Cationic Substitutions in Hydroxyapatite: Current Status of the Derived Biofunctional Effects and Their In Vitro Interrogation Methods
Abstract
:1. Introduction
2. Preparation Methods and Synthesis Routes of Hydroxyapatite Materials
2.1. Preparation of Bulk Hydroxyapatite (HA) from Natural Resources
2.2. Synthesis of Bulk Synthetic Substituted HA
2.3. Fabrication of Substituted HA Coatings
3. Cation-Substituted Hydroxyapatites
3.1. s-Block Cation-Substituted Hydroxyapatites
3.2. p-Block Cation-Substituted Hydroxyapatites
3.3. d-Block Cation-Substituted Hydroxyapatites
3.4. f-Block Cation-Substituted Hydroxyapatites
3.5. Cytotoxic Concentration of Cationic Species
4. Rigorous In Vitro Testing of Bioactive Materials
- ISO 10993-14:2001—Biological Evaluation of Medical Devices—Part 14: Identification and Quantification of Degradation Products from Ceramics.Medium for extreme tests: buffered citric acid solution, pH = 3.0 ± 0.2 at a temperature of 37 ± 1 °C, in normal atmosphere;Solution for simulated tests: buffered tris(hydroxymethyl)aminomethane (Tris)-HCl solution, pH = 7.4 ± 0.1 at a temperature of 37 ± 1 °C, in normal atmosphere.
- ISO 16428:2005—Implants for Surgery—Test Solutions and Environmental Conditions for Static and Dynamic Corrosion Tests on Implantable Materials and Medical Devices.Medium: aqueous solution of sodium chloride (0.9% NaCl mass fraction) or Ringer’s solution isotonic aqueous solution of NaCl, pH = 7.0 at a temperature of 37 ± 1 °C, in normal atmosphere.
- ISO 16429:2004—Implants for Surgery—Measurements of Open-Circuit Potential to Assess Corrosion Behaviour of Metallic Implantable Materials and Medical Devices over Extended Time Periods.Medium: aqueous solution of sodium chloride (0.9% NaCl mass fraction), pH = 7.0 at a temperature of 37 ± 1 °C, in normal atmosphere. For more stringent test conditions, more acidic test solutions are recommended.
- ISO 23317:2014—Implants for surgery—In vitro Evaluation for Apatite-Forming Ability of Implant Materials. (i.e., Bioactivity/Biomineralization Capacity Testing).Medium: Tris-buffered simulated body fluid (ionic concentration in mM: 142.0 Na+, 5.0 K+, 1.5 Mg2+, 2.5 Ca2+, 147.8 Cl−, 4.2 HCO3−, 1.0 HPO42−, and 0.5 SO42−), pH = 7.4 at a temperature of 36.5 ± 0.2 °C, in normal atmosphere.
- ISO 10993-5:2009—Biological Evaluation of Medical Devices—Part 5: Tests for in vitro Cytotoxicity.Medium: culture medium (e.g., Dulbecco’s Modified Eagle Medium) with or without serum such as to meet the growth requirements of the selected cell line, pH = 7.4 at a temperature of (37 ± 1) °C, in a humidified atmosphere of 5% CO2.
- ISO 22196:2011—Measurement of Antibacterial Activity on Plastics and Other Non-Porous Surfaces.Medium for suspension assays: nutrient broth (containing meat extract, peptone, NaCl), at a temperature of (35 ± 1) °C and a relative humidity of not less than 90% for 24 ± 1 h, in normal atmosphere.
4.1. Biomineralization Capability (Bioactivity Testing)
4.2. Degradation and Corrosion Tests
- Using pure inorganic fluids for testing (i.e., citric acid, (Tris)-HCl, 0.9% NaCl, Ringer’s solutions) is not a viable choice because, as presented before, the organic component of the intercellular fluid interacts with the implant surface and greatly modifies the interactions with the biomaterial. The use of a suitable testing environment is of foremost importance since these specific material features (degradation rate and corrosion resistance) are dependent on the material surface properties and its ability to adsorb organic moieties, partial dissolution and the consequent ionic exchanges.
- In the attempt to compress the time needed for a degradation test and peek into the future, the ISO 10993-14:2001 standard uses buffered citric acid solution (at a pH = 3.0 ± 0.2) to force degradation. However, since this solution is only inorganic and with a pH value never to be encountered at the implantation site, results can significantly vary from the actual events that will occur in vivo for the tested material over the long-term.
