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University of Missouri at Kansas City, School of Medicine, Basic Medical Science, 2411 Holmes Street, Kansas City, Missouri 64108
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ABSTRACT |
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Early Holocene bison mandibles (Bison antiquus) from Nebraska, ca. 8500 y ago, were examined with a variety of modern histotechnological procedures and staining techniques. A pathological, anatomical diagnosis of moderately severe, locally extensive, mandibular osteomyelitis with intralesional spherules morphologically consistent with fungal pathogens in the genus Coccidioides was made. The modern distribution of the organisms in North America is restricted to the arid Southwest. This implies either the fossil home range of the fungi was larger than it is today or fossil bison migrated between endemic and nonendemic foci during the early Holocene.
Key words: bison, Coccidioides, coccidioidomycosis, Holocene, Valley Fever
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). The specimens were collected in the flood plain along the Middle Loup River, near Milburn, Custer County, Nebraska. The region was a peat bog at the end Pleistocene-early Holocene.
After gross examination specimens were taken for histological examination from affected areas of each bison hemimandible. Individual lesions were sectioned on a rotary saw with a water-cooled, diamond blade and an advancing-screw drive. Multiple transverse sections approximately 1–3 mm thick were cut from each lesion. Tissues were processed in a variety of ways, including ground thin sections, paraffin-embedded sections and methyl methacrylate-embedded sections. Both stained and unstained thin sections of undecalcified bone were prepared with a modification of the Buehler thin-sectioning method (Sognaees 1947, Chinsamy and Raath 1992).
To enhance histological detail some sections were treated with the following techniques that allow staining of ground bone sections (Morrow 2002). This technique is essentially a modified Romanovsky-type method originally used for the staining of blood smears. Prepared thin sections were demineralized by placing sections in a solution of 15% HCl for approximately 1 min. The section was removed and flushed with running water. The slide was dipped sequentially in three different solutions 10 times for approximately 1 s each, beginning with 95% ethanol, then Leukostat I (an eosin-based stain) and finally Leukostat II (a methylene blue and azure A stain). Excess stain was blotted off the end of the slide between cytology stains. The slide was rinsed with running water and allowed to air dry. Although cover slips were not applied in the present study, they can be added to protect and preserve the specimen if desired.
One ground section was treated with Sedi-Stain, a gram-equivalent stain normally used to examine urine sediment. This is an additional staining application that should allow visualization and discrimination of bacteria present in ground bone sections. On the other hand a routine gram stain could be used. Bone first was demineralized by placing the section in a solution of 15% HCl for approximately 1 min. The section was removed and flushed with running water. One drop of Sedi-Stain was added to the wet section after demineralization, which subsequently was rinsed with running water and allowed to air dry.
Additional paraffin-embedded specimens were prepared from decalcified bone to produce histological sections that were stained with several procedures, including hematoxylin and eosin (H & E), gram, Grocott’s methenamine silver (GMS), and Perl’s iron (Luna 1968). Methyl methacrylate (MMA) embedded sections were processed with a modified Donath technique using the Exakt Tissue Processing Method (Enlow 1953, Sheehan and Hrapchak 1980, Rohrer and Schubert 1992, Donath 1995, Sanderson 1997), which is a proprietary, marketed system (Exakt-Apparatebau, Hamburg, Germany). All sections were examined with a compound microscope under varying magnifications.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). The mass on UNSM 38034 was approximately 5 x 4.5 x 3.5 cm and incorporated the fourth premolar (P4) and that of UNSM 38035 was approximately 12 x 6 x 3.5 cm and included the fourth premolar (P4) and first molar (M1). The surface of each mass contained numerous fistulae of approximately 1–3 mm diam. The lesions show signs of tooth root involvement, including elevation of the bone surrounding the margin of the tooth sockets and widening of the tooth socket, with a 1–2 mm gap formed between the wall of the tooth and the socket.
