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The Impact of Tick-Borne Diseases on the Bone microorganisms Review The Impact of Tick-Borne Diseases on the Bone Imran Farooq 1 and Tara J. Moriarty 1,2,* 1 Faculty of Dentistry, University of Toronto, Toronto, ON M5G 1G6, Canada; [email protected] 2 Department of Laboratory Medicine and Pathobiology, Faculty of Medicine, University of Toronto, Toronto, ON M5G 1G6, Canada * Correspondence: [email protected]; Tel.: +1-416-978-6685 Abstract: Tick-borne infectious diseases can affect many tissues and organs including bone, one of the most multifunctional structures in the human body. There is a scarcity of data regarding the impact of tick-borne pathogens on bone. The aim of this review was to survey existing research literature on this topic. The search was performed using PubMed and Google Scholar search engines. From our search, we were able to find evidence of eight tick-borne diseases (Anaplasmosis, Ehrlichiosis, Babesiosis, Lyme disease, Bourbon virus disease, Colorado tick fever disease, Tick-borne encephalitis, and Crimean–Congo hemorrhagic fever) affecting the bone. Pathological bone effects most commonly associated with tick-borne infections were disruption of bone marrow function and bone loss. Most research to date on the effects of tick-borne pathogen infections on bone has been quite preliminary. Further investigation of this topic is warranted. Keywords: tick; infection; bone; virus; Anaplasma; Ehrlichia; Babesia; Borrelia 1. Introduction Citation: Farooq, I.; Moriarty, T.J. A wide range of bacterial, viral, and protozoan pathogens can be transmitted by The Impact of Tick-Borne Diseases on ticks, which act as vectors transporting pathogens to hosts, including humans [1,2]. These the Bone. Microorganisms 2021, 9, 663. pathogens are responsible for many known human diseases, including those described in https://doi.org/10.3390/ Table1 below. microorganisms9030663 Table 1. Human diseases caused by tick-borne pathogens. Academic Editor: Pat Nuttall Bacterial Viral Parasitic Received: 28 November 2020 Nairoviral diseases: Accepted: 18 March 2021 Crimean-Congo Hemorrhagic Fever Babesiosis (Babesia microti, Published: 23 March 2021 Anaplasmosis (Anaplasma (CCHFV)[4]; Nairobi B. divergens, B. duncani, B. phagocytophilum)[3] Sheep Disease (NSDV)[5]; venatorum)[7] Publisher’s Note: MDPI stays neutral Songling Virus Disease with regard to jurisdictional claims in (SGLV)[6] published maps and institutional affil- Phenuiviral diseases: iations. Heartland Virus Disease Ehrlichiosis (Ehrlichia chaffeensis, E. (HRTV)[9]; Severe Fever ewingii, E. muris)[8] with Thrombocytopenia Syndrome (SFTSV)[10] Lyme Disease (Borreliella afzelii, B. Orthomyxoviral diseases: Copyright: © 2021 by the authors. burgdorferi sensu stricto, B. garinii, Bourbon virus disease Licensee MDPI, Basel, Switzerland. B. mayonii)[11] (BRBV)[12] This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https:// creativecommons.org/licenses/by/ 4.0/). Microorganisms 2021, 9, 663. https://doi.org/10.3390/microorganisms9030663 https://www.mdpi.com/journal/microorganisms Microorganisms 2021, 9, 663 2 of 11 Microorganisms 2021, 9, x FOR PEER REVIEW 2 of 11 Table 1. Cont. RickettsiosesBacterial, including Flinders Island Viral Parasitic (R.Rickettsioses honei), Israeli, including (R. conorii Flinders subsp. israelen- sis)Island, Mediterranean (R. honei), Israeli (R. conorii (R. subsp. Flaviviral diseases [15]: conorii)conoriisubsp., Japanese ( israelensisR. japonica), ) and Rocky Alkhurma Hemorrhagic MountainMediterranean (R. rickettsii) (R. conoriisubsp. Spotted Fevers;Flaviviral Fever diseases (AHFV)[ 15[16]]: ; Ky- conorii), Japanese (R. japonica) and Alkhurma Hemorrhagic RockyIndian Mountain (R. conorii (R. subsp. rickettsii indica) Spotted), Queens-Feverasanur (AHFV Forest)[16]; Disease land (R. australis) and Siberian Tick Ty- (KFDV) [17]; Omsk Fevers; Indian (R. conorii subsp. Kyasanur Forest Disease phusindica ),(R. Queensland sibirica subsp. (R. australis sibirica)) and; Far East-(KFDVHemorrhagic)[17]; Omsk Fever ernSiberian (R. heilongjiangensis) Tick Typhus (R. sibirica and Lymphangi- subsp. Hemorrhagic(OHFV) [15] Fever; Powassan sibirica); Far Eastern (R. (OHFV)[15]; Powassan tis-Associated (R. sibirica subsp. mongoliti- Disease (POWV) [15,18]; heilongjiangensis) and Disease (POWV)[15,18]; monaeLymphangitis-Associated) Rickettsioses; African (R. sibirica Tick Bite Tick-borne(R. Tick-borne Encephalitis Encephalitis rickettsii)subsp. mongolitimonae and Astrakhan) Rickettsioses; (R. conorii subsp. (TBEV(TBEV)[19] ) [19] Africancaspia) TickFevers; Bite SE(R.NLAT rickettsii) (R.and raoultii) Astrakhan (R. conorii[13,14] subsp. caspia) Fevers; SENLAT (R. raoultii)[13,14] TickTick-borne-borne RelapsingRelapsing Fever