- Email: [email protected]
Which Theory for the Origin of Syphilis Is True?
3112
SEXUAL MEDICINE HISTORY Which Theory for the Origin of Syphilis Is True? Ivana Anteric, MSc,* Zeljana Basic, MSc,* Katarina Vilovic, PhD, MD,† Kresimir Kolic, MD,‡ and Simun Andjelinovic, PhD, MD*§ *University Department for Forensic Sciences, University of Split, Split, Croatia; †School of Medicine, Department of Anatomy, Histology, and Embryology, University of Split, Split, Croatia; ‡Clinical Department for Diagnostic and Interventional Radiology, Clinical Hospital Center Split, Split, Croatia; §Clinical Institute for Pathology, Forensic Medicine, and Cytology, Clinical Hospital Center Split, Split, Croatia DOI: 10.1111/jsm.12674
ABSTRACT
Introduction. There are four theories about the origin of syphilis, of which the mostly represented one is the Columbian theory. This theory suggests that syphilis was brought into Europe in 1493 ad by the ship from Caribbean islands. Aim. The aim of this study is to test all theories on a sample of 403 skeletons: 135 from prehistory, 134 from antique, and 134 from medieval period and new age from the Dalmatia (Croatia). Methods. All skeletons were examined using standard anthropological methods. Paleopathological analysis was performed on each skeleton as well as additional radiographic method on one isolated skeleton. Main Outcome Measures. Paleopathological changes on skeletal remains connected with treponematosis. Results. Paleopathological analysis revealed one skeleton from the antique period (second to 6th century ad) that exhibited skeletal markers similar to those described in one clinical case in which congenital syphilis was confirmed by a Wasserman reaction. Skeletal remains of this person were examined macroscopically and radiographically, and the differential diagnostics eliminated other considered pathologies as well as trauma. Conclusions. The finding of skeletal markers of syphilis on a skeleton from the antique supports the theory of pre-Columbian syphilis origin. Anteric I, Basic Z, Vilovic K, Kolic K, and Andjelinovic S. Which theory for the origin of syphilis is true? J Sex Med 2014;11:3112–3118. Key Words. Dalmatia (Croatia); Treponematosis; Syphilis; Pre-Columbian Theory; Paleopathology
Introduction
S
yphilis is a systematic disease with various clinical manifestations caused by bacteria Spirochaete Treponema Pallidum. It is most often transmitted sexually and congenitally, but in some world parts, it is an endemic nonvenereal disease. One of the most controversial issues considering syphilis is the origin of syphilis. There are three major theories that try to explain its origin and rapid expansion through Europe at the end of the 15th century. The first theory assumes that syphilis was brought into Europe in 1493 ad by the ship from Caribbean islands—this theory is called the Columbian theory. The second theory assumes
J Sex Med 2014;11:3112–3118
that syphilis was first present in Africa and was brought by slaves to Spain and Portugal. The third theory assumes that syphilis was present for a long time in the old and new worlds and that, depending on the geographical area, four different syndromes developed [1]. There are four different types of treponematosis (bacterial infection caused by bacterial species Treponema): venereal syphilis (gained or congenital), frambesia, pinta, and endemic syphilis (bejel). All but pinta can leave marks on bones [2]. Despite all the theories, the origin of the disease is still an enigma [3]. The aim of this research is to test these three theories by examination of the syphilis marks on osteological material from the Dalmatian area © 2014 International Society for Sexual Medicine
Syphilis Origin Reexamined (Croatia) from different historical periods. By examination of the “And¯elinovic´” osteological collection with around 3,000 skeletons dated from prehistory to new age, we will try to find an answer about the origin and expansion of syphilis. For purposes of this study, a random sample of 403 skeletons was examined: 135 from prehistory, 134 from antique, and 134 from medieval period and new age. Prehistory and antique sample are chosen as a control group given that the most accepted theory (Columbian) about the origin of syphilis supports the fact that syphilitic changes will be found on skeletons dated after the 15th century. All skeletal remains included in this study are found in present-day Dalmatian territory, which was inherited in the past due to its favorable geographic location and mild climate. Because of turbulent history caused by numerous migrations, historical turmoil, merchandise, and idea exchange, it can be expected that various diseases that affected Europe and the world will also be seen on skeletal remains from this area. Until now in the area of present-day Croatia, anthropological research of archeological populations produced only one case of syphilis—venereal syphilis was found on a female skeleton from 15th to 17th century ad [2]. Materials and Methods
Archeological Context Osteological material analyzed in this study was recovered from prehistoric, antique, medieval, and new age excavation sites. The prehistory sample is composed of skeletal remains from five excavation sites archeologically dated to the Iron Age. A total of 52 graves were anthropologically analyzed (18 from Nadin flat necropolis, 28 from necropolis Ljubacˇ-venac, four from Jokina glavica, one from Duševic´a glavica, and one from Ljubacˇ-barrow 4), and a total of 135 skeletons were examined [4]. This area was populated by the Liburns, one of the Illyrian tribes. They inherited the area of northern Dalmatia from 12/11 century bc until the Roman arrival in this area. During that time, they lived in clans. In 9th century bc, they isolated as a separate community which differed from the rest of the Illyrian tribes by social and cultural practices. It is believed that this was a reflection of strong pre-Indo European influences. The community was also specific by the female importance in the society that was unusual for that time period. Maternal kinship was very important, and the community had a female-
