joint, fused phalanges, forefoot eburnation) along with the least number of cases of calcaneal spur in the total collection. Results demonstrate the Italian and Spanish series having significant Contrasting each country by period (Table 6), Spanish populations differences between themselves and when compared by periods. Par- demonstrated differences in some variables (calcaneal spur and adoxically, the Spanish and Omani series do not show differences, 220 TABLE 3 Chi-square test and contingency coefficient values of the whole collection Variables OSTST PMSTA SPURC ACHIL CTOST FLACC PERTR TRART OMANK TTRNK LIPHD NECHD OCUCB N 366 361 320 327 365 336 259 339 431 426 422 424 240 Pearson χ 2 4.283 4.264 8.860 3.964 0.740 5.233 10.523 1.954 8.771 0.975 1.427 5.441 4.698 P value 0.117 0.119 0.012 0.138 0.691 0.073 0.005 0.376 0.012 0.614 0.490 0.066 0.095 Cont. Coef. 0.018 0.109 0.164 0.109 0.045 0.124 0.198 0.076 0.141 0.048 0.058 0.113 0.139 OHEAD DISHN EXTTT TRIGM TAILO TFOST CUBFC LPCUN COMMAS EXTUB FLCUC OCCJN CUNOS N 424 424 394 393 393 308 275 297 308 246 302 299 301 2 Pearson χ 0.860 6.295 5.543 4.432 1.286 5.244 4.086 0.723 4.061 1.362 2.749 4.653 8.560 p value 0.650 0.043 0.063 0.109 0.526 0.073 0.130 0.697 0.131 0.506 0.253 0.098 0.014 Cont. Coef. 0.045 0.122 0.118 0.106 0.057 0.129 0.121 0.049 0.114 0.074 0.095 0.125 0.166 ONCUN STFUS COALT MERGE EBRME EBANT OCDRT HVALG CCLOS OCMTT FRACT N 297 361 518 510 508 362 512 275 353 296 511 Pearson χ 2 17.443 3.324 0.249 11.456 3.732 12.607 1.941 5.123 0.021 0.853 3.716 p value 0.000 0.190 0.883 0.003 0.155 0.002 0.379 0.077 0.989 0.653 0.156 Cont. Coef. 0.236 0.096 0.022 0.148 0.085 0.183 0.061 0.135 0.008 0.054 0.085 Note. In bold are significant differences between countries/variables (p value) and the highest contingency coefficient. SALDÍAS ET AL. SALDÍAS ET AL. 221 F I G U R E 1 (a) Head/neck of the talus displaced to medial plane (DISHN). (b) Periosteal reaction in the talar neck (OMANK). (c) Forefoot eburnation (EBANT). (d) Fused phalanges (MERGE) [Colour figure can be viewed at wileyonlinelibrary.com] F I G U R E 2 (e) Calcaneal spur (SPURC). (f) Hypertrophic peroneal trochlea (PERTR). (g) Osteophytes in along cuboid articular surface to the lateral cuneiform (CUNOS). (h) Osteophytes in cuneiform-navicular joint (ONCUN) [Colour figure can be viewed at wileyonlinelibrary.com] TABLE 4 Chi-square test values: Significant differences between pairs of series Country Test SPURC PERTR OMANK DISHN CUNOS ONCUN MERGE EBANT Spain/Italy Pearson χ 2 6.268 9.726 8.788 4.068 8.433 16.763 11.675 8.729 p value 0.012 0.002 0.003 0.044 0.004 0.000 0.001 0.003 Spain/Oman Pearson χ 2 3.461 1.515 0.182 0.894 0.543 1.787 0.275 1.489 p value 0.063 0.218 0.669 0.344 0.461 0.181 0.600 0.222 Italy/Oman Pearson χ 2 1.037 0.015 1.872 6.385 3.929 3.759 7.767 14.217 p value 0.309 0.902 0.171 0.012 0.047 0.053 0.005 0.000 Note. Spanish, Italian, and Omani series are in bold. 222 TABLE 5 Frequencies of variables in studied populations, divided by sex, and estimated age range Spain II–IX CE Spain X–XIX CE Granollers Variables N Presence ♂ ♀ 18–39 40–69 +70 N Presence ♂ ♀ 18–39 40–69 +70 N Presence ♂ ♀ 18–39 40–69 +70 SPURC 66 11 7 4 3 8 0 95 30 11 2 4 7 0 31 21 10 11 0 8 11 16.6% 31,6% 67,7% PERTR 55 32 25 7 20 9 0 79 55 22 12 15 16 0 28 20 12 8 2 7 11 58,2% 69,6% 71,4% OMANK 77 4 3 1 1 2 0 123 19 5 3 5 3 0 31 10 6 4 0 4 4 5,2% 16,8% 32.3% DISHN 74 5 4 1 1 4 0 110 6 1 1 2 0 0 31 1 1 0 0 0 1 6.8% 5.5% 3.2% CUNOS 62 3 2 1 1 2 0 58 5 4 1 2 3 0 29 2 0 2 0 0 1 4.8% 8.6% 6.9% ONCUN 60 7 4 3 2 5 0 54 11 9 1 2 8 0 28 3 2 1 0 0 3 11.7% 20.4% 10.7% MERGE 88 4 2 2 1 2 0 123 1 1 0 1 0 0 32 8 4 4 0 3 4 4.5% 0.8% 25% EBANT 85 1 1 0 1 0 0 73 2 1 1 0 1 0 32 15 6 9 0 6 9 1.2% 2.7% 46.9% Italy II–IX CE Italy X–XIX CE Ras al-Hamra 5 Variables N Presence ♂ ♀ 18–39 40–69 +70 N Presence ♂ ♀ 18–39 40–69 +70 N Presence ♂ ♀ 18–39 40–69 +70 SPURC 48 11 5 4 2 7 0 67 11 10 1 4 4 0 13 1 1 0 0 1 0 22,9% 16,4% 7.7% PERTR 27 23 12 7 10 7 0 58 49 31 16 18 11 0 12 10 