Bioactivity and antibacterial activity of iodine-containing calcium titanate against implant-associated infection

[1] S. Spriano, S. Yamaguchi, F. Baino, S. Ferraris, A critical review of multifunctional

titanium surfaces: new frontiers for improving osseointegration and host response,

avoiding bacteria contamination, Acta Biomater. 79 (2018) 1–22, https://doi.org/

10.1016/j.actbio.2018.08.013.

[2] J.C.M. Souza, M.B. Sordi, M. Kanazawa, S. Ravindran, B. Henriques, F.S. Silva,

C. Aparicio, L.F. Cooper, Nano-scale modification of titanium implant surfaces to

enhance osseointegration, Acta Biomater. 94 (2019) 112–131, https://doi.org/

10.1016/j.actbio.2019.05.045.

[3] W.Q. Yan, T. Nakamura, M. Kobayashi, H.M. Kim, F. Miyaji, T. Kokubo, Bonding of

chemically treated titanium implants to bone, J. Biomed. Mater. Res. 37 (1997)

267–275, https://doi.org/10.1002/(SICI)1097-4636(199711)37:2<267::AIDJBM17>3.0.CO;2-B.

10

N. Ikeda et al.

Biomaterials Advances 138 (2022) 212952

[4] T. Kokubo, F. Miyaji, H.M. Kim, T. Nakamura, Spontaneous formation of bonelike

apatite layer on chemically treated titanium metals, J. Am. Ceram. Soc. 79 (1996)

1127–1129, https://doi.org/10.1111/j.1151-2916.1996.tb08561.x.

[5] K. Kawanabe, K. Ise, K. Goto, H. Akiyama, T. Nakamura, A. Kaneuji, T. Sugimori,

T. Matsumoto, A new cementless total hip arthroplasty with bioactive titanium

porous-coating by alkaline and heat treatment: average 4.8-year results, J Biomed

Mater Res B Appl Biomater 90 (2009) 476–481, https://doi.org/10.1002/jbm.

b.31309.

[6] C.R. Arciola, D. Campoccia, P. Speziale, L. Montanaro, J.W. Costerton, Biofilm

formation in staphylococcus implant infections. A review of molecular mechanisms

and implications for biofilm-resistant materials, Biomaterials 33 (2012)

5967–5982, https://doi.org/10.2106/JBJS.19.01397.

[7] B. Wang, Z. Wu, J. Lan, Y. Li, L. Xie, X. Huang, A. Zhang, H. Qiao, X. Chang, H. Lin,

H. Zhang, T. Li, Y. Huang, Surface modification of titanium implants by silk

fibroin/Ag co-functionalized strontium titanate nanotubes for inhibition of

bacterial-associated infection and enhancement of in vivo osseointegration, Surf.

Coat. Technol. 405 (2021), 126700, https://doi.org/10.1016/j.

surfcoat.2020.126700.

[8] H. Qiao, C. Zhang, X. Dang, H. Yang, Y. Wang, Y. Chen, L. Ma, S. Han, H. Lin,

X. Zhang, J. Lan, Y. Huang, Gallium loading into a polydopamine-functionalised

SrTiO3 nanotube with combined osteoinductive and antimicrobial activities,

Ceram. Int. 45 (2019) 22183–22195, https://doi.org/10.1016/j.

ceramint.2019.07.240.

[9] B. Wang, Z. Wu, S. Wang, S. Wang, Q. Niu, Y. Wu, F. Jia, A. Bian, L. Xie, H. Qiao,

X. Chang, H. Lin, H. Zhang, Y. Huang, Mg/Cu-doped TiO2 nanotube array: a novel

dual-function system with self-antibacterial activity and excellent cell

compatibility, Mater. Sci. Eng. C. 128 (2021), 112322, https://doi.org/10.1016/j.

msec.2021.112322.

[10] C.R. Arciola, D. Campoccia, P. Speziale, L. Montanaro, J.W. Costerton, Biofilm

formation in Staphylococcus implant infections. A review of molecular

mechanisms and implications for biofilm-resistant materials, Biomaterials 33

(2012) 5967–5982, https://doi.org/10.1016/j.biomaterials.2012.05.031.

[11] S.J. McConoughey, R. Howlin, J.F. Granger, M.M. Manring, J.H. Calhoun,

M. Shirtliff, S. Kathju, P. Stoodley, Biofilms in periprosthetic orthopedic infections,

Future Microbiol. 9 (2014) 987–1007, https://doi.org/10.2217/fmb.14.64.