3113 maintained ancestor cult. They used a special technique for wooden boat production—wood was not attached with pins but was sawed by ropes using a special technique. Their big war ships (Liburns) were used by Romans as part of their war fleet. The antique sample is composed of a sample from the excavation site Solin-Smiljanovac. More than 1,000 graves were excavated at this site, and by random computer sampling, 134 individuals were chosen for analysis. Solin-Smiljanovac was a great necropolis of antique Salona, the metropolis of the Roman province of Dalmatia. Salona was a coastal stronghold and port of Illyrian Delmats. In that time in Salona, besides the Illyrians and inhabitants from Greece, a large number of Italic also lived there. After the civil war between Caesar and Pompei in 48 bc, Salona, who sided with Caesar, became a Roman colony with full name Colonia Martia Ivlia Salona and became the centre of the Roman province of Illyricum, later a province of Dalmatia. After the Illyrian rebellion was suppressed (Baton rebellion that lasted from 6th to 9th year ad), a period of peace and prosperity occurred, mostly seen through its urban development and strong building activity. According to the Roman custom, outside the city walls, alongside the roads leading from the city, four necropolis were built: western, eastern, northern, and southeastern. The medieval and new age samples consist of skeletons from two excavation sites. From the late medieval excavation site Kamen Most Kaldrma (dated in 14th–15th century ad), 31 skeletons were analyzed [5], and from late medieval/new age excavation site Saint Catherine (dated in 16th–19th century), 103 skeletons were analyzed [6]. Kamen Most Kaldrma is a medieval cemetery situated in a location of present-day Kamen, most of which was inherited during the antique period. Graves were oriented in an east–west direction and were regularly situated, which indicates that other tombstones besides the one found at the site were present at the time. Most of the diseased were put in a barrow without architecture, and eight graves were covered by stone sheets. Although there were no burial findings, the burial image and tombstone revelation dates this excavation site to the late medieval period, to the14th–15th century ad. The cemetery in the Dominican monastery of Saint Catherine (town Split) is dated by archeological findings (ceramics, crown pearls from bone, glass, etc) in the second half and the end of 16th century ad. The last time period in which inhumation was allowed in the town environment was J Sex Med 2014;11:3112–3118
3114
Anteric et al.
the beginning of the 19th century. Both the members of monastery community and newcomers (for a period of time, a monastery used as a lazaretto) were buried in this graveyard. This was a mass burial, with the minimum number of 103 individuals buried at this graveyard.
Paleopathological Analysis All skeletal remains were examined for osteological markers of venereal or congenital syphilis. Endemic syphilis (bejel) was not considered during analysis as it is not characteristic for this climate area and affects only children. Frambesia was not considered during analysis as it is not characteristic for this climate, and pinta was excluded because it does not leave marks on bones. Venereal syphilis is caused by acute, subacute, or chronic treponematosis. It is manifested in three stages: primary (ulcer on genital area), secondary (characterized by rash), and tertiary (which usually appears years after primary infection). On osteological material, the following changes are visible: lesions on tibia, skull (parietal and frontal bone), nasal–palatal region, sternum, clavicle, vertebra, femur, fibula, humerus, ulna, and radius. In 10–20% of cases, gummatous and nongummatous lesions are visible. Nongummatous lesions include periostitis, osteitis, and osteoperiostitis and are usually seen on tibia (saber shin), fibula, clavicle, femur, ulna, and radius. A bilateral lesion on the tibia is strong evidence of tertiary syphilis. Gummatous lesions are seen in later syphilis phases on the skull and long bones. They can be recognized macroscopically by thickened cortex and rough outer surfaces. It often affects the joints, most often the knee. It can be recognized by osteophytes, eburnation, and destruction of joint surface. Syphilis can appear similar to other types of lesions, and therefore, it is necessary to exclude tumors, infections (tuberculosis, pyogenic osteomyelitis), and Paget disease [7]. Table 1
Congenital syphilis develops as a result of a bacterial transmission from mother to fetus. This infection often leads to abortion, while in milder cases, bacteria may remain inactive for some years. On bone material, it often manifests as osteohondritis, periostitis, and osteitis. Later forms of the disease can manifest as nongummatous periostitis (most often on long bone diaphysis, mostly on tibia), gummatous osteomyelitis (most often on tibia, rarely on facial bones), dactilitis (more often on hand fingers), joint pathology (syphilitic arthritis, most often on a knee), and dental pathology [7]. Results
A total of 403 skeletons were examined for signs of venereal or congenital syphilis: 89 female, 149 male, 45 adults of an unknown sex, and 120 children. The number of individuals by excavation site is listed in Table 1. Of all analyzed skeletons, only one had anomalies that required further analysis to include or exclude connection with treponemal infection. This skeleton was found on the antique excavation site Solin-Smiljanovac in grave 210. Using anthropological methods for sex and age determination [8–10], we concluded that this individual was a male 20–29 years old. Examination of dental material showed signs of enamel hypoplasia and periodontitis. Mild osteoarthritis signs are visible on vertebra. There is also a marked bowing of the left femur (Figure 1). The left femur is curved, with the medial part of femur being flattened, almost flat, and orthogonal. It is approximately 10 cm shorter than other femur (partially fragmented). The point of greatest convexity is 13.6 cm below the femoral head. The sagittal diameter of the left femur at the point of greatest convexity is 23.5 mm and transversal is 46 mm. The left femur was shorter than the right. There are no visible signs of
Demographic characteristics by excavation sites Excavation site
Sex distribution Female Male Sex unknown (adult) Child Total
LjubacˇNekropola Venac
Nadin-Nekropola Na Ravnom
Duševic´a Glavica
Jokina Glavica
Ljubacˇ Tumul 4
Solin Smiljanovac
Kamenmost Kaldrma
St. Katarina Monastery
Total
24 35 9
5 9 9
1 1 0
1 0 1
1 0 0
25 66 8
13 16 0
19 22 18
89 149 45
16 84
21 44
0 2
2 4
0 1
35 134
2 31
44 103
120 403
J Sex Med 2014;11:3112–3118
3115
Syphilis Origin Reexamined
lar areas of osteoporosis and osteosclerosis in the middle part of the tibia and discrete periostal thickening (hyperostosis) with slight obliteration of the medullary cavity (Figure 4). Discussion
Figure 1 Photo of the left and right femora.