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) the bulk of each mass consists of patchy regions varying from cancellous, medullary trabeculae with enlarged lacunae extending into cortical bone to thickened, laminar, cortical regions with obvious periosteal elevation and subjacent deposition of new laminar bone. Occasional fistulous tracts extend throughout the lesion. Affected medullary bone is continuous with tooth alveoli. The gross appearance is consistent with moderate, focal, chronic, mandibular osteomyelitis. Histologically sections from the bony lesions of both fossil bison appear almost identical. Although cell detail is lacking, bone preservation is excellent in both hematoxylin-and-eosin-stained, paraffin-embedded sections and unstained, methyl methacrylate-embedded sections. The cortex consists of dense, laminar bone containing the primary osteons of Haversian systems overlaid by a patchwork of secondary osteons. Lacunae are numerous but devoid of osteocytes; evidence of osteoclastic and osteoblastic activity must be inferred. Medullary bone is open and cancellous and lacks secondary osteons. Multifocal areas of bony lysis and proliferation are scattered throughout the lesion and incorporate both cortex and medulla indiscriminately. Bone in lytic areas exhibits a moth-eaten appearance, with trabeculae that are thin and have scalloped, irregular margins. The presence of proliferative, woven bone with remodeling on both endosteal and periosteal surfaces varies from minimal to florid. Evidence of bony lysis occasionally is superimposed on woven or remodeled bone. In places new woven bone rivals cortical bone in density and thickness, although it is nonlaminar and, in general, orientation of collagen is initially perpendicular to the periosteum. This change in orientation frequently allows easy identification of original periosteal location. Occasional vascular channels or fistulae traverse the section. Infrequent clumps of red-brown to black, amorphous, seemingly friable material occlude vessels. This material stained variably with a Perl’s iron stain and might represent cellular debris or hemosiderin from red blood cells. Small amounts of amorphous, occasionally mineralized debris line occasional medullary spaces.
Scattered throughout affected areas and occasionally extending into adjacent bone are locally abundant, opaque, black spheres (FIG. 3). Two distinct size classes of spheres are present, the first approximately 1–5 µm diam and the second about 20–120 µm diam. In some sections spheres of the smaller class are visible within spheres of the larger class (FIG. 4). These are morphologically consistent with spherules and endospores of the fungus Coccidioides immitis and C. posadasii, which are morphologically identical. Endospores number approximately 20–150 per spherule. Large numbers of spheres are present in some sections, occasionally occluding Haversian and Volkmann’s canals. Fungal arthrospores and mycelia were not seen. Organisms are not randomly scattered throughout sections, as might be expected from airborne contamination, but are confined to affected areas or bone adjacent to a lesion. In many cases organisms are clustered within blood vessels, implying an antemortem, hematogenous mode of dissemination. The quality of preservation of organisms varies with processing technique, with the best preservation in unstained MMA sections. Although organisms morphologically consistent with the parasitic phase of C. immitis and C. posadasii were present in stained sections, they remained unstained, regardless of the staining technique or method of processing used. Organisms appear uniformly opaque black on all sections, both paraffin- and MMA-embedded, and both stained and unstained. This lack of differential staining characteristics presumably is an artifact of fossilization or represents some diagenetic alteration of the surface features of the organism that renders it unable to take up stain of any kind. The histological appearance is consistent with a moderately severe, locally extensive, mandibular osteomyelitis, with intralesional fungal organisms. The etiologic agent is consistent morphologically with the parasitic phase of the fungi C. immitis and C. posadasii. Both gross and histological lesions resemble those seen in modern cattle affected with coccidioidomycosis.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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, Luna 1968). If this uptake is inhibited or compromised, as might be expected due to mineralization of tissue during fossilization, successful staining might not occur. Mineralogical composition of the specimen itself is affected by such evanescent factors as temperature, pH and salinity during diagenesis (Dodd and Stanton 1990). Any chemical or physical modification of the cell membrane or fungal cell wall resulting in decreased cell permeability or change in overall charge will affect staining characteristics. Permineralization of cells with iron-laden water during fossilization presumably produces just such a stain barrier, possibly by binding with charged protein molecules within the cell wall and altering their isoelectric point, thus inhibiting staining. In the case of stains specific for fungi, competition for or inhibition of oxidation of polysaccharides within the fungal cell wall would prohibit staining (Sheehan and Hrapchak 1980). Consequently it is not surprising that fossil fungal organisms as described here should fail to stain with a variety of techniques. In contrast a modern fungus, whether contaminant or pathogen, would be expected to exhibit differential staining characteristics, suggesting that these organisms represent fossil pathogens and not modern contaminants. The distribution of organisms was limited to the immediate vicinity of osteolytic lesions, being most common within Haversian systems, further suggesting possible hematogenous dissemination. In addition all organisms observed in tissue sections were the parasitic phase; infectious arthrospores and free-living mycelia of the saprophytic phase were not observed. Because this is a noncontagious disease, spherules form only in the tissues of infected hosts and do not survive in the environment outside the host for any period of time. It is unlikely that the organisms seen in these specimens are other than etiologic agents of disease. In addition coccidioidomycosis is not endemic to Kansas, Nebraska or Pennsylvania, the three states in which tissue samples were collected, housed and studied. Therefore contamination of the specimens by modern Coccidioides was almost impossible.