[12] B.H. Kapadia, R.A. Berg, J.A. Daley, J. Fritz, A. Bhave, M.A. Mont, Periprosthetic

joint infection, Lancet 387 (2016) 386–394, https://doi.org/10.1016/S0140-6736

(14)61798-0.

[13] R.O. Darouiche, Treatment of infections associated with surgical implants, N. Engl.

J. Med. 350 (2004) 1422–1429, https://doi.org/10.1056/nejmra035415.

[14] W. Zimmerli, Clinical presentation and treatment of orthopaedic implantassociated infection, J. Intern. Med. 276 (2014) 111–119, https://doi.org/

10.1111/joim.12233.

[15] J.R. Lex, R. Koucheki, N.A. Stavropoulos, J. Di Michele, J.S. Toor, K. Tsoi, P.

C. Ferguson, R.E. Turcotte, P.J. Papagelopoulos, Megaprosthesis anti-bacterial

coatings: a comprehensive translational review, Acta Biomater. 140 (2022),

https://doi.org/10.1016/j.actbio.2021.11.045.

[16] B. Wang, A. Bian, F. Jia, J. Lan, H. Yang, K. Yan, L. Xie, H. Qiao, X. Chang, H. Lin,

H. Zhang, Y. Huang, “Dual-functional” strontium titanate nanotubes designed

based on fusion peptides simultaneously enhancing anti-infection and

osseointegration, Mater. Sci. Eng. C. (2022), 112650, https://doi.org/10.1016/J.

MSEC.2022.112650.

[17] T. Kizuki, H. Takadama, T. Matsushita, T. Nakamura, T. Kokubo, Effect of Ca

contamination on apatite formation in a Ti metal subjected to NaOH and heat

treatments, J. Mater. Sci. Mater. Med. 24 (2013) 2836–2842, https://doi.org/

10.1007/s10856-012-4837-6.

[18] Y. Okuzu, S. Fujibayashi, S. Yamaguchi, K. Yamamoto, T. Shimizu, T. Sono,

K. Goto, B. Otsuki, T. Matsushita, T. Kokubo, S. Matsuda, Strontium and

magnesium ions released from bioactive titanium metal promote early bone

bonding in a rabbit implant model, Acta Biomater. 63 (2017) 670–680, https://doi.

org/10.1016/j.actbio.2017.09.019.

[19] T. Kizuki, H. Takadama, T. Matsushita, T. Nakamura, T. Kokubo, Preparation of

bioactive ti metal surface enriched with calcium ions by chemical treatment, Acta

Biomater. 6 (2010) 2836–2842, https://doi.org/10.1016/j.actbio.2010.01.007.

[20] A. Fukuda, M. Takemoto, T. Saito, S. Fujibayashi, M. Neo, S. Yamaguchi, T. Kizuki,

T. Matsushita, M. Niinomi, T. Kokubo, T. Nakamura, Bone bonding bioactivity of ti

metal and ti-zr-nb-ta alloys with ca ions incorporated on their surfaces by simple

chemical and heat treatments, Acta Biomater. 7 (2011) 1379–1386, https://doi.

org/10.1016/j.actbio.2010.09.026.

[21] S. Yamaguchi, P.T. Minh Le, M. Ito, S.A. Shintani, H. Takadama, Tri-functional

calcium-deficient calcium titanate coating on titanium metal by chemical and heat

treatment, Coatings 9 (2019) 561, https://doi.org/10.3390/coatings9090561.

[22] Y. Okuzu, S. Fujibayashi, S. Yamaguchi, K. Masamoto, B. Otsuki, K. Goto, T. Kawai,

T. Shimizu, K. Morizane, T. Kawata, Y. Shimizu, M. Hayashi, S. Matsuda, In vitro

study of antibacterial and osteogenic activity of titanium metal releasing strontium

and silver ions, J. Biomater. Appl. 35 (2021) 670–680, https://doi.org/10.1177/

0885328220959584.

[23] K. Masamoto, S. Fujibayashi, S. Yamaguchi, B. Otsuki, Y. Okuzu, T. Kawata,

K. Goto, T. Shimizu, Y. Shimizu, T. Kawai, M. Hayashi, K. Morizane, M. Imamura,

N. Ikeda, Y. Takaoka, S. Matsuda, Bioactivity and antibacterial activity of

strontium and silver ion releasing titanium, J Biomed Mater Res B Appl Biomater

109 (2021) 238–245, https://doi.org/10.1002/jbm.b.34695.

[24] S. Yamaguchi, P.T. Le, S.A. Shintani, H. Takadama, M. Ito, S. Ferraris, S. Spriano,

Iodine-loaded calcium titanate for bone repair with sustainable antibacterial

activity prepared by solution and heat treatment, Nanomaterials 11 (2021) 2199,

https://doi.org/10.3390/nano11092199.