- Such standards are designed mainly for testing bulk materials, and are focused on the weight of the specimen, not taking into account one of the most important parameters: the contact area with the fluid. The focus is on the ratio between the mass of specimen and volume of fluid, but systems to be studied differ a lot with respect to the interaction area per gram of substance. Pellets, scaffolds (with macro- and micro-porosity), powders with different particle size, and thin (or thick) smooth (or rough) films induce huge differences in the ratios between the mass of substance and the area of interaction with the testing medium. An overview of this particular matter along with a several proposals can be found in [492].
4.3. Biocompatibility Assays
- Classic, MTT (3-(4,5-Dimethylthiazol-2-yl)-2,5-Diphenyltetrazolium Bromide), MTS (3-(4,5-dimethylthiazol-2-yl)-5-(3-carboxymethoxyphenyl)-2-(4-sulfophenyl)-2H-tetrazolium)), XTT (2,3-bis-(2-methoxy-4-nitro-5-sulphenyl)-(2H)-tetrazolium-5-carboxanilide) assays, that returns a value linked to general mitochondrial activity of the cells. Errors are given by different factors (e.g., differentiation of stem cells induces growth of mitochondria number per cell and increased activity). Advantages: simple and fast procedure, reliable results when working with homogenous terminally differentiated cells, cheap equipment and kits; Disadvantages: low reliability when working with heterogeneous cell cultures for differentiating experiments, indirect measure of proliferation;
- Quantifying double-stranded (ds) DNA by fluorescence (more ds-DNA, means more cells, ergo higher proliferation). Commercial kits are available. Advantages: direct measure of proliferation, very good and reliable results when working with heterogeneous cell cultures with many cell types (differentiation experiments), affordable equipment (98 well fluorescence reader), commercial kits are available; Disadvantage: complicated procedure;
- Cell counting when possible. Advantage: can be somewhat automated with a flow cytometer; Disadvantages: the classic counting technique uses microscopy, which is very laborious, time consuming, and impossible when dealing with a large number of situations (i.e., at least 10 microscopy fields per situation are required, with minimum 500 cells, numbered by three different examiners).
- Studying their morphology, when possible (as presented in ISO 10993-5:2009). This is a laborious method as it requires examination of a minimum 500 cells per situation acquired from a minimum 10 different randomly-chosen microscopy fields by three separate individuals. This renders the method almost impossible, when the experiment would involve a large number of materials;
- Measuring the LDH (lactate dehydrogenase) activity in the medium in which the cells were cultivated. LDH is an active intracellular enzyme found in all cells. Upon death, the cell releases this LDH into the medium and, therefore, this enzyme activity is proportional to the number of dead cells [501]. The method is easy to perform, fast, and returns reliable results on the same samples investigated for cell proliferation by mitochondrial activity tests;
- Measuring mitochondrial activity (MTT, MTS, XTT), as presented in the ISO 10993-5:2009 standard. It is a surrogate test for cytotoxicity: lower values with respect to control, due to lower general mitochondrial activity, are interpreted as results of cellular death, but this can also be an effect of slower proliferation values induced by the material. Thereby, it should not be used as stand-alone assay for cytotoxicity;
- Fluorescence apoptosis and cell viability kits (e.g., DAPI, annexinV, propidium iodide kit and Calcein AM/EthD-1 kit) are simple and widely used assays that provide good results, especially for flat substrates and examination with a confocal microscope. Calcein AM enters live cells and is converted in the cytoplasm in a green fluorescent compound, which does not exit from the cytoplasm. The dead cell nuclei have a red fluorescence due to EthD-1 that can penetrate only through the membrane of dead cells. As such, by fluorescence confocal microscopy the ratio of dead cells can be assessed. For 3D scaffolds it provides good results when the reading is done by a flow cytometer only, if the protocol recuperates and counts also the prior detached cells (which makes it a more difficult variant);
- Measuring the intracellular colorant uptake, as presented in the ISO 10993-5:2009 standard. The procedure is time consuming, but offers reliable results.
4.4. Osteoinduction Ability
4.5. Cell Differentiation Capacity
4.6. Pro-Angiogenic Properties
4.7. Antimicrobial Activity
- The tested material should be flat and compact with a surface of minimum 6.25 cm2, of which 4 cm2 should be reserved for bacterial interaction;
- Various types of nutrient broth have been observed to interact differently with the biomaterials, causing a variety of degradation rates, and therefore dissimilar antibacterial activities;
- Because of their nature and geometry, powders and 3D scaffolds with macro- and micro-porosity, cannot be tested according to this ISO standard protocol. Therefore, adaptive measures should be devised.