Fever(Borrelia (Borrelia cro-ReoviralReoviral diseases diseases: : Col- cidurae,crocidurae B. duttoni,, B. duttoni B., hermsii,B. hermsii B., B. hispanica,Colorado orado Tick Tick Fever Fever Dis- B.hispanica miyamotoi,, B. miyamotoi B. parkeri,, B. B. parkeri persica,, B. B. tu-Diseaseease (CTFV (CTFV)); Eyach; Eyach Vi- persica, B.ricatae) turicatae [20])[20 ] Virusrus Disease Disease (EYAV (EYAV)[21] ) [21] Tularemia (Francisella tularensis)[22] Tularemia (Francisella tularensis) [22] OneOne ofof thethe mostmost essentialessential structuresstructures inin vertebratesvertebrates isis bone,bone, whichwhich supportssupports thethe body, protectsprotects vital organs and and stores stores minerals minerals [23]. [23 Bone]. Bone is a ismixture a mixture of inorganic of inorganic content content (min- (mineralserals primarily primarily in the in form the form of hydroxyapatite of hydroxyapatite crystals), crystals), organic organic components components such suchas colla- as collagen,gen, cells cellsand proteins, and proteins, and water and water [24,25]. [24 There,25]. Thereare two are major two majortypes of types bone: of (1) bone: cortical (1) cortical(compact) (compact) and (2) trabecular and (2) trabecular (spongy, (spongy,cancellous cancellous or porous). or In porous). trabecular In trabecular bone, the spaces bone, thebetween spaces minera betweenlized mineralized bone trabecula bone are trabecula filled with are filled bone withmarrow bone and marrow fat tissue and (Figure fat tissue 1). (FigureBone marrow1). Bone is marrow highly vascularized is highly vascularized and innervated and innervated and is responsible and is responsible for the production for the productionof red blood of cells, red blood granulocytes, cells, granulocytes, platelets, monocytes platelets, monocytesand lymphocytes and lymphocytes [26]. [26]. FigureFigure 1.1. HematoxylinHematoxylin andand eosineosin (H(H andand E)E) stainedstained decalcifieddecalcified sectionsection showingshowing bonybony trabeculae of spongyspongy bonebone withwith marrowmarrow spacesspaces andand fatfat tissue. tissue. Bone in most parts of the body is renewed by a dynamic process called bony remod- elling [27], which involves four basic steps: resorption, reversal, formation and resting Microorganisms 2021, 9, 663 3 of 11 Microorganisms 2021, 9, x FOR PEER REVIEW 3 of 11 Bone in most parts of the body is renewed by a dynamic process called bony remod- elling [27], which involves four basic steps: resorption, reversal, formation and resting (Figure 2). Bony remodelling is driven by counterbalancing activities of osteoclasts, which (Figure2). Bony remodelling is driven by counterbalancing activities of osteoclasts, which are responsible for bone resorption, and osteoblasts, which are responsible for bone build- are responsible for bone resorption, and osteoblasts, which are responsible for bone build- ing (apposition) [28]. ing (apposition) [28]. FigureFigure 2. 2. FlowFlow chart chart depicting depicting sequence sequence of of events events during during bony bony remodelling remodelling process process.. Adapted Adapted from fromRaggat Raggat and and Partridge Partridge [29]. [29]. BBoneone plays plays a a complex complex and importantimportant rolerole in in immune immune responses, responses, and and local local and and systemic sys- temicinfections infections can also can cause also cause bone pathologybone pathology [30–32 ].[30 Osteoblasts–32]. Osteoblasts and osteocytes and osteocytes can regulate can regulatenumbers numbers and differentiation and differentiation of B-cells of and B-cells T-cells and in T bone-cells marrow in bone [ 33marrow,34], and [33,34], osteoclasts and osteoclastscreate the bonecreate marrow the bone cavity marrow required cavity for required normal hematopoiesisfor normal hematopoiesis [35]. Infections [35]. and Infec- con- tionsditions and accompanied conditions accompanied by systemic immuneby systemic responses, immune such responses, as inflammatory such as inflammatory bowel disease, bowelcan cause disease, bone can loss cause because bone inflammatory loss because cytokinesinflammatory can stimulate cytokines osteoclastogenesis can stimulate osteo- and clastogenesisbone resorption and bone [36]. Microbesresorption also [36]. directly Microbes colonize also directly bone, ascolonize a result bone, of injury, as a result surgery, of injury,implanted surgery, devices implanted and hematogenous devices and disseminationhematogenous from dissemination more distant from infection more distant sites. In infectionsome cases, sites. colonization In some cases, is accompanied colonization by is infectious accompanied pathologies by infectious including pathologies bone marrow in- cludingdysfunction
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