The authors report two cases of destructive cranial lesions associated with Mycobacterium tuberculosis–HIV coinfection in a male and female cadaver. Both cadavers were of African origin, from the Western Cape, South Africa. The authors present grossly abnormal tuberculosis–associated lesions of the anterior and middle cranial fossae, involving the ethmoid and sphenoid bones. Both individuals presented with tubercular intrasellar masses and obliteration of the paranasal sinuses. Current literature on cases such as these are extremely rare and others typically focus on lesions of the calvarium. Here we report on the gross anatomical findings as well as the relevant anatomical aspects of the probable aetiology. Both cases presented here hold interest for medical professionals in Africa and other geographic regions. It further illustrates the importance of understanding the venous drainage of the paranasal sinuses when considering the manifestation and treatment of extrapulmonary TB

Correia, Jc

Taylor, Adam Michael

Wessels, Quenton

Lancaster E-Prints

  1  Anatomical aspects of Mycobacterium tuberculosis–1 associated destructive cranial lesions 2  3 Quenton Wessels, PhD, FHEA1, Adam Michael Taylor, PhD, SFHEA2, Janine Carla 4 Correia, MMedSci3 5 1. Department of Anatomy, School of Medicine, University of Namibia, Windhoek, Namibia. 6 2. Lancaster Medical School, Faculty of Health and Medicine, Lancaster University, Lancaster, United 7 Kingdom. 8 3. Department of Biomedical Sciences, Division of Clinical Anatomy, Stellenbosch University, 9 Stellenbosch, South Africa. 10  11 Correspondence to:  12 Dr Quenton Wessels  13 School of Medicine  14 Faculty of Health and Medicine 15 University of Namibia 16 Windhoek 17 Namibia 18  19 Case Report 20  21 Anatomical aspects of Mycobacterium tuberculosis–associated destructive 22 cranial lesions 23  24 Abstract 25 The authors report two cases of destructive cranial lesions associated with Mycobacterium 26 tuberculosis–HIV coinfection in a male and female cadaver. Both cadavers were of African origin, 27 from the Western Cape, South Africa. The authors present grossly abnormal tuberculosis–associated 28 lesions of the anterior and middle cranial fossae, involving the ethmoid and sphenoid bones. Both 29 individuals presented with tubercular intrasellar masses and obliteration of the paranasal sinuses. 30 Current literature on cases such as these are extremely rare and others typically focus on lesions of 31 the calvarium. Here we report on the gross anatomical findings as well as the relevant anatomical 32   2  aspects of the probable aetiology. Both cases presented here hold interest for medical professionals 33 in Africa and other geographic regions. It further illustrates the importance of understanding the 34 venous drainage of the paranasal sinuses when considering the manifestation and treatment of 35 extrapulmonary TB.  36  37 Key words: Mycobacterium tuberculosis, HIV, coinfection, cranial lesions, paranasal sinuses 38  39 Introduction 40 Tuberculosis (TB) and human immunodeficiency virus (HIV) are the two most significant infectious 41 diseases with high mortality rates in developing countries [1]. In 2013, Mycobacterium tuberculosis 42 infections in HIV positive individuals affected at least a third of individuals in sub-Saharan Africa 43 alone. South Africa falls within the high-burden list of countries for TB, TB-HIV, and Multi-drug-44 resistant tuberculosis (MDR-TB) [2,3]. The exact causes of death in some cases of TB-HIV coinfection 45 associated mortality are typically unclear and this emphasises the importance of post-mortem 46 investigations. Such investigations have the potential to elucidate the pathogenesis and further aid the 47 improvement of public-health strategies, improve death certification and assist in clinical education [2]. 48 The skeletal changes associated with TB in modern South African individuals typically involve the 49 vertebral column and ribs. HIV coinfection became more prominent after 1985 [4]. Steyn et al. further 50 continues to state that antibiotic treatment and an increase in patient survival allows more time for the 51 development of lesions [4]. TB-associated lesions of the cranial base are an exception to the rule and 52 more so when considering tubercular intrasellar masses [5]. The two cases presented here, as well as 53 their anatomical considerations, are extremely rare. Both hold value when considering the 54 manifestation and treatment of extrapulmonary TB.  55       56  57  58 CASE REPORTS 59 Two gross abnormalities were discovered during routine dissections of crania of formalin-embalmed 60 adult cadavers. Both individuals, according to their death certificates, purportedly died of 61 Mycobacterium tuberculosis–HIV coinfection. Prior to maceration, the dura mater within each of the 62 crania were intact and intrasellar masses were found in both, along with extreme ruin of the ethmoid 63 and spheroid bones (Fig. 1A). The skulls were subsequently macerated and prepared for osteological 64 examination. The skull base of the 31-year-old female subject, of African descent, presented with 65 profound TB lesions. In the anterior cranial fossa (Fig. 1A), the ethmoid bone was completely 66 destroyed as well as the jugum of the sphenoid bone. The anterior clinoid processes remained intact. 