The described case is one which calls for discussion or elaborate differential diagnosis. First, the bone was examined for possible signs of ante mortem trauma. No osteological markers of trauma were visible, including those on the radiographs. After we excluded trauma as a cause of changes observed on the femur and tibia, we used differential diagnosis to narrow down the possible cause of the following disease. A literature search for conditions that can cause observed changes revealed the following: Paget disease, unilateral femoral hypoplasia, and syphilis hereditaria tarda of femur. Paget’s disease of bone is a chronic affliction of the adult skeleton with areas of aggressive osteoclast-mediated bone resorption preceding imperfect osteoblast-mediated bone repair. It usually manifests in middle or advanced age and is slightly more common in men [11,12]. It usually involves one bone (monostotic) or a few bones (polyostotic), usually affecting the skull or pelvis, or a vertebra, femur, or tibia [12,13]. Osteolytic fronts progress approximately 1 cm yearly [14]. Cortical thickening (hyperostosis), disorganized coarse trabeculae (osteosclerosis), and bone expansion can be seen. In advanced stages of the disease, bones are widened and heterogeneously ossified [15]. Most clinical manifestations are skeletal [16], but the prevalence of various signs and symptoms and complications is uncertain [17]. The bowing of the femur is anterior and lateral and usually
Figure 2 Radiograph of the left and right femora.
trauma. Radiograph exam shows alternating, irregular areas of osteoporosis and osteosclerosis in the middle part of the femur and discrete periostal thickening (hyperostosis) with slight obliteration of the medullary cavity (Figure 2). The right tibia also has a specific curved appearance, especially in the anterior–posterior plane (Figure 3). Periostitis on the right tibia led to excessive new bone growth on the anterior surfaces and anterior bowing, or characteristic saber shin. Radiograph exam shows alternating, irregu-
Figure 3 Photo of the left and right tibia.
J Sex Med 2014;11:3112–3118
3116
Figure 4 Radiograph of the left and right tibia.
involves most of the femoral shaft. Paget disease has a characteristic appearance on radiographs with coarsened trabeculae and thickening of the cortex. Also, Looser’s zones may form which are inadequately healed stress fractures. Unilateral femoral hypoplasia is a disorder which clinically manifests as a short femur. It has been suggested that coxa vara and the short femur are variations of the same congenital anomaly [18]. If coxa vara is absent, it is considered to be simple hypoplasia of the femur. In this condition, broadening of the upper epiphyseal cartilage of the femur and an area of cortical sclerosis and bowing can be seen. In the early stages of femoral development, an excessive formation of new bone can be seen, but growth in breadth of the femur is not disturbed. Broadening of the upper epiphyseal plate indicates a failure of the metaphysis to replace cartilage by bone. Probably, a delay in ossification and bone bowing is a result of the primary defect of the cartilage [19]. Through literature search, we found an interesting case of syphilis hereditaria tarda of femur J Sex Med 2014;11:3112–3118
Anteric et al. on living patient. Diagnosis of syphilis was made using a positive Wassermann reaction. The illness affected the femur on which no inflammatory manifestations, areas of softening, or sinuses were found. The following changes were found: an increase in diameter of the upper half of the femur, obliteration of the medullary cavity, alternating areas of osteoporosis and osteosclerosis, and the line of an incomplete fracture at the point of greatest convexity of the femur [20]. By examination of the osteological findings on the femur and Davis’ description of the manifestation of syphilis hereditaria tarda in this clinical case, as well as by examination of radiographs of the bone and living patient, it is visible that the skeletal features share a resemblance. Both femurs are mostly curved on the upper diaphysis part, flattened, and have an increased bone diameter in the mentioned area. Considering that radiographs did not reveal cortex thickening or coarsened trabeculae characteristic for Paget disease, as well as no signs of broadening of the upper epiphyseal plate characteristic for unilateral femoral hypoplasia are visible, these two pathologies can be excluded as a potential reason for observed skeletal changes. Gummatous lesions have not been observed on this individual, but a nongummatous lesion on tibia (saber shin) has been seen. The examination of femur revealed the resemblance with previously published paper in which the similar changes were noticed on patients’ femur and the treponemal infection confirmed by the Wasserman test [20]. This only additionally confirmed the assumption that the findings on femur and tibia are caused by the treponemal infection, which was not in advanced state in this individual and did not affect other bones. Many theories support the existence of syphilis before 1492. Pales believes that syphilis (as well as osteomyelitis, spondylitis, and tumors) existed in ancient times, while Cockburn believes that treponematosis in the past differed from current treponematosis given that, historically, a smaller number of people lived in one area [21]. There is some written material that suggests that syphilis infected ancient Chinese dynasties and that Augustus Caesar was afflicted by hereditary syphilis, but all of this data are unconfirmed [22]. Existence of venereal syphilis in Italy 600 bc is discussed by Dr. Mattie Hennenberg and his wife [23]. Because of everything just stated, we believe that the Columbian theory of syphilis origin is not sustainable. Syphilis was most likely present in the