[25] G. Mcdonnell, A.D. Russell, Antiseptics and disinfectants: activity, action, and

resistance, Clin. Microbiol. Rev. 12 (1999) 147–179, https://doi.org/10.1128/

cmr.12.1.147.

[26] E.T. Houang, J.A. Gilmore, C. Reid, E.J. Shaw, Absence of bacterial resistance to

povidone iodine, J. Clin. Pathol. 29 (1976) 752–755.

[27] R. Cooper, A review of the evidence for the use of topical antimicrobial agents in

wound care, World Wide Wounds 1 (2004) 1–15.

[28] G. Selvaggi, S. Monstrey, K. Van Landuyt, M. Hamdi, P. Blondeel, The role of iodine

in antisepsis and wound management: a reappraisal, Acta Chir. Belg. 103 (2003)

241–247, https://doi.org/10.1080/00015458.2003.11679417.

[29] P.L. Bigliardi, S.A.L. Alsagoff, H.Y. El-Kafrawi, J.K. Pyon, C.T.C. Wa, M.A. Villa,

Povidone iodine in wound healing: a review of current concepts and practices, Int.

J. Surg. 44 (2017) 260–268, https://doi.org/10.1016/j.ijsu.2017.06.073.

[30] H. Vermeulen, S.J. Westerbos, D.T. Ubbink, Benefit and harm of iodine in wound

care: a systematic review, J. Hosp. Infect. 76 (2010) 191–199, https://doi.org/

10.1016/j.jhin.2010.04.026.

[31] W.H. Song, S.R. Hyun, S.H. Hong, Antibacterial properties of ag (or Pt)-containing

calcium phosphate coatings formed by micro-arc oxidation, J. Biomed. Mater. Res.

A 88 (2009) 246–254, https://doi.org/10.1002/jbm.a.31877.

[32] T. Nakamura, T. Yamamuro, S. Higashi, T. Kokubo, S. Itoo, A new glass-ceramic for

bone replacement: evaluation of its bonding to bone tissue, J. Biomed. Mater. Res.

19 (1985) 472–484, https://doi.org/10.1002/jbm.820190608.

[33] S. Fujibayashi, T. Nakamura, S. Nishiguchi, J. Tamura, M. Uchida, H.M. Kim,

T. Kokubo, Bioactive titanium: effect of sodium removal on the bone-bonding

ability of bioactive titanium prepared by alkali and heat treatment, J. Biomed.

Mater. Res. 56 (2001) 562–570, https://doi.org/10.1002/1097-4636(20010915)

56:4<562::AID-JBM1128>3.0.CO;2-M.

[34] Y. Shimizu, S. Fujibayashi, S. Yamaguchi, S. Mori, H. Kitagaki, T. Shimizu,

Y. Okuzu, K. Masamoto, K. Goto, B. Otsuki, T. Kawai, K. Morizane, T. Kawata,

S. Matsuda, Bioactive effects of strontium loading on micro/nano surface Ti6Al4V

components fabricated by selective laser melting, Mater. Sci. Eng. C. 109 (2020),

110519, https://doi.org/10.1016/j.msec.2019.110519.

[35] K. Masamoto, S. Fujibayashi, T. Yabutsuka, T. Hiruta, B. Otsuki, Y. Okuzu, K. Goto,

T. Shimizu, Y. Shimizu, C. Ishizaki, K. Fukushima, T. Kawai, M. Hayashi,

K. Morizane, T. Kawata, M. Imamura, S. Matsuda, In vivo and in vitro bioactivity of

a “precursor of apatite” treatment on polyetheretherketone, Acta Biomater. 91

(2019) 48–59, https://doi.org/10.1016/j.actbio.2019.04.041.

[36] G. Chu, C. Zhang, Y. Liu, Z. Cao, L. Wang, Y. Chen, W. Zhou, G. Gao, K. Wang,

D. Cui, A gold nanocluster constructed mixed-metal metal-organic network film for

combating implant-associated infections, ACS Nano 14 (2020) 9117–9123, https://

doi.org/10.1021/acsnano.0c06446.

[37] J. Peng, P. Liu, W. Peng, J. Sun, X. Dong, Z. Ma, D. Gan, P. Liu, J. Shen, Poly

(hexamethylene biguanide) (PHMB) as high-efficiency antibacterial coating for

titanium substrates, J. Hazard. Mater. 411 (2021), 125110, https://doi.org/

10.1016/j.jhazmat.2021.125110.