7 3 6 2 0 85,2% 84,5% 83,3% OMANK 98 7 3 2 3 1 0 79 3 3 0 1 1 0 33 4 1 2 1 2 0 7,1% 3.8% 12.1% DISHN 101 1 1 0 1 0 0 78 2 1 1 2 0 0 30 3 3 0 1 2 0 1.0% 2.6% 10% CUNOS 5 0 0 0 0 0 0 69 0% 0 0 0 0 0 31 1 1 0 0 1 0 0% 0% 3.2% ONCUN 48 0 0 0 0 0 0 74 1 1 0 0 1 0 33 2 2 0 1 1 0 0% 1.4% 6.1% SALDÍAS ET AL. SALDÍAS ET AL. 223 whereas the Italian versus Omani series show differences in half of +70 the variables. These results are very far from expectations, mainly due 0 0 40–69 to the Omani comparisons. The Spanish collections are not homogeneous among themselves as statistical differences can be found between the two periods. Con- 0 1 versely, the Italian series are statistically significant concerning the 18–39 pathological affectation and anatomical variables. Partially, it could be 0 3 due to the low number of individuals in each Italian series or possibly due to a specific lifestyle. This is the main problem of ♀ 0 2 paleoepidemiology: It is not always possible to select samples ♂ 2 4 according to their size or specific characteristics such as age, sex, social status, lifestyle, and so on. For this reason, it is seldom possible Presence Ras al-Hamra 5 16.2% to have a representative sample from a country, geographic area, or 3.6% period. Furthermore, stress and/or habitual activities could have 2 6 played a role with most of the incidences seen in the collections. We 55 37 N must therefore rely on the documented data of each archaeological site to explain these differences. +70 Overall, more males constituted the samples (59% vs. 36.4%) 0 0 having an average age range of 18–39 years. As Table 5 displays, bar- 40–69 ring exceptions, the frequency of variables was similar within each population. This could be explained by the different frequencies 0 1 among sexes and the shorter life expectancy from the period in which 18–39 each collection hailed from. 0 0 The significant differences found in this study might be due to specific activities of each population. Populations from the 10th–19th ♀ 0 0 centuries CE Italian group (Leopoli-Cencelle and Allumiere) lived dur- ing the same period, settled in similar geographic settings (irregular ♂ 0 1 soil), under the same cultural system, the result being low pathological Presence frequency. In contrast, the 10th–19th centuries CE Spanish group rev- Italy X–XIX CE 1.2% ealed a diversity of occupations, footwear, geography, and dates 0% 0 1 resulting in high pathological frequency; this could explain the obtained outcome. Furthermore, the calcaneal spur and periosteal 93 81 N reaction in the talar neck demonstrated significant differences in the +70 Spanish series, related to both occupational stress/lifestyle and human 0 0 variation within the muscles of the plantar vault. Footwear also could be an important socio-cultural factor to con- 40–69 sider that is able to influence the osteological alterations observed. 0 0 Ancient populations have less tendency to develop foot deformities than their modern counterparts, possibly related to inappropriate 18–39 footwear and an increase in life expectancy (Balint et al., 2003; 0 0 Haines & McDougall, 1954; Kapandji, 1998; Sorrentino et al., 2020). ♀ 0 1 Styles in footwear, its usage, and social context can change over time Note. Indeterminate individuals are excluded. depending on the historical period and culture, with their influence ♂ 0 0 being a catalyst in the higher occurrences of some foot diseases of their respective era. Frey et al. (1993) observed that pain and foot Presence deformities among modern women are mainly related to the use of 1.9% Italy II–IX CE 0% (Continued) shoes that are too small for their feet. Mays (2005), likewise, associ- 0 1 ated the influence of shoes/boots with the prevalence of hallux valgus 119 54 in different populations throughout human history, due to toe con- N striction (Haines & McDougall, 1954). Variables TABLE 5 MERGE In our study, the influence of the Roman Empire was important in EBANT the lifestyle of the individuals from Spain and Italy