67 Further abnormalities were seen and included; absence of both orbital plates of the frontal bone and 68 the perpendicular plate of the ethmoid bone. These gross pathological changes resulted in the 69 formation of one continuous cavity with the destruction of the medial portions of the orbital surfaces of 70 the frontal, lacrimal and maxillary bones (Fig. 1A and B). The maxillary sinuses were completely 71 exposed on their medial aspects. The most startling find was the complete destruction of the sella 72   3  turcica in the middle cranial fossa and extended as far as the clivus, just posterior of the sphenoid 73 sinus (Fig. 1A and B). The optic and pterygoid canals were intact, however both orbital roofs 74 presented with cribra orbitalia. Similarly, lesions of the ethmoid and sphenoid bones were observed in 75 the cranial base of the 27-year-old male cranium (also of African descent) (Fig. 1C and D). Some 76 lesions appeared to be more advanced than others with those seen in the paranasal sinuses 77 appearing some of the most significant. The medial and lateral walls of the maxillary sinuses were 78 obliterated. The orbital surfaces of the maxillary bones were nearly completely destroyed as well as 79 the middle and inferior nasal conchae (Fig. 2). In both cases, the complete absence of the ethmoid 80 bones was accompanied by a loss of the olfactory fibres and ethmoidal arteries. Furthermore, the 81 structures entering the sphenopalatine foramen, i.e. sphenopalatine artery and vein, posterior 82 superior lateral nasal nerve and nasopalatine nerves, were absent. A tuberculoma, containing 83 calcifications and caseous necrosis, were present in the sella turcica of both crania.   84  85 DISCUSSION 86 Mycobacterial bone infections have increased over the past few decades and are related to the global 87 HIV/AIDS epidemics [6,7]. HIV-related TB is most frequently seen in sub-Saharan Africa and the 88 region is known to contribute towards 79% of such cases worldwide. TB remains the most common 89 HIV-related cause of death and matters are made worse due to the emergence of drug-resistant TB 90 during the 1980s [6]. HIV/AIDS rapidly advances the clinical manifestation of TB and is known to drive 91 dormant cases into full-blown TB in immunocompromised individuals [7].  92  93 Mycobacterial infections of bones and joints are well documented and cases affecting the ribs and the 94 spine (Pott's disease and tuberculous vertebral osteomyelitis) have been described extensively. The 95 same holds true for elements of the appendicular skeleton and lytic lesions of the calvarium [4,8]. 96 However, tuberculous involvement of paranasal sinuses and infections of the central nervous system 97 (tuberculoma, tuberculous meningitis, and spinal tuberculous arachnoiditis) are extremely rare [5,9]. 98 More recently, a case of tubercular septic cavernous sinus thrombosis (SCST) was reported and 99 believed to have spread from the paranasal sinuses or dental infections to the veins linked to the 100 cavernous sinus. The microbiology of SCST is well documented [10]. The two cases presented here 101 appear to have followed a similar aetiology. We believe both patients presented with tuberculosis of 102 the ethmoid and sphenoid sinuses which subsequently spread to the cavernous sinus and lead to 103 tubercular intrasellar masses. The aetiology can be explained by considering the venous drainage of 104 the paranasal sinuses as outlined below. 105  106 The venous drainage of the maxillary sinuses is either through a single trunk, a continuation of the 107 spheno-palatine vein, or through a series of three venous plexuses. The latter includes the alveolar 108 plexus and anterior and posterior pterygoid plexuses. Of interest is that the posterior pterygoid plexus 109 that is connected to the alveolar plexus and drains into the maxillary and facial veins [11]. The facial 110 vein in turn drains partly into angular and internal jugular veins. It is through the angular vein that 111 infection can spread to the cavernous sinus. The venous drainage of the ethmoidal air cells can reach 112   4  the cavernous sinus via the superior ophthalmic vein, which drains into the angular vein, or the 113 pterygoid plexus. The connection of the pterygoid venous plexus with the facial vein is the most likely 114 route of entry to the cavernous sinus. The venae comitantes of the ethmoidal arteries, the ethmoidal 115 veins (both anterior and posterior), drain into superior ophthalmic vein. These routes relate to the 116 venous drainage of the sphenoid sinus, which drains into the posterior ethmoidal vein to the superior 117 ophthalmic vein. In summary, any infection in the paranasal sinuses can reach the cavernous sinus in 118 most instances via the superior ophthalmic vein [11,12].  