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- A nutrient media powder suspension is inoculated with a known number of colony-forming units (CFU) to a final concentration of around 105−106 CFU mL−1, under continuous agitation in an incubator at 37 °C for a desired period of time. The number of bacterial cells that remained viable (viable cell count, VCC) is to be investigated by serial dilutions from each situation and seeding on simple agar plates (in an analogue manner to the ISO standard protocol);
- ○
- Colorimetric or fluorescence tests can be performed on samples, and rapid results are obtained based on previous control measuring curves established for each type of bacteria (e.g., MTS/XTT, cresyl violet, fluorescein diacetate). The fluorescence techniques use more expensive reagents and readers, but their measurement is more reliable since turbidity of the sample generated by powder material dissolution does not affect the reading. Fluorescein diacetate is used in a standard method for the assessment of water contaminated with microorganisms and could be considered very reliable.
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- The scaffold would require an incubation in a given volume of nutrient media inoculated with a known number of CFU;
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- Antimicrobial activity of a 3D structure is very hard to investigate because not all the bacterial cells can be harvested, since some of them could be very strongly adhered inside the scaffold, and therefore hard to detach;
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- After the desired testing period, since the bacterial cells could be adhered inside the scaffold and cannot be reached, only a reading of a soluble coloured/fluorescent product of bacterial metabolism can provide insights. Some materials absorb coloured substances and make such tests impossible to carry out.
5. Future Perspectives: Co-Substituted Hydroxyapatite Bioceramics
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
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Elements | Source | Synthesis Method | Refs. |
---|---|---|---|
Bovine | Cortical bone | Pre-cleaning: (i) removal of soft tissue; (ii) cut into small pieces and boiled in water for 2 to 3 h; (iii) dry in an oven at 80 °C for 72 h; (iv) crush and subsequently grind by ball milling for 24 h. Heating: calcination in a furnace at temperatures in the range of 600–1100 °C, for 3 h, with heating and cooling rates of 5 °C min−1. | [93] |
Cortical bone | Pre-cleaning: (i) removal of soft tissue; (ii) crushing and milling process. Heating: sintering in a furnace at 1200 °C for 2 h or 4 h, with a heating and cooling rate of 5 °C min−1 and 10 °C min−1, respectively. | [92] | |
Teeth | Pre-cleaning: (i) removal of soft tissue; (ii) removal of remnant impurities by mechanical scraping; (iii) boiling in distilled water for 30 min; (iv) repeated the aforementioned steps three times; (v) drying in the sun for 3 days. Heating: (i) calcination in humid atmosphere at 735 °C for 1 h with a heating rate of 7 °C min−1; (ii) sintering at 1150 °C for 1 h with a heating rate of 7 °C min−1. | [108] | |
Pig | Cortical bone | Pre-cleaning: (i) hot water treatment; (ii) removal of organic compounds by scraping; (iii) de-proteinization in a boiled mixture of 1 M NaOH and 1 M HCl at 100 °C for 5–10 min; (iv) dried in an oven at 100 °C overnight; (v) crushing and grinding. Heating: calcination in air at 600 °C, 800 °C or 1000 °C at a heating rate of 5 °C min−1 followed by cooling to room temperature. | [99] |
Cortical bone | Pre-cleaning: (i) removal of soft tissues and fluids; (ii) boiling bone slices at 154 °C, 4 atm; (iii) drying in vacuum; (iv) milling; (v) removal of remnant fat and protein moieties by hydrothermal process. Heating: (i) calcination at 5 °C min−1 at 600 °C (allows the decomposition of organic tissue); (ii) sintering at 1000 °C (induces physico-chemical changes) from 1 to 50 h; (iii) cooling in the furnace in air. | [100] | |