Differential diagnoses.— –
Bone has a limited response repertoire to disease and injury, sometimes making accurate diagnosis difficult. In themselves the bony histopathological lesions described are not unique, or pathognomonic, for any one disease or condition. In the absence of an etiologic agent the diagnosis would be speculative at best. Differential diagnoses in this case include several bacterial and fungal diseases, as well as neoplasia and metabolic bone disease. No evidence of bacterial etiologic agents was seen, including either the characteristic "sulfur granules" of actinomycosis and attendant Splendore-Hoeppli reaction or tubercles of mycobacteria. Most fungal pathogens are smaller than the observed organisms, are yeast-like, often reproduce by budding and lack endospores (Connor et al 1997, Rippon 1988, Jubb et al 1992, Conant et al 1971). Many have restricted geographic ranges. Rhinosporidium, which may produce endospores, has large, spherical sporangia (100–400 µm diam) surrounded by minimal tissue reaction. Bony lesions are rare. Adiaspiromycosis, caused by Emmonsia crescens, also may produce endospores within spherules (10–40 µm or 250–400 µm diam) depending on the species ( Jellison 1970). Infection however is self-limiting and restricted to the lungs. Oral and bony lesions in adiaspiromycosis are unknown ( Jones and Hunt 1983). Bony changes were inconsistent with neoplasia, lacking a swirling or streaming pattern and not suggestive of pleomorphism, with relatively uniform size, shape and distribution of lacunae within osteons. Although bony changes were similar to those seen in hypertrophic pulmonary osteopathy (HPO), such changes are widespread regionally, being most common in distal extremities. Single, focal lesions are rare and when present mandibular involvement is generally diffuse ( Jubb et al 1992).
Coccidioidomycosis.— –
The disease (also known as Valley Fever or San Joaquin Valley Fever) is a highly infectious, noncontagious, mycotic disease first described in humans in 1892 (Posada). The first case infecting animals (cattle) was recorded in 1918 by Giltner. The causative agents of coccidioidomycosis are two morphologically identical species within a single genus, Coccidioides immitis and C. posadasii. Both are dimorphic ascomycetes within the family Onygenaceae, with a free-living, soil-inhabiting, saprophytic phase and a parasitic, tissue-dwelling phase (Fisher et al 2002). The saprophytic, soil-inhabiting phase forms fungal mycelium of branching, septate hyphae, which produce infectious arthrospores. The parasitic, or tissue, form is characterized by sporangia, or "spherules," containing endospores. Endospores are commonly 2–5 µm diam, and spherules commonly average 20 µm diam, although sizes up to 100 µm diam are not uncommon (Connor et al 1997, Rippon 1988, Maddy 1960). There is a larger size range in the current study, with slightly smaller endospores and moderately larger spherules. Infection occurs primarily via inhalation of arthrospores. Endospores mature directly into spherules containing endospores to complete the cycle. Unlike other pathogenic fungi, the parasitic, or tissue phase, of Coccidioides normally does not reproduce by budding. Endospores disseminate through pulmonary blood vessels to lodge in regional lymph nodes. Two forms of infection are recognized. The most common is an acute, transient, upper respiratory infection, either asymptomatic or with flu-like symptoms. Recovery from primary infection confers lifelong immunity. The second is a coccidioidal granuloma, a rare, chronic, progressive, usually fatal, disseminated form of the disease. Although uncommon, primary cutaneous infection similar to actinomycosis is also possible, usually secondary to trauma; most common sites include distal extremities and the head. Secondary cutaneous or bony lesions are similar to primary lesions in all respects. While symptomatology and clinical progression of the disease vary with portal of entry, the ultimate histopathological appearance of the disease is identical, consisting of a chronic-active to granulomatous, mixed inflammatory cell infiltrate regardless of whether the infective agent is a spherule or arthrospore (Wilson et al 1953). The