119  120 Both cases presented here illustrate the importance of understanding the venous drainage of the 121 nasal cavity and paranasal sinuses when considering tuberculous involvement of the paranasal 122 sinuses and infections of the central nervous system. The venous communication between these 123 structures, the facial vein and the cavernous sinus should be considered when assessing patients’ 124 extrapulmonary TB. Lastly, our findings also reiterate the importance of post-mortem investigations in 125 order to elucidate the cause pathogenesis of TB-HIV coinfections. 126  127 ETHICAL APPROVAL 128 The cadaveric material was handled and processed in accordance with the Anatomical Donations 129 and Post-mortem Ordinance, No. 12 of 1977.  No further ethical approval was applicable. 130  131 REFERENCES 132 1. Mathers CD, Boerma T, Ma Fat D. Global and regional causes of death. Br Med Bull 2009;92:7-32. 133 2. Burton JL, Underwood J. Clinical, educational, and epidemiological value of autopsy. Lancet 134 2007;369:1471-80. 135 3. World Health Organization. Global tuberculosis control. WHO Report. Geneva, Switzerland: World 136 Health Organization, viewed 11 November 2018, 137 http://www.who.int/tb/publications/global_report/en/index.html 138 4. Steyn M, Scholtz Y, Botha D, Pretorius S. The changing face of tuberculosis: Trends in tuberculosis 139 associated skeletal changes. Tuberculosis 2013;93:467-474. 140 5. Majumdar K, Barnard M, Ramachandra S, Berovic M, Powell M. Tuberculosis in the pituitary fossa: 141 a common pathology in an uncommon site. Endocrinol Diabetes Metab Case Rep 2014;2014:140091 142 6. Harries AD. The association between HIV and tuberculosis in the developing world. In: Davies 143 PDO, editor. Clinical tuberculosis. London: Chapman & Hall Medical; 1998. p. 315-345. 144 7. Selwyn PA, Hartel D, Lewis VA. A prospective study of the risk of tuberculosis among intravenous 145 drug users with human immunodeficiency virus infection. New Eng J Med 1989;320:545-550. 146 8. Pigrau-Serrallach C, Rodriguez-Pardo D. Bone and joint tuberculosis. Eur Spine J 2013;22(Suppl. 147 4):556–566. 148 9. Rai DK, Kumar S, Thakur S. A rare case of tubercular pansinusitis with orbital and intracranial 149 extension. Lung India 2016;33(3):349-351. 150 10. Xia P, Jiao Y. Septic cavernous sinus thrombosis caused by tuberculosis infection. BMJ Case 151 Rep 2014;2014:206209.  152   5  11. Dargaud J, Lamotte C, Dainotti JP, Morin A. Venous drainage and innervation of the maxillary 153 sinus. Morphologie 2001;85(270):11-13. 154 12. Zhang J, Stringer MD. Ophthalmic and facial veins are not valveless. Clin Exp Ophthalmol 155 2010;38(5):502-510. 156  157   6  Fig. 1. A: The presentation of the 31-year-old female subject after removal of the brain with the dura 158 still intact. The damage was noted prior to maceration with extreme damage to the ethmoid and 159 sphenoid bones. B: Norma frontalis of the same cranium (after maceration) demonstrating the extent 160 of the tuberculosis-associated bone destruction of the nasal cavity. The asterisks denote the 161 infraorbital foramina and thinning of the anterior wall of the maxillary sinus was observed (dashed 162 circle). C: The 27-year-old male skull (macerated) with damage to the anterior and middle cranial 163 fossae, involving the ethmoid and sphenoid bones. The skull presented with obliteration of the sella 164 turcica and exposed the vomer inferiorly and the same findings were made in the female skulls after 165 maceration.  D: Norma frontalis of the same skull demonstrating similar bone lesions compared to the 166 female subject. Legend: C, clivus; CF, cerebellar fossa; FC, frontal crest; FM, foramen magnum; G, 167 glabella; GW, greater wing (of sphenoid); LW, lesser wing (of sphenoid); M, Maxilla; MP, mental 168 protuberance; NC, nasal cavity; NS, nasal spine; ST, sella turcica; TC, tentorium cerebelli; V, vomer; 169 Z, zygomatic bone.        170  171 Fig. 2. A diagrammatic representation of the extent of damage to the paranasal sinuses in both 172 crania. The red dashed circle and its content represents the elements of the viscerocranium that were 173 obliterated. Legend: EB, ethmoidal bulla; ES, ethmoidal sinus; HP, hard palate; Ic, inferior concha; 174 Mc, middle concha; MO, maxillary ostium; MS, maxillary sinus; NS, nasal septum; LO, left orbit; RO, 175 right orbit; Sc, superior concha.  176   177 

Anatomical aspects of Mycobacterium tuberculosis–associated destructive cranial lesions

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Anatomical aspects of Mycobacterium tuberculosis–associated destructive cranial lesions

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