3117
Syphilis Origin Reexamined old world, but not to the extent that it was in post-Columbian time. It is interesting and indicative that no evidence of syphilis was found in graveyards from post-Columbian time in this research, and in the territory of present-day Croatia, only few cases of probably syphilis were published. All evidence supports the theory that syphilis is not a new illness, but its manifestations were randomly recorded or misclassified. Tanya et al. (cited in Von Hunnius et al.) state that skeletal evidence from recent excavations in Europe pushed back the clock concerning a preColumbian presence of syphilis in the Old World. They believe that more excavations with more skeletons examined will support the syphilis or treponemal precursors prior to 1492 [24]. As syphilis remains an international, still growing disease [3], paleopathological analysis can give a new insight into its origin. Acknowledgments
We would like to express our gratitude to Brunislav Marjanovic´, Sineva Kukoc´, Slavko Galiot, Helga Martinac, and Ljubomir Gudelj for providing osteological material and data about archeological findings. We would also like to thank Ayano Rachel Fox for valuable comments and suggestions on the manuscript language. This research was supported by the Ministry of Science, Education and Sports of the Republic of Croatia Grant No. 258 – 2160800 – 033. Corresponding Author: Ivana Anteric, MSc, University Department for Forensic Sciences, University of Split, Rudjera Boskovica 31, Split 21000, Croatia. Tel: 0038521417001; Fax: 0038521417001; E-mail: [email protected] Conflict of Interest: The author(s) report no conflicts of interest. Statement of Authorship
Category 1 (a) Conception and Design Ivana Anteric; Zeljana Basic; Katarina Vilovic; Kresimir Kolic; Simun Andjelinovic (b) Acquisition of Data Ivana Anteric; Zeljana Basic; Simun Andjelinovic (c) Analysis and Interpretation of Data Ivana Anteric; Zeljana Basic; Katarina Vilovic; Kresimir Kolic; Simun Andjelinovic
Category 2 (a) Drafting the Article Ivana Anteric; Zeljana Basic; Kresimir Kolic; Simun Andjelinovic
(b) Revising It for Intellectual Content Ivana Anteric; Zeljana Basic; Katarina Vilovic; Kresimir Kolic; Simun Andjelinovic
Category 3 (a) Final Approval of the Completed Article Ivana Anteric; Zeljana Basic; Katarina Vilovic; Kresimir Kolic; Simun Andjelinovic References 1 Cartwright FF, Biddiss M. Bolest i povijest. Zagreb: Naklada Ljevak; 2006. 2 Šlaus M, Novak M. A case of venereal syphilis in the modern age horizon of graves near the church of St. Lawrence in Crkvari. Pril Inst Arheol Zagrebu 2007;24:503–10. 3 Maatouk I, Moutran R. History of syphilis: Between poetry and medicine. J Sex Med 2014;11:307–10. doi: 10.1111/ jsm.12354. 4 Anteric´ I, Bašic´ Ž, And¯elinovic´ Š. Nadin—Results of the anthropological analysis of the Liburnian population. Asseria 2011;9:75–112. 5 And¯elinovic´ Š, Drnasin Ž, Anteric´ I, Škoric´ E, Becˇic´ K. Antropological analysis of osteological material from late medieval location Kamen Most—Kaldrma (in Croatian). In: Šeparovic´ T, ed. Zbornik radova, Znanstveni skup Stjepan Gunjacˇa. Split: Muzej hrvatskih arheoloških spomenika; 2010:451–62. 6 Bašic´ Ž, Anteric´ I, Škoric´ E, Vilovic´ K, And¯elinovic´ Š. Split from the 16th to 19th century through the prism of anthropological research (in Croatian). ShP 2011;38:329–53. 7 Aufderheide AC, Rodríguez-Martín C, Langsjoen O. The Cambridge encyclopedia of human paleopathology. Cambridge: Cambridge University Press; 1998. 8 Krogman WM, Iscan MY. The human skeleton in forensic medicine. Springfield: Charles C. Thomas; 1986. 9 Bass WM. Human osteology. Columbia: Missouri Archaeological Society; 1987. 10 Ubelaker DH. Human skeletal remains: Excavation, analysis, interpretation. Washington, DC: Taraxacum; 1999. 11 Paget J. On a form of chronic inflammation of bones (osteitis deformans). Med Chir Trans 1877;60:37–63. 12 Kanis J. Pathophysiology and treatment of Paget’s disease of bone. London: Martin Dunitz; 1998. 13 Altman RD. Paget’s disease of bone. Disorders of bone and mineral metabolism. In: Coe FL, Favus MJ, eds. Disorders of bone and mineral metabolism. Philadelphia: Lippincott Williams & Wilkins; 2002:1020–2002. 14 Doyle FH, Banks LM, Pennock JM. Radiologic observations on bone resorption in Paget’s disease. Arthritis Rheum 1980;23:1205–14. 15 Smith SE, Murphey MD, Motamedi K, Mulligan ME, Resnik CS, Gannon FH. Radiologic spectrum of Paget disease of bone and its complications with pathologic correlation. Radiographics 2001;22:1191–216. 16 Altman RD. Musculoskeletal manifestations of Paget’s disease of bone. Arthritis Rheum 1980;23:1121–7. 17 Selby PL, Davie MW, Ralston SH, Stone MD. Guidelines on the management of Paget’s disease of bone. Bone 2002;31:366–73. 18 Golding FC. Congenital coxa vara and the short femur. Proc R Soc Med 1938;32:641–6. 19 Ring PA. Congenital short femur simple femoral hypoplasia. J Bone Joint Surg 1959;41:75–8. 20 Davis GG. Transactions of the Philadelphia academy of surgery, stated meeting held October 7, 1912. Available at:
J Sex Med 2014;11:3112–3118
3118 http://www.academyofsurgery.org/1908December.pdf (accessed September 25, 2012). 21 Cockburn TA. The origin of the treponematoses. Bull World Health Organ 1961;24:221–8. Geneva. 22 Pearce J. A note on the origins of syphilis. J Neurol Neurosurg Psychiatry 1998;64:542–7.
J Sex Med 2014;11:3112–3118
Anteric et al. 23 Morton RS, Rashid S. The syphilis enigma: The riddle resolved? Sex Transm Infect 2001;77:322–4. doi: 10.1136/ sti.77.5.322. 24 Von Hunnius TE, Roberts CA, Boylston A, Saunders SR. Histological identification of syphilis in pre-Columbian England. Am J Phys Anthropol 2006;129:559–66.