gross and histologic appearance of lesions is also similar regardless of species affected (Jubb et al 1992, Jones and Hunt 1983, Maddy 1959b). In the case of fossil bone, lytic and granulomatous foci are absent of course and their presence must be inferred by the presence of reactive bone at the periphery of the lesion, with or without organisms. Without first identifying a primary lesion in the lungs it is difficult to determine whether a cutaneous or bony lesion is primary or secondary because soft tissues are required to confirm pathogenesis. Relatively rapid involution or resolution of primary cutaneous lesions is common and the persistence of a cutaneous lesion for longer than several months is considered strong evidence of primary pulmonary infection with secondary dissemination (Wilson et al 1953). In the present case it is impossible to determine whether the lesions were solitary or multiple. Multiple osteomyelitic lesions in a single individual also would support a diagnosis of disseminated coccidioidomycosis.
The modern geographic distribution of Coccidioides is confined to the Lower Sonoran Life Zone of the New World (FIG. 5) (Merriam 1898). In North America this constitutes portions of the American southwest, including parts of California, New Mexico, Arizona, Texas and northern Mexico. Disjunct endemic foci also occur in southern Mexico and Central and South America (Pappagianis 1988, Ajello 1971, Maddy 1958a, 1959b, 1960). C. immitis is restricted to the southern San Joaquin Valley of California. This distribution corresponds roughly with sage brush and chaparral vegetative zones as described by Barbour and Major (1988). C. posadasii, previously referred to as non-California C. immitis, is the more widespread of the two species. C. posadasii is sympatric with C. immitis in part of is range and encompasses all other endemic foci of Coccidioides outside the San Joaquin Valley. Rainfall within the Lower Sonoran Life Zone is approximately 10–50 cm per year and is confined to the winter months, and summers are hot and dry. Mean temperatures for July are 26–32 C and for January 4–12 C, with only occasional frosts. Soils typical of this region include red desert soil, reddish-brown soil and noncalcic brown soil with much lithosol. The light, sandy soil allows rapid drainage after rainfall and concentration of salts, resulting in an alkaline pH (Rippon 1988, Conant et al 1971, Maddy 1957, 1958a, Kellogg 1941). Edaphic factors appear to play an important role in the distribution of Coccidioides. This is a common characteristic of the distribution of many plant taxa in arid regions and appears to be due not to a requirement for a particular soil type but an absence of competition from species in other soil types (Barbour and Major 1988). Throughout its range the distribution of Coccidioides is patchy. The organism frequently is associated with animal burrows near creosote bushes and with areas of disturbed soil, especially construction and archeological sites or fossil beds (Kaplan 1973, Swatek 1970, Maddy 1958a, Egeberg and Ely 1955). Growth and sporulation of the fungus seems to occur when the soil is moist, after rains. Dissemination of arthrospores and coincidental infections occur during hot, dry months (Pappagianis 1988, Maddy 1960). Perhaps the burrows act as ameliorating microclimates, cooling and humidifying air during hot summer months and providing aeration to waterlogged soils during rainy periods. Many authors have postulated that the soil sterilizing effect of the hot summers followed by winter rains allows growth of the organism in an arena free of competition from other soil inhabitants (Rippon 1988, Maddy 1960, Conant et al 1971, Elconin et al 1957). On the other hand increased nitrogen content of the soil near animal burrows might provide necessary nutrients for enhanced growth of the organism (Egeberg and Ely 1955). Predisposing factors for infection include inhalation of windborne dust and digging in infected soils (Kaplan 1973). All mammals presumably are susceptible to infection. Among domestic animal species, dogs are most commonly affected, while cats, horses, sheep and cattle are less commonly affected (Jubb et al 1992, Jones and Hunt 1983, Maddy 1959b).