from the II–IX cen- turies CE series. Different models of Roman footwear (Van Driel- 224 SALDÍAS ET AL. TABLE 6 Chi-square test values: Spanish and Italian series divided by age Country/time Test SPURC PERTR OMANK DISHN CUNOS ONCUN MERGE EBANT Spain II–IX/X–XIX CE Pearson χ 2 4.563 1.863 5.811 0.133 0.689 1.619 3.089 0.515 p value 0.033 0.172 0.016 0.715 0.407 0.203 0.079 0.473 Italy II–IX/X–XIX CE Pearson χ 2 0.763 0.007 0.918 0.662 - 0.654 - 0.085 p value 0.382 0.933 0.338 0.416 - 0.419 - 0.771 Spain II–IX/Italy II–IX CE Pearson χ 2 0.697 5.979 0.278 4.289 2.584 5.988 5.516 0.106 p value 0.404 0.014 0.598 0.038 0.108 0.014 0.019 0.744 Spain X–XIX/Italy X–XIX CE Pearson χ 2 4.778 4.040 7.765 0.936 6.192 13.291 0.760 0.455 p value 0.029 0.044 0.005 0.333 0.013 0.000 0.383 0.500 Spain II–IX/X–XX CE Pearson χ 2 11.230 2.299 8.821 0.296 0.595 0.804 0.176 12.347 p value 0.001 0.129 0.003 0.587 0.441 0.370 0.675 0.000 Spain X–XX/Italy X–XX CE Pearson χ 2 11.611 4.170 11.084 0.734 5.813 11.063 5.603 11.701 p value 0.001 0.041 0.001 0.391 0.016 0.001 0.018 0.001 Cont. Coef. Spain/Italy X–XIX CE 0.238 0.157 0.218 0.058 0.190 0.257 0.149 0.243 Note. Significant p values are in bold. Contingency coefficient between Spain versus Italy X–XIX centuries CE and variables is in the last row. The strongest values are in black. Murray, 2001) existed with common elements. Several authors such centuries CE) a necropolis located near Termens castle, whose individ- as Croom (2010) and Van Driel-Murray (2001) indicated a series of uals are dated to 1830–1860 and correspond to an agricultural different designs (shoes, sandals and boots) that differed according to population. social status, activity, etc. Most Roman footwear were constructed Combining these two periods encompassing the Spanish from leather or vegetable sources such as palm fiber, straw, and reed collection (2nd–19th centuries CE) displays that almost all variables (Croom, 2010). These perishable materials (Fernández Ochoa (apart from head/neck of the talus displaced to medial plane and fused et al., 2018) are difficult to recover in archaeological sites in a well- phalanges; both being degenerative processes) demonstrated a higher preserved state. There is no accompanying archaeological information frequency of occurrence throughout the centuries. However, only the about footwear for our collections; therefore, we cannot categorically calcaneal spur (SPURC) and periosteal reaction in the talar neck relate its influence upon their pathologies. The only exception to this (OMANK) variables show significant differences. A calcaneal spur is is Granollers, a contemporary series with known sex and age. defined as a bone spicule in the proximal attachment of the fascia On the other hand, in detail, the Spanish collections (including plantar and is related to tensile and traction movement, for instance, both periods) correspond to ecclesiastic or rural lifestyles. St Pere high-stress activities like ballet or running (Weiss, 2012), and obesity (I and II), for example, commenced as a high social class necropolis of (Wearing et al., 2006). It can be also associated with microtrauma and bishops (2nd–9th centuries CE) (Ferran, 1987; Vives, 1990), repetitive tears (Benjamin et al., 2000), compression of the plantar fas- transitioning between the 9th and 12th centuries CE into a parish due cia by structural alteration of the foot vault, rheumatoid arthritis, and to a Muslim invasion. The status change of these churches possibly other seronegative spondyloarthritis (Bouysset et al., 2011). It is pre- allowed for more diversity in the social class of the buried, increasing sent in 16.6% of the 2nd–9th centuries CE group versus 31.6% of the the probability of the various foot pathologies observed. individuals from the 10th–19th centuries CE group. Individuals from the first Spanish period could possibly be linked The etiology of periosteal reaction in the talar neck (OMANK) is to a high social status where degenerative diseases