Camel | Cortical bone | Pre-cleaning: (i) removal of organic compound; (ii) dry-heating at 100 °C for 1 h; (iii) cut in small pieces and immersion in acetone for 1 h. Heating: calcination at 1000 °C for 3 h at a heating rate of 10 °C min−1, and then slowly cooled down to room temperature. | [102] |
Sheep | Cortical bone | Pre-cleaning: (i) removal of femoral heads; (ii) de-proteinization with NaOH; (iii) washing and drying. Heating: (i) calcination at 850 °C for 4 h in air; (ii) crushing and milling. | [103] |
Dentine | Pre-cleaning: cleaning and washing the teeth. Heating: (i) calcination at 750 °C for 5–6 h; (ii) separation of dentine from enamel; (iii) ball grinding; (iv) sintering at 1000–1300 °C for 4 h. | [109] | |
Chicken | Egg-shells | Pre-cleaning and synthesis: (i) crushing egg-shells; (ii) simultaneous removal of organics and transformation of CaCO3 into CaO by calcination at 900 °C for 1 h; (iii) addition of water and phosphoric acid; (iv) precipitation overnight, followed by filtration and washing; (v) drying the HA product at 60 °C for 24 h. Heating: sintering in air (after sieving and pressing) at 900–1300 °C for 1 h, with a heating rate of 10 °C. | [110] |
Fish | Bones | Pre-cleaning: (i) removal of organic compounds by brushing and then boiling at 100 °C for 10 min; (ii) drying at 90 °C for 100 min and then crushing to powder; (iii) de-proteinization by reflux method using a 5% KOH solution. Heating: sintering at 600–1000 °C. | [111,112] |
Mussel | Shells | Pre-cleaning and synthesis: (i) mechanical cleaning and calcination in air at 1300 °C for 6 h (ii) Rathje fabrication method: mixing seashells powder with water and H3PO4 with magnetic stirring during the synthesis for 2 h at 700 rpm; (iii) filtering, followed by drying at room temperature for 168 h, and then at 100 °C for 24 h. Heating: sintering at 1200 °C for 10 h. | [57] |
Snail | Shells | Pre-cleaning and synthesis: (i) thoroughly cleaning of sand particles and other foreign materials; (ii) drying, crushing into small particles, ball-milling; (iii) sieving; (iv) mixing the as-obtained CaCO3 powder with water and H3PO4 solution, followed by continuous stirring at 80 °C for 8 h; (v) drying at 100 °C overnight in an incubator. Heating: calcination at 800 °C for 4 h in air. | [63] |
Cuttlefish | Whole | Pre-cleaning and synthesis: (i) cutting into small pieces; (ii) heat-treatment at 110, 500, 1000 °C with a heating rate of 5 °C min−1; (iii) mixing the as-obtained CaCO3 powder with an aqueous NH4H2PO4 solution to a Ca/P molar ratio of 1.67; (v) drying at 200 °C for 1–72 h, using heating and cooling rates of 5 °C min−1. | [60] |
Dolomic marble | Origin: Ruschiţa, Romania | Pre-cleaning and synthesis: (i) mechanical cleaning and calcination in air at 1300 °C for 6 h (ii) Rathje fabrication method: mixing seashells powder with water and H3PO4 with magnetic stirring during the synthesis for 2 h at 700 rpm; (iii) filtering, followed by drying at room temperature for 168 h, and then at 100 °C for 24 h. Heating: sintering at 1200 °C for 10 h. | [57] |
Red algae | Whole | Pre-cleaning: (i) rinsing at high-pressure; (ii) drying at room temperature for 24 h; (iii) sieving; (iv) thermal treatment to burn-off the organic material, at 650–700 °C for 12 h, with a low heating rate of 0.5 °C min−1 to prevent decomposition of algae; (v) alkalinisation with ammonium hydroxide at ambient pressure and 100 °C for 12 h under continuous stirring at speed of 100 rpm; (vi) filtration and neutralisation by repeating washing and drying overnight at 90 °C. Heating: thermal treatment at 60 °C, 105 °C, 450 °C, 550 °C and 1000 °C for 1 h each. | [113] |
Cation Dopant | Field of Application [Refs.] |
---|---|
Na | Sensors [162]; Catalysis [163] |
Sr | Catalysis [164] |
Ba | Water decontamination [165]; Catalysis [166] |
Al | Environment decontamination [167,168,169]; Catalysis [170] |