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). This xereothermic trend became even more pronounced 8000–4000 y ago, during the Holocene, influencing the modern day distribution of many taxa and likely including C. posadasii. The implications of this trend to biogeography in California have been complicated by the complex coastal geography of the region. The modern distribution of C. immitis might represent that of a paleoendemic species with islands of endemicity based primarily on rainfall and soil type (CLIMAP 1976, COHMAP 1988).
The presence of active sand dunes on the northern plains at approximately 35–45°N during the last glacial maximum (Williams et al 1998) is evidence of an arid environment. Sand dunes also were present in South America, at approximately 10°N in the region of modern Columbia and Venezuela and 20–40°S in the region of Argentina and Paraguay, which roughly corresponds to the modern day distribution of C. posadasii in South America. Subsequent climatic shifts might have caused localized extinction of northern populations, leading to the modern day distribution of the organism. Two separate cooling events in the early Holocene 9000–8000 y ago (Baldini et al 2002, Hu et al 1999) might have been responsible for increased mortality of pathogens, as well as infected hosts at that time. If the mosaic models of Guthrie (1970, 1984) and others are correct, C. posadasii might have enjoyed a more widespread, although disjunct, distribution in the Pleistocene, or even throughout the Tertiary, distributed as endemic islands across North America in noncontiguous, semiarid areas corresponding to the Lower Sonoran Life Zone. It also is possible that C. posadasii might have existed in habitats outside the Lower Sonoran Life Zone within the Pleistocene or early Holocene, including Nebraska. Although morphologically similar to modern C. immitis and C. posadasii the fossil specimens might represent an ecotype with different physiological adaptations or biotic requirements and therefore a different geographic distribution. This ecotype could represent a different, and now extinct, population of C. posadasii or perhaps even a different, yet closely related, species. The broader size range of endospores and spherules might indicate some degree of genetic distance between extant Coccidioides and fossil specimens, implying a different genetic lineage. Samples have been sent to Alan Cooper for a-DNA analysis to address this possibility.
A second hypothesis to explain observed pathogenesis involves migration of vectors. The Lower Sonoran Life Zone in the present day American Southwest represents an emerging biotic region that first developed approximately10 000 y ago (Guthrie 1984). Changing paleoclimate resulting in increased aridity in the Southwest might have given rise to new or expanded endemic foci of C. posadasii in the burgeoning Lower Sonoran Life Zone. Because these foci lie outside the collection area of the current bison specimens it necessitates migration of bison between endemic and nonendemic foci. Affected bison might have migrated from a more southerly endemic focus of the disease to a nonendemic region such as Nebraska and died there (FIG. 6). Migration of host vectors also might have resulted in colonization of disjunct, previously nonendemic sites by C. posadasii. Seasonal north-south migration of modern Bison bison herds before their decimation by Europeans has been well documented (Hornaday 1889, Moodie and Ray 1976) and could serve as a model for fossil bison migration. Analysis of tooth eruption and wear patterns from bone beds at Paleoindian kill sites in Texas and Nebraska suggest seasonal mortalities consistent with an annual north-south migration of fossil bison during the late Pleistocene-early Holocene (Todd et al 1990). Regional, annual, seasonal migration for B. antiquus has been demonstrated to have occurred in the late Pleistocene in Rancho La Brea (Jefferson and Goldin 1989). Evidence presented in the present paper supports the theory of an annual north-south or northeast-southwest migration of fossil bison in the Great Plains. DNA sequencing suggests that South American populations of C. posadasii appear to represent a genetically depauperate population derived from a single introduction from Texas (Fisher et al 2001). Fisher postulates migration of paleoindians from North America to South America 9000–140 000 y ago as vectors or primary dispersal agents responsible for the organism’s colonization of South America. The current research suggests a parallel between north-south migration of bison herds in North America and human migration from North to South America as a mechanism of dispersal for C. posadasii between suitably habitable, although geographically disjunct, arid environments.
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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1 Phone (816) 235-5717, Fax (816) 235-6517; E-mail: morroww{at}umkc.edu
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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