caused by aging, not clear, however. It could be a reaction related to an overexertion of lifestyle habits, or shoe type could be responsible for the foot patholo- the dorsal talo-navicular ligament (Hansen, 2015), responsible for glid- gies on display. This data is supported by documents about secular ing movements in the foot. This zone is one of the most important and administrative functions performed by bishops and functionaries areas of impingement in the dorsiflexion of the ankle, which is also and includes female group data (53% of total population) that demon- involved in rotation and gliding motions (Magee, 2008). The periosteal strated low skeletal disorders (Jordana et al., 2010). Pathologies and reaction in the talar neck variable increased from 5.2% in the 2nd–9th entheses from the second period, however, could have more of a rela- centuries CE group to 16.8%, in the 10th–19th centuries CE group. tion to agricultural labor and their associated muscular stress induced Although statistically significant differences were not seen, almost all activities. variables (except head/neck of the talus displaced to medial plane and In contrast, the second period representing Spain includes fused phalanges; both degenerative processes) increased in frequency Avinganya (13th–17th centuries CE), a Trinitarian Monastery where a over time. high prevalence of osteoarthritis in females has been highlighted Lastly, within the Spanish collection, the Granollers/UAB collec- (74.1%) (Fuentes-Sánchez et al., 2016) and Termens, (18th–19th tion (Saldias et al., 2016) was analyzed in a separate group due to it SALDÍAS ET AL. 225 being dated to a later period (20th century CE) and with an average and/or similar frequencies between some of the variables from the sample age of over 70 years. Their age is important in understanding Italian series help to convey the uniformity seen in the results of the that their pathologies are derived from degenerative processes such analysis. as osteoarthritis and its secondary signs due to the age-related The Spanish and Italian series show compelling differences when increased risk of skeletal disorders (Glencross & Sawchuk, 2003) compared with one another. The 2nd–9th centuries CE group of both (Table 5). Being a more modern collection exhibits that footwear could collections exhibit significant differences in three variables (hypertro- be regarded as one of the main sources of stress in the Granollers phic peroneal trochlea, head/neck of the talus displaced to medial series as non-suitable footwear causes damage to the foot mostly in plane and osteophytes in the cuneiform-navicular joint). Interestingly, female population (Balint et al., 2003; Frey et al., 1993; Mays, 2005) the discrepancies between the 10th–19th centuries CE groups are as we observed here (Table 5). the greatest encountered within this study and have displayed signifi- The Italian series from the 2nd–9th centuries CE includes cant differences in most of the variables: entheses (calcaneal spur, populations with a probable mixture of lifestyles, who lived in the final hypertrophic peroneal trochlea), musculoskeletal activity markers years of the Roman and Byzantine Empires. At Crypta Balbi, the (periosteal reaction in the talar neck), and degenerative processes stratigraphy and archaeological elements revealed site re-usage with (osteophytes in along cuboid articular surface to the lateral cuneiform, different functions over time. Bronze metalwork and glass were osteophytes in cuneiform-navicular joint). Overall, the highest fre- found, demonstrating industrial activities of Roman urban life quencies of these variables are exhibited within the Spanish popula- (Sagui, 1998). To perform these jobs, the use of constant physical tion, barring hypertrophic peroneal trochlea. force and manual dexterity is required, where one is in near- Hypertrophic peroneal trochlea (PERTR or retrotrochlear emi- permanent contact with heat to melt the materials. To transfer heavy nence) was the