[38] Y. Zhuang, L. Ren, S. Zhang, X. Wei, K. Yang, K. Dai, Antibacterial effect of a

copper-containing titanium alloy against implant-associated infection induced by

methicillin-resistant Staphylococcus aureus, Acta Biomater. 119 (2021) 472–484,

https://doi.org/10.1016/j.actbio.2020.10.026.

[39] N. Dinjaski, M. Fern´

andez-Guti´

errez, S. Selvam, F.J. Parra-Ruiz, S.M. Lehman,

J. San Rom´

an, E. García, J.L. García, A.J. García, M.A. Prieto, PHACOS, a

functionalized bacterial polyester with bactericidal activity against methicillinresistant Staphylococcus aureus, Biomaterials 35 (2014) 14–24, https://doi.org/

10.1016/j.biomaterials.2013.09.059.

[40] S.Y. Yeh, C.H. Sung, T.L. Lin, T.L. Cheng, C.C. Chou, The effects of crossbreeding,

age, and sex on erythrocyte indices and biochemical variables in crossbred pet

rabbits (Oryctolagus cuniculus), Vet. Clin. Pathol. 48 (2019) 469–480, https://doi.

org/10.1111/vcp.12775.

[41] I.M. Washington, G. Van Hoosier, The laboratory rabbit, Guinea pig, hamster, and

other rodents, Am. Coll. Lab. Anim. Med. (2012) 57–116, https://doi.org/

10.1016/B978-0-12-380920-9.00003-1.

[42] S. Yamaguchi, H. Takadama, T. Matsushita, T. Nakamura, T. Kokubo, Apatiteforming ability of ti-15Zr-4Nb-4Ta alloy induced by calcium solution treatment,

J. Mater. Sci. Mater. Med. 21 (2010) 439–444, https://doi.org/10.1007/s10856009-3904-0.

[43] P.J. Marie, The calcium-sensing receptor in bone cells: a potential therapeutic

target in osteoporosis, Bone 46 (2010) 571–576, https://doi.org/10.1016/j.

bone.2009.07.082.

[44] M.M. Dvorak, A. Siddiqua, D.T. Ward, D.H. Carter, S.L. Dallas, E.F. Nemeth,

D. Riccardi, Physiological changes in extracellular calcium concentration directly

control osteoblast function in the absence of calciotropic hormones, Proc. Natl.

Acad. Sci. U. S. A. 101 (2004) 5140–5145, https://doi.org/10.1073/

pnas.0306141101.

[45] J.M. Lachapelle, O. Castel, A.F. Casado, B. Leroy, G. Micali, D. Tennstedt,

J. Lambert, Antiseptics in the era of bacterial resistance: a focus on povidone

iodine, Clin. Pract. 10 (2013) 285–291, https://doi.org/10.2217/cpr.13.50.

[46] J. Davies, Remarks on the use of iodine, locally applied in various surgical diseases

and external injuries, Lancet 32 (1839) 658–660, https://doi.org/10.1016/S01406736(02)80236-7.

[47] H. Banwell, What is the evidence for tissue regeneration impairment when using a

formulation of PVP-I antiseptic on open wounds? Dermatology 212 (2006) 66–76,

https://doi.org/10.1159/000089202.

[48] J.X. Liu, J.A. Werner, J.A. Buza, T. Kirsch, J.D. Zuckerman, M.S. Virk, Povidoneiodine solutions inhibit cell migration and survival of osteoblasts, fibroblasts, and

myoblasts, Spine 42 (2017) 1757–1762, https://doi.org/10.1097/

BRS.0000000000002224.

11

N. Ikeda et al.

Biomaterials Advances 138 (2022) 212952

[49] S.J. Van Meurs, D. Gawlitta, K.A. Heemstra, R.W. Poolman, H.C. Vogely, M.

C. Kruyt, Selection of an optimal antiseptic solution for intraoperative irrigation:

an in vitro study, J. Bone Jt. Surg. - Ser. A 96 (2014) 1757–1762, https://doi.org/

10.2106/JBJS.M.00313.

[50] J.L. Zamora, Chemical and microbiologic characteristics and toxicity of povidoneiodine solutions, Am. J. Surg. 151 (1986) 400–406, https://doi.org/10.1016/00029610(86)90477-0.

[51] A. Grzybowski, H. Nakashizuka, H. Shimada, Prevention and treatment of

postoperative endophthalmitis using povidone-iodine, Curr. Pharm. Des. 23 (2016)

574–585, https://doi.org/10.2174/1381612822666161205105404.

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