SEXUAL MEDICINE HISTORY Which Theory for the Origin of Syphilis Is True? Ivana Anteric, MSc,* Zeljana Basic, MSc,* Katarina Vilovic, PhD, MD,† Kresimir Kolic, MD,‡ and Simun Andjelinovic, PhD, MD*§ *University Department for Forensic Sciences, University of Split, Split, Croatia; †School of Medicine, Department of Anatomy, Histology, and Embryology, University of Split, Split, Croatia; ‡Clinical Department for Diagnostic and Interventional Radiology, Clinical Hospital Center Split, Split, Croatia; §Clinical Institute for Pathology, Forensic Medicine, and Cytology, Clinical Hospital Center Split, Split, Croatia DOI: 10.1111/jsm.12674
ABSTRACT
Introduction. There are four theories about the origin of syphilis, of which the mostly represented one is the Columbian theory. This theory suggests that syphilis was brought into Europe in 1493 ad by the ship from Caribbean islands. Aim. The aim of this study is to test all theories on a sample of 403 skeletons: 135 from prehistory, 134 from antique, and 134 from medieval period and new age from the Dalmatia (Croatia). Methods. All skeletons were examined using standard anthropological methods. Paleopathological analysis was performed on each skeleton as well as additional radiographic method on one isolated skeleton. Main Outcome Measures. Paleopathological changes on skeletal remains connected with treponematosis. Results. Paleopathological analysis revealed one skeleton from the antique period (second to 6th century ad) that exhibited skeletal markers similar to those described in one clinical case in which congenital syphilis was confirmed by a Wasserman reaction. Skeletal remains of this person were examined macroscopically and radiographically, and the differential diagnostics eliminated other considered pathologies as well as trauma. Conclusions. The finding of skeletal markers of syphilis on a skeleton from the antique supports the theory of pre-Columbian syphilis origin. Anteric I, Basic Z, Vilovic K, Kolic K, and Andjelinovic S. Which theory for the origin of syphilis is true? J Sex Med 2014;11:3112–3118. Key Words. Dalmatia (Croatia); Treponematosis; Syphilis; Pre-Columbian Theory; Paleopathology
Introduction
S
yphilis is a systematic disease with various clinical manifestations caused by bacteria Spirochaete Treponema Pallidum. It is most often transmitted sexually and congenitally, but in some world parts, it is an endemic nonvenereal disease. One of the most controversial issues considering syphilis is the origin of syphilis. There are three major theories that try to explain its origin and rapid expansion through Europe at the end of the 15th century. The first theory assumes that syphilis was brought into Europe in 1493 ad by the ship from Caribbean islands—this theory is called the Columbian theory. The second theory assumes
J Sex Med 2014;11:3112–3118
that syphilis was first present in Africa and was brought by slaves to Spain and Portugal. The third theory assumes that syphilis was present for a long time in the old and new worlds and that, depending on the geographical area, four different syndromes developed [1]. There are four different types of treponematosis (bacterial infection caused by bacterial species Treponema): venereal syphilis (gained or congenital), frambesia, pinta, and endemic syphilis (bejel). All but pinta can leave marks on bones [2]. Despite all the theories, the origin of the disease is still an enigma [3]. The aim of this research is to test these three theories by examination of the syphilis marks on osteological material from the Dalmatian area © 2014 International Society for Sexual Medicine
Syphilis Origin Reexamined (Croatia) from different historical periods. By examination of the “And¯elinovic´” osteological collection with around 3,000 skeletons dated from prehistory to new age, we will try to find an answer about the origin and expansion of syphilis. For purposes of this study, a random sample of 403 skeletons was examined: 135 from prehistory, 134 from antique, and 134 from medieval period and new age. Prehistory and antique sample are chosen as a control group given that the most accepted theory (Columbian) about the origin of syphilis supports the fact that syphilitic changes will be found on skeletons dated after the 15th century. All skeletal remains included in this study are found in present-day Dalmatian territory, which was inherited in the past due to its favorable geographic location and mild climate. Because of turbulent history caused by numerous migrations, historical turmoil, merchandise, and idea exchange, it can be expected that various diseases that affected Europe and the world will also be seen on skeletal remains from this area. Until now in the area of present-day Croatia, anthropological research of archeological populations produced only one case of syphilis—venereal syphilis was found on a female skeleton from 15th to 17th century ad [2]. Materials and Methods
Archeological Context Osteological material analyzed in this study was recovered from prehistoric, antique, medieval, and new age excavation sites. The prehistory sample is composed of skeletal remains from five excavation sites archeologically dated to the Iron Age. A total of 52 graves were anthropologically analyzed (18 from Nadin flat necropolis, 28 from necropolis Ljubacˇ-venac, four from Jokina glavica, one from Duševic´a glavica, and one from Ljubacˇ-barrow 4), and a total of 135 skeletons were examined [4]. This area was populated by the Liburns, one of the Illyrian tribes. They inherited the area of northern Dalmatia from 12/11 century bc until the Roman arrival in this area. During that time, they lived in clans. In 9th century bc, they isolated as a separate community which differed from the rest of the Illyrian tribes by social and cultural practices. It is believed that this was a reflection of strong pre-Indo European influences. The community was also specific by the female importance in the society that was unusual for that time period. Maternal kinship was very important, and the community had a female-