variable with the highest overall presence throughout metal elements, the foot needs to make a greater effort in the fascia the analysis. This feature arises due to the subluxation of the peroneal plantar and longitudinal arch to stabilize the body. tendons or chronic peroneal tendonitis, activities that could have pos- Likewise, Villa Gordiani showed a high presence of males (66.7%) sibly been common in the Italian series (II–XIX CE), whose individuals and the highest population between 18 and 39 years old (80%). demonstrated the highest incidence of this variable from our Archaeological findings have been associated with Roman imperial collections. families (Palombi & Leone, 2008). According to the social status of the By incorporating the Granollers collection into the Spanish collec- individuals, their foot features could be related to their affluent life, tion, the differences between the Spanish and Italian series increased including diet and genetics. (Table 6), with age being a major factor. This is due to degenerative The rest of the series from the first group (2nd–9th CE centuries) diseases, such as osteoarthritis (osteophytes along the cuboid articular are located in the current city of Rome and Castro dei Volsci (Baldoni surface to the lateral cuneiform, osteophytes in cuneiform-navicular et al., 2016; Baldoni, Ferrito, & Martinez-Labarga, 2018; Rothschild joint, forefoot eburnation, fused phalanges), whose frequencies were et al., 2004; Rubini & Mogliazza, 2005). Their lifestyles are related to higher in Spanish populations. agriculture, animal husbandry, farming, and pastoral activities, which The last country analyzed was the Sultanate of Oman. Ras al- were the basis of their economy. In the particular case of Castro dei Hamra 5 is a Neolithic series (3700–3400 centuries BCE) of sedentary Volsci, previous anthropological reports (Rubini, 2009) indicated the fishermen who inhabited the Arabian coast (Coppa et al., 1985; Coppa evidence of notorious muscular insertions and small number of et al., 1990). They collected mollusks from mangrove swamps and pathologies related to traumas. other sea resources. The individuals analyzed in our study present dif- Regarding the Italian series from the 10th–19th centuries, ferent degrees of spina bifida (Coppa, 2012), and according to Swa- Leopoli-Cencelle (9th–15th centuries CE) and Allumiere (15th–16th roop and Dias (2011), a correlation between severe degrees of spina centuries CE) demonstrated a low number of cases in all variables, bifida and joint deformations has been observed. RH5 individuals dis- exception being the calcaneal spur and hypertrophic peroneal troch- play the highest frequency of head/neck of the talus displaced to lea. It is possible that similar stratigraphy (mountainous terrains) could medial plane of the entire series (10%), along with a significant num- influence the results. Allumiere was a mining city with a high percent- ber of hypertrophic peroneal trochlea (83.3%), and low percentage of age of males (Baldoni, Scorrano, et al., 2018). As an aftereffect due to forefoot eburnation (16.2%). Despite Ras al-Hamra 5 and the Spanish the high stress load of extracting and processing alum, robust bones series belonging to different chronological and geographical periods were observed in the collection; individuals developed musculoskele- and having marked differences in physical activity patterns, results are tal activity markers that correspond with this repetitive action. Addi- similar. tionally, they observed that workers who participated in the Summarizing, we found significant differences between countries excavation, moistening, and lixiviation stages developed osteoarthritis and periods in the frequencies of degenerative processes, entheses in their feet (Baldoni, Scorrano, et al., 2018). and normal variability, which could be produced by diverse factors. Statistically, significant differences were not found within the Furthermore, we found an increase in the frequencies of the