Sn | Radionuclides and heavy metals scavengers (decontamination) [171] |
Pb | Catalysis [172,173] |
Y | Electrochemical devices [174] |
Ti | Catalysis [175,176,177] |
V | Catalysis [178] |
Mn | Catalysis [179]; Optoelectronics [180] |
Fe | Sensors [181]; Catalysis [182,183] |
Co | Sensors [184] |
Ni | Catalysis [185,186,187,188] |
Pd | Catalysis [189,190] |
Pt | Catalysis [191,192] |
Cu | Catalysis [193,194,195,196]; Water decontamination [197] |
Ag | Catalysis [198,199,200] |
Au | Catalysis [194,201,202] |
Zn | Catalysis [203,204,205] |
Sm | Optoelectronics [206] |
Eu | Optoelectronics [206,207]; Environmental [208] |
Gd | Optoelectronics [206] |
Tb | Catalysis [209]; Optoelectronics [210] |
Dy | Optoelectronics [211] |
Cation (M) | Sample Form | Doping Range [M/(M + Ca)]∙100 (at.%) | Bio-Functionality/Effect of the Dopant | Refs. |
Li | Powder Scaffold Coating | 0.5–2 |
| [98,221,222,223,224] |
Na | Powder Coating | 5 |
| [227,229] |
K | Powder | 2.5–47 |
| [232,233] |
Mg | Powder Coating | 1–53 |
| [235,236,237,238,239,240,242,243] |
Sr | Powder Coating | 1–40 |
| [240,243,244,245,246,249,250,251,252,255,257] |
Ba | Powder | 0.5–2 |
| [261,262] |
Al | Powder | 0.5–2.5 |
| [263] |
Ga | Powder | n/a |
| [264,266] |
In | Powder | 1; 3 |
| [238,267] |
Bi | Powder | 5–25 |
| [267,268,269] |
Te | Powder | 0.04–0.22 |
| [272] |
Ag | Powder Scaffold Coating | 0.5–5 |
| [250,261,273,275,276,277,278,279,280,281,282,283,284,285,286] |
Zn | Powder Coating | 0.1–50 |
| [66,238,243,274,277,281,282,287,288,289,291,292,293,294,295,296,297,298] |
Cu | Powder Coating | 0.04–5 |
| [238,299,300,301,302,303] |
Mn | Powder Coating | 0.4–20 |
| [304,305,306,307,308,309] |
Fe | Powder | 1–50 |
| [308,309,310,311,312,313,314] |
Ti | Powder Coating | 1–13 |
| [68,177,301,316,317,318] |
Cr | Powder | 0.5–2.5 |
| [319,320] |
Co | Powder | 0.2–27 |
| [238,321,322,323] |
Ta | Powder | 0.13–0.27 |
| [324] |
Ni | Powder | 0.8–8.3 (theoretical)0.2–2.4(determined by ICP-OES) |
| [328,329] |
Mo | Powder | 0.05–5.2 |
| [330] |
Y | Powder Coating | 1.3–7 |
| [267,331,332,333] |
Cd | Powder | n/a |
| [334,335] |
W | Powder | 0.7–32.3 |
| [336] |
Hf | Powder | 0.5–15 |
| [339] |
La | Powder Coating | 2–30 |
| [314,340,342,379,380,405] |
Ce (3+) | Powder Coating | 4–20 |
| [344,346,377,382,383,384] |
Ce (4+) | Powder | 0.1–0.5 |
| [348,381,385] |
Sm | Powder Coating | 0.2–0.5 |
| [355,357] |
Eu | Powder | 0.1–20 |
| [361,362,363,364,365,366,388,389,390,391,392,393] |
Tb | Powder | 2–17 |
| [361,393,399] |
Gd | Powder | 1–17 |
| [128] |
Dy | Powder | 0.5–10 |
| [392,403] |
Nd | Powder | 1–17 |
| [128,352] |
Er | Powder | 2–10 |
| [372] |
U | Solution | 0.1–10 |
| [375] |
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Tite, T.; Popa, A.-C.; Balescu, L.M.; Bogdan, I.M.; Pasuk, I.; Ferreira, J.M.F.; Stan, G.E. Cationic Substitutions in Hydroxyapatite: Current Status of the Derived Biofunctional Effects and Their In Vitro Interrogation Methods. Materials 2018, 11, 2081. https://doi.org/10.3390/ma11112081
Tite T, Popa A-C, Balescu LM, Bogdan IM, Pasuk I, Ferreira JMF, Stan GE. Cationic Substitutions in Hydroxyapatite: Current Status of the Derived Biofunctional Effects and Their In Vitro Interrogation Methods. Materials. 2018; 11(11):2081. https://doi.org/10.3390/ma11112081
Chicago/Turabian StyleTite, Teddy, Adrian-Claudiu Popa, Liliana Marinela Balescu, Iuliana Maria Bogdan, Iuliana Pasuk, José M. F. Ferreira, and George E. Stan. 2018. "Cationic Substitutions in Hydroxyapatite: Current Status of the Derived Biofunctional Effects and Their In Vitro Interrogation Methods" Materials 11, no. 11: 2081. https://doi.org/10.3390/ma11112081
APA StyleTite, T., Popa, A.-C., Balescu, L. M., Bogdan, I. M., Pasuk, I., Ferreira, J. M. F., & Stan, G. E. (2018). Cationic Substitutions in Hydroxyapatite: Current Status of the Derived Biofunctional Effects and Their In Vitro Interrogation Methods. Materials, 11(11), 2081. https://doi.org/10.3390/ma11112081