3113 maintained ancestor cult. They used a special technique for wooden boat production—wood was not attached with pins but was sawed by ropes using a special technique. Their big war ships (Liburns) were used by Romans as part of their war fleet. The antique sample is composed of a sample from the excavation site Solin-Smiljanovac. More than 1,000 graves were excavated at this site, and by random computer sampling, 134 individuals were chosen for analysis. Solin-Smiljanovac was a great necropolis of antique Salona, the metropolis of the Roman province of Dalmatia. Salona was a coastal stronghold and port of Illyrian Delmats. In that time in Salona, besides the Illyrians and inhabitants from Greece, a large number of Italic also lived there. After the civil war between Caesar and Pompei in 48 bc, Salona, who sided with Caesar, became a Roman colony with full name Colonia Martia Ivlia Salona and became the centre of the Roman province of Illyricum, later a province of Dalmatia. After the Illyrian rebellion was suppressed (Baton rebellion that lasted from 6th to 9th year ad), a period of peace and prosperity occurred, mostly seen through its urban development and strong building activity. According to the Roman custom, outside the city walls, alongside the roads leading from the city, four necropolis were built: western, eastern, northern, and southeastern. The medieval and new age samples consist of skeletons from two excavation sites. From the late medieval excavation site Kamen Most Kaldrma (dated in 14th–15th century ad), 31 skeletons were analyzed [5], and from late medieval/new age excavation site Saint Catherine (dated in 16th–19th century), 103 skeletons were analyzed [6]. Kamen Most Kaldrma is a medieval cemetery situated in a location of present-day Kamen, most of which was inherited during the antique period. Graves were oriented in an east–west direction and were regularly situated, which indicates that other tombstones besides the one found at the site were present at the time. Most of the diseased were put in a barrow without architecture, and eight graves were covered by stone sheets. Although there were no burial findings, the burial image and tombstone revelation dates this excavation site to the late medieval period, to the14th–15th century ad. The cemetery in the Dominican monastery of Saint Catherine (town Split) is dated by archeological findings (ceramics, crown pearls from bone, glass, etc) in the second half and the end of 16th century ad. The last time period in which inhumation was allowed in the town environment was J Sex Med 2014;11:3112–3118
3114
Anteric et al.
the beginning of the 19th century. Both the members of monastery community and newcomers (for a period of time, a monastery used as a lazaretto) were buried in this graveyard. This was a mass burial, with the minimum number of 103 individuals buried at this graveyard.
Paleopathological Analysis All skeletal remains were examined for osteological markers of venereal or congenital syphilis. Endemic syphilis (bejel) was not considered during analysis as it is not characteristic for this climate area and affects only children. Frambesia was not considered during analysis as it is not characteristic for this climate, and pinta was excluded because it does not leave marks on bones. Venereal syphilis is caused by acute, subacute, or chronic treponematosis. It is manifested in three stages: primary (ulcer on genital area), secondary (characterized by rash), and tertiary (which usually appears years after primary infection). On osteological material, the following changes are visible: lesions on tibia, skull (parietal and frontal bone), nasal–palatal region, sternum, clavicle, vertebra, femur, fibula, humerus, ulna, and radius. In 10–20% of cases, gummatous and nongummatous lesions are visible. Nongummatous lesions include periostitis, osteitis, and osteoperiostitis and are usually seen on tibia (saber shin), fibula, clavicle, femur, ulna, and radius. A bilateral lesion on the tibia is strong evidence of tertiary syphilis. Gummatous lesions are seen in later syphilis phases on the skull and long bones. They can be recognized macroscopically by thickened cortex and rough outer surfaces. It often affects the joints, most often the knee. It can be recognized by osteophytes, eburnation, and destruction of joint surface. Syphilis can appear similar to other types of lesions, and therefore, it is necessary to exclude tumors, infections (tuberculosis, pyogenic osteomyelitis), and Paget disease [7]. Table 1
Congenital syphilis develops as a result of a bacterial transmission from mother to fetus. This infection often leads to abortion, while in milder cases, bacteria may remain inactive for some years. On bone material, it often manifests as osteohondritis, periostitis, and osteitis. Later forms of the disease can manifest as nongummatous periostitis (most often on long bone diaphysis, mostly on tibia), gummatous osteomyelitis (most often on tibia, rarely on facial bones), dactilitis (more often on hand fingers), joint pathology (syphilitic arthritis, most often on a knee), and dental pathology [7]. Results
A total of 403 skeletons were examined for signs of venereal or congenital syphilis: 89 female, 149 male, 45 adults of an unknown sex, and 120 children. The number of individuals by excavation site is listed in Table 1. Of all analyzed skeletons, only one had anomalies that required further analysis to include or exclude connection with treponemal infection. This skeleton was found on the antique excavation site Solin-Smiljanovac in grave 210. Using anthropological methods for sex and age determination [8–10], we concluded that this individual was a male 20–29 years old. Examination of dental material showed signs of enamel hypoplasia and periodontitis. Mild osteoarthritis signs are visible on vertebra. There is also a marked bowing of the left femur (Figure 1). The left femur is curved, with the medial part of femur being flattened, almost flat, and orthogonal. It is approximately 10 cm shorter than other femur (partially fragmented). The point of greatest convexity is 13.6 cm below the femoral head. The sagittal diameter of the left femur at the point of greatest convexity is 23.5 mm and transversal is 46 mm. The left femur was shorter than the right. There are no visible signs of
Demographic characteristics by excavation sites Excavation site
Sex distribution Female Male Sex unknown (adult) Child Total
LjubacˇNekropola Venac
Nadin-Nekropola Na Ravnom
Duševic´a Glavica
Jokina Glavica
Ljubacˇ Tumul 4
Solin Smiljanovac
Kamenmost Kaldrma
St. Katarina Monastery
Total
24 35 9
5 9 9
1 1 0
1 0 1
1 0 0
25 66 8
13 16 0
19 22 18
89 149 45
16 84
21 44
0 2
2 4
0 1
35 134
2 31
44 103
120 403
J Sex Med 2014;11:3112–3118
3115
Syphilis Origin Reexamined
lar areas of osteoporosis and osteosclerosis in the middle part of the tibia and discrete periostal thickening (hyperostosis) with slight obliteration of the medullary cavity (Figure 4). Discussion
Figure 1 Photo of the left and right femora.