variables Italian series despite their occupations. Considering stress inducing with significant differences from Spain (calcaneal spur and periosteal mining activities in Allumiere, it is possible that the miners developed reaction in the talar neck), and uniform results among Italian collec- other pathologies without statistically significant differences. The low tions. During the 10th–19th centuries CE, Spanish and Italian samples 226 SALDÍAS ET AL. demonstrated divergences in most of the variables, whose frequencies ACKNOWLEDG MENTS are higher in the Spanish population, except for the presence of We would like to thank to Antonio Moro from Museu de Terrassa, hypertrophic peroneal trochlea. There are clear differences among the Nuria Montes and Eulàlia Subirà from Unitat d'Antropologia of ecclesiastic and rural lifestyles in the Spanish series, whereas in the Universitat Autònoma de Barcelona for access to the Esglesies de Italian series, the differences are not as visible between the Sant Pere and the Avinganya series. To Gianluca Zanzi from agricultural and physical work lifestyles. Sovrintendenza Capitolina ai Beni Culturali di Roma Capitale, and Granollers and RH5 are series with particular features. Despite Marica Baldoni from Tor Vergata University of Rome for the access to the small sample size, they demonstrated high frequencies of some some Italian collections and information from Villa Gordiani. In addi- variables. Old age/footwear and endogamy might explain these fre- tion, we want to thank CONICYT PAI/2014-73130722 (ES) and quencies. Finally, most of the significant variables correspond to  d'Ajuts Universitaris i de Recerca, Spain Agència de Gestio degenerative processes, some of which increased their frequencies (2017SGR1630) for their financial support. across time, particularly in the Spanish series. CONFLIC T OF INT ER E ST None. 5 | C O N CL U S I O N S DATA AVAILABILITY STAT EMEN T Recent geographic and temporal human foot variability has not been The data that support the findings of this study are available from the widely studied in paleopathology. The present study shows a compar- corresponding author upon reasonable request. ative view of this topic from two regions, Catalonia, Spain and Lazio, Italy. Overall, both populations share a relatively similar history within OR CID the last two millennia as southwestern European countries. However, Eduardo Saldías https://orcid.org/0000-0003-4087-6675 when compared on a smaller scale such as from town to town, pro- Albert Isidro https://orcid.org/0000-0001-8784-2945 nounced differences are observed. From the 26 pathological conditions and five musculoskeletal RE FE RE NCE S activity markers present in the samples, only eight differences were Albee, M. E. (2020). Diagnosing tarsal coalition in medieval Exeter. Interna- found to differ significantly between countries. They correspond to tional Journal of Paleopathology, 28, 32–41. https://doi.org/10.1016/j. osteophytes in cuneiforms (in cuneiform-navicular joint, and along ijpp.2019.11.005 Anderson, T. (2004). The treatment of the feet in medieval Britain. The cuboid articular surface to the lateral cuneiform) alteration of the neck Foot, 14, 61–67. https://doi.org/10.1016/j.foot.2003.10.005 of the talus (displaced to medial plane), localized bone damage (fused Baldoni, M. (2019). Beyond the autopsy table: The potentials of a forensic phalanges, forefoot eburnation), musculoskeletal activity markers anthropology approach for biological profiling of unknown skeletal (periosteal reaction in the talar neck), and some entheses (calcaneal individuals from ancient. A morphological, metric and isotopic analysis spur, hypertrophic peroneal trochlea). These differences seem to be of the Medieval population of Leopoli-Cence. Università degli Studi di Roma “Tor Vergata.” related to activities of specific populations, their occupations and/or Baldoni, M., Ferrito, G., & Martinez-Labarga, C. (2018). 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