The described case is one which calls for discussion or elaborate differential diagnosis. First, the bone was examined for possible signs of ante mortem trauma. No osteological markers of trauma were visible, including those on the radiographs. After we excluded trauma as a cause of changes observed on the femur and tibia, we used differential diagnosis to narrow down the possible cause of the following disease. A literature search for conditions that can cause observed changes revealed the following: Paget disease, unilateral femoral hypoplasia, and syphilis hereditaria tarda of femur. Paget’s disease of bone is a chronic affliction of the adult skeleton with areas of aggressive osteoclast-mediated bone resorption preceding imperfect osteoblast-mediated bone repair. It usually manifests in middle or advanced age and is slightly more common in men [11,12]. It usually involves one bone (monostotic) or a few bones (polyostotic), usually affecting the skull or pelvis, or a vertebra, femur, or tibia [12,13]. Osteolytic fronts progress approximately 1 cm yearly [14]. Cortical thickening (hyperostosis), disorganized coarse trabeculae (osteosclerosis), and bone expansion can be seen. In advanced stages of the disease, bones are widened and heterogeneously ossified [15]. Most clinical manifestations are skeletal [16], but the prevalence of various signs and symptoms and complications is uncertain [17]. The bowing of the femur is anterior and lateral and usually
Figure 2 Radiograph of the left and right femora.
trauma. Radiograph exam shows alternating, irregular areas of osteoporosis and osteosclerosis in the middle part of the femur and discrete periostal thickening (hyperostosis) with slight obliteration of the medullary cavity (Figure 2). The right tibia also has a specific curved appearance, especially in the anterior–posterior plane (Figure 3). Periostitis on the right tibia led to excessive new bone growth on the anterior surfaces and anterior bowing, or characteristic saber shin. Radiograph exam shows alternating, irregu-
Figure 3 Photo of the left and right tibia.
J Sex Med 2014;11:3112–3118
3116
Figure 4 Radiograph of the left and right tibia.
involves most of the femoral shaft. Paget disease has a characteristic appearance on radiographs with coarsened trabeculae and thickening of the cortex. Also, Looser’s zones may form which are inadequately healed stress fractures. Unilateral femoral hypoplasia is a disorder which clinically manifests as a short femur. It has been suggested that coxa vara and the short femur are variations of the same congenital anomaly [18]. If coxa vara is absent, it is considered to be simple hypoplasia of the femur. In this condition, broadening of the upper epiphyseal cartilage of the femur and an area of cortical sclerosis and bowing can be seen. In the early stages of femoral development, an excessive formation of new bone can be seen, but growth in breadth of the femur is not disturbed. Broadening of the upper epiphyseal plate indicates a failure of the metaphysis to replace cartilage by bone. Probably, a delay in ossification and bone bowing is a result of the primary defect of the cartilage [19]. Through literature search, we found an interesting case of syphilis hereditaria tarda of femur J Sex Med 2014;11:3112–3118
Anteric et al. on living patient. Diagnosis of syphilis was made using a positive Wassermann reaction. The illness affected the femur on which no inflammatory manifestations, areas of softening, or sinuses were found. The following changes were found: an increase in diameter of the upper half of the femur, obliteration of the medullary cavity, alternating areas of osteoporosis and osteosclerosis, and the line of an incomplete fracture at the point of greatest convexity of the femur [20]. By examination of the osteological findings on the femur and Davis’ description of the manifestation of syphilis hereditaria tarda in this clinical case, as well as by examination of radiographs of the bone and living patient, it is visible that the skeletal features share a resemblance. Both femurs are mostly curved on the upper diaphysis part, flattened, and have an increased bone diameter in the mentioned area. Considering that radiographs did not reveal cortex thickening or coarsened trabeculae characteristic for Paget disease, as well as no signs of broadening of the upper epiphyseal plate characteristic for unilateral femoral hypoplasia are visible, these two pathologies can be excluded as a potential reason for observed skeletal changes. Gummatous lesions have not been observed on this individual, but a nongummatous lesion on tibia (saber shin) has been seen. The examination of femur revealed the resemblance with previously published paper in which the similar changes were noticed on patients’ femur and the treponemal infection confirmed by the Wasserman test [20]. This only additionally confirmed the assumption that the findings on femur and tibia are caused by the treponemal infection, which was not in advanced state in this individual and did not affect other bones. Many theories support the existence of syphilis before 1492. Pales believes that syphilis (as well as osteomyelitis, spondylitis, and tumors) existed in ancient times, while Cockburn believes that treponematosis in the past differed from current treponematosis given that, historically, a smaller number of people lived in one area [21]. There is some written material that suggests that syphilis infected ancient Chinese dynasties and that Augustus Caesar was afflicted by hereditary syphilis, but all of this data are unconfirmed [22]. Existence of venereal syphilis in Italy 600 bc is discussed by Dr. Mattie Hennenberg and his wife [23]. Because of everything just stated, we believe that the Columbian theory of syphilis origin is not sustainable. Syphilis was most likely present in the
3117
Syphilis Origin Reexamined old world, but not to the extent that it was in post-Columbian time. It is interesting and indicative that no evidence of syphilis was found in graveyards from post-Columbian time in this research, and in the territory of present-day Croatia, only few cases of probably syphilis were published. All evidence supports the theory that syphilis is not a new illness, but its manifestations were randomly recorded or misclassified. Tanya et al. (cited in Von Hunnius et al.) state that skeletal evidence from recent excavations in Europe pushed back the clock concerning a preColumbian presence of syphilis in the Old World. They believe that more excavations with more skeletons examined will support the syphilis or treponemal precursors prior to 1492 [24]. As syphilis remains an international, still growing disease [3], paleopathological analysis can give a new insight into its origin. Acknowledgments
We would like to express our gratitude to Brunislav Marjanovic´, Sineva Kukoc´, Slavko Galiot, Helga Martinac, and Ljubomir Gudelj for providing osteological material and data about archeological findings. We would also like to thank Ayano Rachel Fox for valuable comments and suggestions on the manuscript language. This research was supported by the Ministry of Science, Education and Sports of the Republic of Croatia Grant No. 258 – 2160800 – 033. Corresponding Author: Ivana Anteric, MSc, University Department for Forensic Sciences, University of Split, Rudjera Boskovica 31, Split 21000, Croatia. Tel: 0038521417001; Fax: 0038521417001; E-mail: [email protected] Conflict of Interest: The author(s) report no conflicts of interest. Statement of Authorship
Category 1 (a) Conception and Design Ivana Anteric; Zeljana Basic; Katarina Vilovic; Kresimir Kolic; Simun Andjelinovic (b) Acquisition of Data Ivana Anteric; Zeljana Basic; Simun Andjelinovic (c) Analysis and Interpretation of Data Ivana Anteric; Zeljana Basic; Katarina Vilovic; Kresimir Kolic; Simun Andjelinovic
Category 2 (a) Drafting the Article Ivana Anteric; Zeljana Basic; Kresimir Kolic; Simun Andjelinovic
(b) Revising It for Intellectual Content Ivana Anteric; Zeljana Basic; Katarina Vilovic; Kresimir Kolic; Simun Andjelinovic
Category 3 (a) Final Approval of the Completed Article Ivana Anteric; Zeljana Basic; Katarina Vilovic; Kresimir Kolic; Simun Andjelinovic References 1 Cartwright FF, Biddiss M. Bolest i povijest. Zagreb: Naklada Ljevak; 2006. 2 Šlaus M, Novak M. A case of venereal syphilis in the modern age horizon of graves near the church of St. Lawrence in Crkvari. Pril Inst Arheol Zagrebu 2007;24:503–10. 3 Maatouk I, Moutran R. History of syphilis: Between poetry and medicine. J Sex Med 2014;11:307–10. doi: 10.1111/ jsm.12354. 4 Anteric´ I, Bašic´ Ž, And¯elinovic´ Š. Nadin—Results of the anthropological analysis of the Liburnian population. Asseria 2011;9:75–112. 5 And¯elinovic´ Š, Drnasin Ž, Anteric´ I, Škoric´ E, Becˇic´ K. Antropological analysis of osteological material from late medieval location Kamen Most—Kaldrma (in Croatian). In: Šeparovic´ T, ed. Zbornik radova, Znanstveni skup Stjepan Gunjacˇa. Split: Muzej hrvatskih arheoloških spomenika; 2010:451–62. 6 Bašic´ Ž, Anteric´ I, Škoric´ E, Vilovic´ K, And¯elinovic´ Š. Split from the 16th to 19th century through the prism of anthropological research (in Croatian). ShP 2011;38:329–53. 7 Aufderheide AC, Rodríguez-Martín C, Langsjoen O. The Cambridge encyclopedia of human paleopathology. Cambridge: Cambridge University Press; 1998. 8 Krogman WM, Iscan MY. The human skeleton in forensic medicine. Springfield: Charles C. Thomas; 1986. 9 Bass WM. Human osteology. Columbia: Missouri Archaeological Society; 1987. 10 Ubelaker DH. Human skeletal remains: Excavation, analysis, interpretation. Washington, DC: Taraxacum; 1999. 11 Paget J. On a form of chronic inflammation of bones (osteitis deformans). Med Chir Trans 1877;60:37–63. 12 Kanis J. Pathophysiology and treatment of Paget’s disease of bone. London: Martin Dunitz; 1998. 13 Altman RD. Paget’s disease of bone. Disorders of bone and mineral metabolism. In: Coe FL, Favus MJ, eds. Disorders of bone and mineral metabolism. Philadelphia: Lippincott Williams & Wilkins; 2002:1020–2002. 14 Doyle FH, Banks LM, Pennock JM. Radiologic observations on bone resorption in Paget’s disease. Arthritis Rheum 1980;23:1205–14. 15 Smith SE, Murphey MD, Motamedi K, Mulligan ME, Resnik CS, Gannon FH. Radiologic spectrum of Paget disease of bone and its complications with pathologic correlation. Radiographics 2001;22:1191–216. 16 Altman RD. Musculoskeletal manifestations of Paget’s disease of bone. Arthritis Rheum 1980;23:1121–7. 17 Selby PL, Davie MW, Ralston SH, Stone MD. Guidelines on the management of Paget’s disease of bone. Bone 2002;31:366–73. 18 Golding FC. Congenital coxa vara and the short femur. Proc R Soc Med 1938;32:641–6. 19 Ring PA. Congenital short femur simple femoral hypoplasia. J Bone Joint Surg 1959;41:75–8. 20 Davis GG. Transactions of the Philadelphia academy of surgery, stated meeting held October 7, 1912. Available at:
J Sex Med 2014;11:3112–3118
3118 http://www.academyofsurgery.org/1908December.pdf (accessed September 25, 2012). 21 Cockburn TA. The origin of the treponematoses. Bull World Health Organ 1961;24:221–8. Geneva. 22 Pearce J. A note on the origins of syphilis. J Neurol Neurosurg Psychiatry 1998;64:542–7.
J Sex Med 2014;11:3112–3118
Anteric et al. 23 Morton RS, Rashid S. The syphilis enigma: The riddle resolved? Sex Transm Infect 2001;77:322–4. doi: 10.1136/ sti.77.5.322. 24 Von Hunnius TE, Roberts CA, Boylston A, Saunders SR. Histological identification of syphilis in pre-Columbian England. Am J Phys Anthropol 2006;129:559–66.